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Financial Sponsors BASF Professional Turf & Ornamentals Dow AgroSciences LLC DuPont Professional Products Turf & Landscape and Consumer Group of Syngenta Crop Protection, Inc. Valent U.S.A.

Cover photo from Shutterstock Images LLC Reference in this publication to a trademark, proprietary product, or company name by personnel of the U.S. Department of Agriculture or anyone else is intended for explicit description only and does not imply approval or recommendation to the exclusion of others that may be suitable. Library of Congress Catalog Card Number: 2010916892 International Standard Book Number: 978-0-89054-392-4 Š 2011 by The American Phytopathological Society All rights reserved. No part of this book may be reproduced in any form, including photocopy, microfilm, information storage and retrieval system, computer database, or software, or by any means, including electronic or mechanical, without written permission from the publisher. Printed in the United States of America on acid-free paper The American Phytopathological Society 3340 Pilot Knob Road St. Paul, Minnesota 55121, U.S.A.

Dedication To Barbara, Eric, Dave, Becca, and Jackie

Acknowledgments Numerous individuals contributed to the completion of this book. I’ve benefited from participating in many discussions of fungicide issues with my turf pathology colleagues in academia and industry. We are, for the most part, a compatible group, and I enjoy the debate and their company. I am especially grateful for the counsel of Lee Burpee, one of the most widely published turf pathologists of our time, who has been a good friend and valuable colleague since our days in graduate school. At Purdue, I appreciate the comments and suggestions by Jin-Rong Xu, Fred Whitford, and Judy Santini. I also thank the undergraduate students who helped improve the illustrations and the graduate students who conducted important experiments that contributed to the science and practice of turf pathology. Outside academia, Glenda Cornstuble deserves special mention for smoothing the narrative’s rough edges and for helping me to relearn composition and grammar. I have such high regard for the remarkable group of turf professionals who comprise the Midwest Regional Turf Foundation. I appreciate their time and willingness to share thoughts about turf disease problems and solutions. Also, I would like to recognize Joe Gerst and Mark Gasvoda for setting great examples. The staff at APS PRESS made this an enjoyable and rewarding experience. Finally, I must thank Barbara for her patience and encouragement—and Eric, Dave, and Becca for providing a continuous source of inspiration.


Preface This book is intended for all individuals interested in the practice and science of maintaining healthy turf with chemicals. My objective was to create a comprehensive, current, and practical resource that addresses fungicides used specifically for disease control on golf course turf. I believe that with an understanding of how and why fungicides work (and why sometimes they don’t work), turf managers will use fungicides more effectively and efficiently and will be able to communicate disease control issues with greater confidence. My position at Purdue University has provided me with the opportunity to interact with the entire spectrum of people who worry about unhealthy turf. So, in writing this book, I tried to address topics and issues with the benefit of a variety of perspectives. As a teacher who regularly interacts with graduate and undergraduate students, I insist on a structured approach that emphasizes information based on critical research rather than on testimonials and anecdotal information. Students who enroll in my class arrive with very limited knowledge of fungicides, and most of their information is inaccurate or only partially true. I encourage them to understand the research that forms the foundation for the practices applied on the golf course. I think that if students understand the principles of fungicide action, they can apply sound reasoning to resolve problems encountered in the real world. As an advisor to golf course superintendents here in the Midwest, I have learned about the important practical concerns they encounter. They are largely an educated and experienced group who ask challenging questions and often influence the direction of my field research program. They help me maintain focus on real issues. In fact, this book evolved from a series of workshops and seminars conducted to address their concerns. Finally, as a member of the same golf club for many years and a veteran of hundreds of weekends of golf, I have learned what gets the membership’s attention from a turf quality standpoint. During my tenure at the club, I have gained an appreciation of the constraints associated with expectations (reasonable or not) of the golfing public. I have benefited greatly from observing the superintendent–member relationship, and I think it has helped me apply a practical perspective to managing turf diseases with chemicals.


Contents Chapter 1

Turf Fungicide Fundamentals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1

Chapter 2

Modes of Action of Fungicides . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 27

Chapter 3

Fungicide Resistance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 49

Chapter 4

Factors That Influence Fungicide Performance . . . . . . . . . . . . . . . . . . 79

Chapter 5

Biofungicides, Phosphonates, and Post-Patent Products . . . . . . . . 107

Chapter 6

Fungicide Interactions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 123

Chapter 7

Scheduling Fungicides for Turf Disease Control . . . . . . . . . . . . . . . . . 137

Chapter 8

Fungicide Regulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 157

Chapter 9

Interpreting Fungicide Performance Research . . . . . . . . . . . . . . . . . . 169

Chapter 10

Turf Disease Characteristics and Control . . . . . . . . . . . . . . . . . . . . . . . 181

Chapter 11

Turf Fungicide Profiles . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 229

Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 261


A Brief History General Use and Safety of Fungicides Fungicide Nomenclature Characterizing Fungicides According to Mode of Action and Application Strategy Characterizing Fungicides According to Phytomobility Fungicide Formulations

Turf Fungicide Fundamentals



A Brief History Mankind’s long history with fungicides is related to limiting the destructive effects of plant diseases. As civilization advanced and humans relied increasingly on cultivated species for food, the consequences of plant diseases became more pronounced and preventing crop failures was an issue of survival. The ancients had no idea why their wheat was shriveled with rust, but they recognized that burning sulfur near their fields reduced rust severity and resulted in more harvested grain. More than a thousand years later, even the most advanced agronomists remained unaware of the infectious nature of plant diseases. In eighteenth-­century France, agriculturalists did not understand that wheat bunt, a fungal disease that turns grain into a sooty dust, resulted from planting contaminated seeds, but they were willing to try anything to save their grain from ruin. Spells and rituals were unsuccessful, but by pure coincidence they observed that wheat bunt was less severe if seeds were soaked in copper sulfate suspensions prior to planting. This spurred activity in soaking seeds in a variety of foul and exotic treatments (such as urine), but most failed because the concept of plant infection by fungi and bacteria was not understood. During the following century, enlightened scientists discovered that living microorganisms were the causes of maladies in plants and animals rather than the results. In the mid 1850s, Anton de Bary concluded that several crop diseases, including rusts, mildews, and potato late blight, were caused by fungal parasites. Ten years later, Louis Pasteur debunked the myth of spontaneous generation. In the late 1870s, Robert Koch proved that pathogenic bacteria caused disease in livestock, and he is credited with establishing the germ theory of infectious disease. Understanding the parasitic nature of plant, animal, and human diseases led to a more informed approach to preventing or limiting damage caused by various pathogens. Despite revelations about the nature of disease, the first fungicide deliberately applied to prevent the effects of fungal infection in plants was discovered


2  Chapter 1

Initial attempts to control turf disease with fungicides in the United States were conducted at the Arlington Turf Gardens near Washington, DC, around 1917.

by chance. In the early 1880s, grapevines growing along roadsides in the Bordeaux region of France were treated with copper sulfate, a compound that left an unappealing blue residue on the grapes and discouraged pilfering by passersby. Scientists observed that copper-­treated vines were hardly affected by downy mildew, a fungal disease that blighted leaves and devastated grape yields. They reasoned that if the copper-­treated vines were healthy and the untreated vines were ravaged by disease, there must be something in the copper that might help them prevent crop damage and spoilage caused by the mildew fungus. Thus began the formal search for antifungal compounds leading to the development of Bordeaux mixture, a preparation of copper sulfate and lime that was subsequently applied to vineyards to control grape downy mildew. With the understanding that microscopic fungi were responsible for crop failures and that copper mixtures could protect plants from infection, other agricultural uses for Bordeaux mixture were launched. Ultimately, Bordeaux mixture was applied to potatoes across Europe to prevent epidemics of late blight, the disease responsible for the Irish Potato Famine some 35 years earlier. Late blight still occurs, and fungicides play an important role in its management. A timeline tracking the introduction of fungicides on turf is presented in Figure 1.1. Initial attempts to control turf disease with fungicides in the United States were conducted at the Arlington Turf Gardens near Washington, DC, around 1917. The turf gardens were operated by the United States Department of Agriculture, but research funding was provided largely by the Green Section of the United States Golf Association. The objective of initial trials was to determine the efficacy of Bordeaux mixture against brown patch of fescue. Although disease progress was checked, the mixture was quite toxic to turf when applied at effective rates. However, disease-­ control benefits apparently outweighed the phytotoxic effects, because by 1919, Bordeaux mixture was used regularly to control brown patch on other turf species, including creeping bentgrass. Early Bordeaux preparations were homemade mixtures with considerable safety risks for turf as well as for the people applying them. Modern Bordeaux fungicides are no longer used against turf diseases, but they are produced by several manufacturers and remain important tools in limiting disease damage to certain crops raised according to organic specifications. Mercury-­ based compounds were introduced into agriculture as seed treatments to limit the effects of wheat bunt as well as seedling-­and root-­ infecting pathogens at the beginning of the twentieth century. Soon after, similar chemicals were tested against a growing list of fungal diseases on turf, including snow molds, dollar spot, and brown patch. When applied to turf at appropriate rates, organomercury compounds provided good disease control without the levels of phytotoxicity attributed to Bordeaux mixture. By the mid 1920s, Semesan, a chlorophenyl mercury compound, was developed for dollar spot and brown patch control. Research and development efforts also resulted in the discovery and production of Calo-­clor, another mercury-­based product that was effective against a variety of diseases for nearly 50 years. Unlike the homemade Bordeaux preparations, Semesan and Calo-­clor were produced commercially with prescribed application rates for more consistent performance with reduced risk of phytotoxicity.

Turf Fungicide Fundamentals  3

Fig. 1.1. Timeline of active ingredient introductions on turf.

4  Chapter 1

Fungicide performance improved as formulations evolved from dusts to granular materials, wettable powders, flowables, and dry flowables.

Through the 1920s, antifungal compounds were limited to inorganic preparations with elemental toxic ingredients such as sulfur, copper, mercury, and, in some cases, arsenic. A significant breakthrough occurred in the 1930s with the discovery of thiram, a dithiocarbamate fungicide with activity against a broad spectrum of plant diseases. Thiram was combined with Semesan to produce Tersan OM, an effective, long-­lasting product that controlled a variety of turf diseases. Currently, the thiram active ingredient remains registered for turf, although the product is used infrequently because other fungicides are more effective. Calo-­clor and Tersan OM registrations were revoked in 1970 because mercury-­based pesticides were banned by the U.S. Environmental Protection Agency (EPA). Several new formulations and numerous compounds were introduced from 1940 to the mid 1960s as the manufacture of agricultural chemicals evolved into a bona fide industry. Fungicides were initially developed to control diseases in high-­value fruit and vegetable crops, but some were also used against turf diseases. Products introduced into turf markets were targeted toward specific diseases: cadmium succinate and phenyl mercury acetate (PMA) for dollar spot, chloroneb and etridiazole for Pythium blight, quintozene (PCNB) for snow molds, and anilazine for Helminthosporium leaf spot. Cyclohexamide, a fungal antibiotic for dollar spot and brown patch control, also was introduced during this period. Several of these fungicides are still available for turf disease control, but their uses are limited compared with those of modern fungicides with greater efficacy, lower application rates, and often activity against a broader spectrum of turf pathogens. Mancozeb and chlorothalonil were introduced in the 1960s and remain two of the most important fungicides on crops and turf. Mancozeb has limited use on turf, but it is the most widely used fungicide on fruits and vegetables worldwide. Chlorothalonil remains an essential component of effective turf fungicide application programs throughout the United States. Remarkable advances in fungicide-­application technology accompanied growth of the manufacturing industry, resulting in improved fungicide efficacy and application precision. Fungicide performance improved as formulations evolved from dusts to granular materials, wettable powders, flowables, and dry flowables. Sprayers and nozzles were engineered to optimize delivery for specific types of pesticides and formulations. New antifungal compounds and advances in application technology significantly improved the capacity to limit the effects of infectious disease and provide high-­quality playing surfaces. At about the same time that McCallan (1967) summarized three eras in fungicide history—the era of sulfur (ancient times to 1885), the era of copper (1885–1935), and the era of synthetic organic contact compounds (1935– 1967)—a fourth era was beginning with the introduction of benomyl, a fungicide capable of penetrating plant surfaces and limiting existing infections. Fungicide active ingredients predating benomyl are considered nonselective general cell toxicants. They poison living cells by disrupting numerous metabolic functions and are just as likely to kill plant cells as fungal cells if they can penetrate leaf surfaces. However, precisely because they are nonselective, fungicides that do not penetrate plant surfaces are active against a

Turf Fungicide Fundamentals  5

broad range of fungi and are very effective as plant protectants. Their utility in terms of turf recovery and duration of control is limited because they are unable to suppress existing plant infections. The newest generation of fungicide compounds includes active ingredients with highly specific modes of action, often interfering with only a single metabolic function in the target pathogen. They safely penetrate plant tissues and stop growth of the pathogen inside the plant. The modern period of fungicide history is defined by the discovery and development of chemotherapeutic active ingredients. The fourth era of fungicide history also witnessed growth and modernization of the agrichemical industry along with expansion of government regulation with regard to pesticides. Safety concerns led to the cancellation of heavy-­metal-­based products, resulting in the loss of cadmium and mercury compounds that were highly effective against turf diseases. Increased awareness about human health risks resulted in the loss of anilazine and cyclohexamide. Environmental stewardship concerns fueled the demand for products with lower application rates to lessen the environmental impact of pesticides. Manufacturers intensified research and development efforts to deliver a remarkable array of new compounds with greater efficacy and safety and with reduced environmental impact. New knowledge about the nature of active ingredients and the modes of action of fungicides often made the search for active compounds more efficient. Fungicides were classified into groups based on modes of action. Once a particularly effective class was identified (e.g., demethylation inhibitors, also called DMIs), competing manufacturers raced to deliver different active ingredients within that class. Important classes of fungicides used for turf disease control include the DMIs, the dicarboximides, and QoI fungicides (strobilurins). A significant consequence of the development and use of fungicides with highly specific modes of action is the rise of fungicide resistance in pathogen populations. Simple genetic changes in individual fungal cells can render the fungicide ineffective, and repeated use of the fungicide promotes the increase of resistant strains to the point that they predominate in a population, thwarting attempts to control disease. University and industry scientists spend considerable effort and resources studying fungicide resistance. Representatives from basic fungicide manufacturers assembled to create the Fungicide Resistance Action Committee (FRAC) in 1980. Their objectives are to anticipate resistance issues with new compounds and to offer strategies and guidelines for dealing with resistance. The list of fungicides introduced in the modern generation includes most of the products currently in use for turf disease control. The benomyl (Tersan 1991) registration was voluntarily withdrawn in 1992 and it is no longer available, but thiophanate-­methyl, a close relative, is still useful against many turf diseases. Introduction of the benzimidazole class was followed in rapid succession by dicarboximide fungicides (iprodione and vinclozolin) and several DMI fungicides (triadimefon, fenarimol, and propiconazole). These are fairly broad-­spectrum compounds, and because they suppress existing infections, their duration of control is greater than that of conventional nonpenetrating fungicides. After the loss of heavy metal compounds and the evolution of benzimidazole-­resistant strains of

A significant consequence of the development and use of fungicides with highly specific modes of action is the rise of fungicide resistance in pathogen populations.

6  Chapter 1 the dollar spot pathogen, Sclerotinia homoeocarpa, DMI fungicides afforded superintendents the capacity to maintain healthy fairways without repeating applications at 1-­to 2-­week intervals. Active ingredients that specifically targeted oomycete pathogens (Pythium and Phytophthora species) were introduced soon after. Metalaxyl and propamocarb were among the first such compounds that provided excellent control of Pythium blight on turf. Fosetyl aluminum, the first truly systemic fungicide (it moves upward and downward in plants), was registered for use against Pythium blight and Pythium root dysfunction. More recent fungicides specific to oomycete pathogens on turf include cyazofamid and fluopicolide. The QoI class of fungicides (often referred to as strobilurins) was introduced in the 1990s. They are unique compounds in that they are derived from naturally occurring, wood-­rotting mushrooms found in forests. These mushrooms produce antifungal compounds to reduce the competition for their own organic substrate. QoI fungicides are among the first to be classified as “reduced risk” pesticides by the EPA, meaning that compared with other pesticides, their inherent risk to human health and the environment is low. Azoxystrobin was the initial introduction into turf markets and was followed by other QoI fungicides including trifloxystrobin, pyraclostrobin, and fluoxastrobin. QoI fungicides are very effective against a broad range of turf pathogens, especially Rhizoctonia species, but are not effective against the dollar spot pathogen. Boscalid, a new material with a novel mode of action, was registered for use on turf in 2004 and is specific for controlling dollar spot. With restrictions imposed on chlorothalonil and resistance issues associated with benzimidazoles, dicarboximides, and DMI fungicides, boscalid provides superintendents with another option for controlling one of the most important diseases on fine turf. Trends for future development will be influenced largely by the cost (measured in hundreds of millions of dollars) to bring a new active ingredient to market. Such an investment can be managed only by companies with great resources in terms of research and development scientists and facilities. Costs have forced a reduction in the number of basic manufacturers from more than 30 to around a dozen through two decades of mergers and acquisitions. Increased regulatory pressures and market competition from post-­patent (“generic”) formulators reduce profit potentials on new compounds, slowing the pace of discovery and development. Because there are more nontarget effects associated with multi-­site compounds, basic manufacturers tend to focus on site-­specific penetrant fungicides. Although the registration process usually avoids certain obstacles from a regulatory perspective, the risk of fungicide resistance may further discourage the advance of promising site-­specific active ingredients beyond the discovery phase. Growing emphasis is being placed on improving formulations and combining existing active ingredients in premixture products tailored for specific markets. For example, Tartan combines DMI and QoI fungicides to address a broad spectrum of turf diseases. Headway, Concert, and Cleary 26/36 also are combinations of existing registered compounds. Efforts to integrate fungicides with traditional disease-­control practices and new unconventional control options will escalate in the future. Biopesticides, plant-­defense activators, and stress-­reducing compounds have the potential

Turf Fungicide Fundamentals  7

to lessen the effects of fungal infection and boost fungicide performance without the risk of fungicide resistance.

General Use and Safety of Fungicides Fungicides are pesticides engineered to prevent or mitigate damage caused by fungal pathogens. In the United States, the EPA regulates all pesticides, including fungicides, to ensure personal and environmental safety associated with their use. In order to reduce human health and environmental safety risks, the EPA requires volumes of toxicological and ecological data before a pesticide registration is granted. The data provide an interesting perspective on comparing risks associated with different active ingredients. For example, compared with other pesticides, fungicides have a relatively low level of toxicity. The risk of acute poisoning by fungicides is much lower than that of almost all insecticides and many substances found in our foods and medicines (Table 1.1). Consequences of chronic exposure to pesticides are not nearly as well defined as acute toxicity effects. Estimating the potential for chronic effects involves many factors, such as the amount of active ingredient contained in a product, the application methods and rates used, and frequency and degree of exposure to the pesticide over time. The EPA provides cancer-­risk classifications for all pesticides by extrapolating data from laboratory and animal studies. The study of long-­term, chronic effects is a continual process that evolves with improvements in technology for detecting and monitoring human health effects. The EPA registers pesticides only if they can be used without posing unreasonable risk to humans or the environment when used according to labeled instructions. However, like all pesticides, fungicides must be handled with utmost care and only according to specific instructions on product labels. Most of the same fungicides used to control turf diseases are applied to fruit, vegetable, and grain crops. In fact, much of the fungicide used in the United States is applied to protect food crops including vegetables, orchard crops, grapes, nuts, and grains. In the Midwest alone, chlorothalonil (the active ingredient in Daconil) is applied weekly to thousands of acres of

Table 1.1. Median lethal dose 50% (LD50), a measure of acute toxicitya Selected substance

Aldicarb (nematicide/insecticide) Nicotine (insecticide)

1 50



Imidacloprid (insecticide; e.g., Merit)




Chlorothalonil (fungicide; e.g., Daconil) Triadimefon (fungicide; e.g., Bayleton) a

Oral LD50 (mg/kg of body weight)

Adapted from Schumann and D’Arcy, 2009.

3,800 10,000

8  Chapter 1 tomatoes over a 3-­month growing period; DMI fungicides (similar to Banner, Bayleton, and Eagle) are part of comprehensive disease-­management programs for apple orchards; and QoI fungicides (with the same active ingredients as Compass, Disarm, Heritage, and Insignia) are applied to millions of acres of corn and soybeans. The point is that as important as these fungicides are for maintaining high-­quality amenity turf, they are absolutely essential for the production of fruits, vegetables, and grains that comprise a healthy diet. Fungicides used on turf also have a comparatively low environmental impact, primarily because grass plants have dense root systems and a highly organic thatch layer that fosters intense microbial activity. Most fungicides washed from leaves bind to the organic matter, where they ultimately are degraded by a vast array of microorganisms that inhabit the thatch. Furthermore, current trends in fungicide development are toward more-­specific fungicides designed to all but eliminate their nontarget effects. The point is that the use of fungicides on turf contributes very little to the volume of fungicides applied worldwide. The public at large (including the golfing public) has a superficial understanding of pesticides and tends to identify them all in very negative terms with apprehension and anxiety. Most recognize that different products address different pest issues, but when it comes to safety and the environment, they perceive them as the same. In fact, there are enormous differences among pesticides with regard to their chemical characteristics and health and environmental effects. Fungicides tend to be the least toxic and have less of an environmental impact than other groups of pesticides, such as herbicides, insecticides, or nematicides. Furthermore, fungicides used on turf should not be considered more dangerous because they are applied to grass, since the very same products are registered for use on almost all of our fruits and vegetables. Superintendents should be able to communicate the facts to patrons and at least be prepared to point them in the right direction for objective information on the topic.

Fungicide Nomenclature All fungicides have three names, and they all appear on the fungicide label. The chemical name is assigned by an internationally sanctioned authority whose function is to determine the appropriate nomenclature for all chemical compounds, including pesticides. Chemical names have little practical value but are very important because they provide universally recognized names for the active ingredients. Common names also are assigned by committee and, in most cases, represent internationally recognized standards. Compared with chemical names, common names are much less complex and simplify the chemical name of the active ingredient to something that is much more useful. Finally, the trade name is assigned by the fungicide manufacturer. It appears most prominently on the label and is the name used to market the product. Chemical, common, and trade names of three fungicides are shown in Box 1.1. Different fungicide products may have the same common name or active ingredient. For example, chlorothalonil is the active ingredient in several fungicide products (Box 1.2). In such cases, legal patent

Turf Fungicide Fundamentals  9

Box 1.1. Examples of chemical, common, and trade names Chemical Name

Common Name

Trade Name



Daconil Ultrex

dimethyl 4,4-ophenylenebis- (3-thioallophanate)


Cleary 3336

N-3-(1-methylethoxy) phenyl-2-(trifluoromethyl) benzamide



Box 1.2. Different products may contain the same active ingredient. Trade Name

Common Name (active ingredient)

Daconil Ultrex Echo 720 Manicure Concorde Chlorostar


protection for the registered active ingredient has expired, and basic manufacturers (those holding the patents) no longer have exclusive rights to manufacture fungicide products with that active ingredient. Companies that specialize in formulating products acquire the off-­patent (generic) compound and produce their own products with different trade names. This is similar to pharmaceuticals developed for human health, for which generics become available when patents expire. Not all fungicides with expired patents are exploited by formulation companies. However, the list is growing, starting with some of the most effective and successful products such as chlorothalonil, propiconazole, and mefenoxam.

Characterizing Fungicides According to Mode of Action and Application Strategy “Mode of action” refers to how an active ingredient interferes with fungal growth. For some fungicides, modes of action have been described down to the smallest details. For others, explanations are vague. Regardless of the extent of our knowledge of modes of action, fungicides may be sorted into two broad groups related to their modes of action. The terms “multi-­site” and “site-­specific” refer to only one aspect of mode of action and describe only the general nature of the inhibitor or active ingredient. Turf fungicides are classified as multi-­site and site-­specific in Table 1.2. Multi-­site compounds disrupt many different metabolic processes in fungal cells and are effective on plant surfaces. Site-­specific active ingredients interfere with particular biochemical reactions in sensitive fungi. Different types of site-­specific fungicides attack different biochemical targets (described in Chapter 2). The practical significance of understanding the difference between these two groups lies in their

10  Chapter 1 application strategies to control disease and manage the threat of fungicide-­ resistant pathogen populations. Details are discussed in subsequent chapters, but in general the risk of resistance is of great concern with site-­specific fungicides but not with multi-­site fungicides. Also, because modern site-­specific compounds affect fungal growth inside the plant, they offer more flexibility in formulating disease-­control strategies. Site-­specific compounds may be applied as curative treatments, to suppress growth of existing infections after disease is apparent, or as preventive or protective treatments in anticipation of a disease threat. In order to be effective, multi-­site compounds must be applied in preventive or protective approaches because they work only on plant surfaces and cannot affect existing infections. The terms “preventive” and “curative” can be confusing because labels of some multi-­site compounds describe a curative application rate. Curative rates are simply very high application rates and are suggested as remedial treatments in response to disease outbreaks. High application rates of multi-­site fungicides may be

Table 1.2. Active ingredients (and trade names) of multi-site and site-specific fungicides registered for use on turf Multi-site

chlorothalonil (Daconil) mancozeb (Fore) thiram (Spotrete)


azoxystrobin (Heritage) boscalid (Emerald) chloroneb (Terrachlor) cyazofamid (Segway) etridiazole (Terrazole) fenarimol (Rubigan) fludioxonil (Medallion) fluopicolide (Stellar) fluoxastrobin (Disarm) flutolanil (Prostar) fosetyl aluminum (Signature) iprodione (Chico 26GT) mefenoxam (Subdue Maxx) metconazole (Tourney) myclobutanil (Eagle) PCNB (Turfcide) phosphonic acids (phosphite fungicides) polyoxin D (Endorse, Affirm) propamocarb (Banol) propiconazole (Banner Maxx) pyraclostrobin (Insignia) tebuconazole (Torque) thiophanate-methyl (Cleary 3336) triadimefon (Bayleton) trifloxystrobin (Compass) triticonazole (Trinity, Triton) vinclozolin (Curalan)

Turf Fungicide Fundamentals  11

more effective in reducing disease spread to healthy plants, but they do not affect existing infections. In describing fungicide-­application tactics, terms such as “postoutbreak” and “preoutbreak” are more accurate than “preventive” and “curative” and ultimately less confusing.

Characterizing Fungicides According to Phytomobility Fungicides are often categorized according to their ability (or inability) to penetrate and move within plants. Couch (1995) referred to this attribute as a fungicide’s topical mode of action in an effort to characterize the location, inside or outside the plant, where fungicide activity takes place. This term is misleading because it has little to do with how active ingredients affect fungi (modes of action). Rather, it describes the fungicide’s relationship with the turf plant, specifically whether it remains on plant surfaces or is absorbed and transported in plant tissues. The term “phytomobility” is used in this text to avoid confusing uptake and transport of fungicides in plants with their biochemical modes of action in fungi. In terms of phytomobility, fungicides may be broadly classified as contacts or penetrants. Depending on the nature of their mobility within plant tissues, penetrant fungicides are further sorted into three groups: local penetrants, acropetal penetrants, and systemic penetrants, as discussed below. The term “systemic” was initially coined as an attribute of benomyl, the first fungicide that could penetrate leaf surfaces and move within plant tissues. The term distinguished benomyl from existing nonphytomobile contact fungicides that remained as deposits on plant surfaces. Many of the fungicides introduced after benomyl differed with respect to how they move within plants and the extent of their mobility; therefore, it is appropriate to revise the terminology used to describe fungicide movement in plants (Box 1.3).

Box 1.3. Modern terminology for contact and penetrant fungicides Contact

Contact fungicides remain on plant surfaces. The only movement is redistribution that may occur with precipitation, irrigation, and dew.


Penetrant fungicides are absorbed into plant tissues. Their capacity to move within plants falls into three categories.

Acropetal penetrant

Acropetal penetrants move between cells along a water potential (pressure) gradient. They are xylem mobile and are translocated upward toward leaf tips and margins.

Local penetrant

Local penetrants diffuse into the waxy cuticle. Most of the active ingredient remains there because local penetrant fungicides have a chemical attraction to the wax compounds. Some active ingredient moves through the cuticle between cells toward the cuticle on the opposite side of the leaf.

Systemic penetrant

Systemic penetrants move through cells with live protoplasts and follow a sugardensity gradient from areas of high concentration (expanded leaves) to areas of low concentration (roots and newly emerging leaves).

12  Chapter 1 Contact Fungicides Contact fungicides are immobile and affect only fungi present on plant surfaces (Fig. 1.2). They have no impact on the extent of colonization of plant tissues after infection has occurred. Contact fungicides are formulated with a certain chemical tenacity that enables them to remain attached to leaf and stem surfaces. Deposits may be redistributed with rain, dew, or irrigation water. If precipitation or irrigation occurs before deposits are thoroughly dried, some fungicide may be washed from leaf surfaces. Contact fungicides are the least soluble of all fungicide products. They bind firmly to high-­ organic-­matter thatch surfaces and therefore have no activity against root diseases. Their efficacy also is limited by regular mowing and removal of clippings, which effectively remove fungicide from the treated area. Contact fungicides are most effective when applied prior to infection by mycelium or germinating spores. When applied after an initial outbreak, contact fungicides limit disease spread to healthy plants, but they cannot influence disease progress inside already infected tissues. Because normal maintenance practices remove contact fungicides from golf turf—and because they cannot affect existing infections—contact fungicides provide relatively brief periods of protection, often requiring reapplication at 7-­to 14-­day intervals. Since contact fungicides have very limited movement beyond the site of the initial dried deposit, coverage plays an important role in fungicide performance. In general, more complete coverage (more deposits per unit area) is required for contact fungicides to achieve satisfactory results. Most widely used contact fungicides have active ingredients with multi-­ site modes of action. They interfere with numerous metabolic functions in living cells, explaining why such active ingredients are formulated to remain

Fig. 1.2. Contact fungicides remain and are active only on plant surfaces.

Turf Fungicide Fundamentals  13

outside plant cells. That is, if these materials did penetrate plant tissue, they would be toxic to the plant. Multi-­site inhibitors are not prone to the development of fungicide-­resistant pathogen populations, making contact fungicides essential components of strategies for avoiding or delaying resistance to modern fungicides with site-­specific active ingredients. Chlorothalonil is the most important and effective contact fungicide registered for use on turf. Mancozeb is less important on turf, but it may be used as part of a resistance-­ management program for some diseases. PCNB, an important compound for snow mold control, is regarded as a contact fungicide, although it reportedly has weak chemotherapeutic abilities. Penetrant Fungicides Penetrant fungicides applied to plant surfaces are absorbed into underlying tissues. In order to be effective, these active ingredients must cross the plant’s protective barriers in concentrations that are toxic to fungi without adversely affecting plant cells. Penetrant fungicides diffuse through the cuticle and enter plant tissues from areas of high concentration to those of low concentration. When equilibrium is reached between the external and internal fungicide concentrations around the deposit site, the rate of diffusion slows to a stop, and no more fungicide can enter the plant until the equilibrium again becomes unbalanced. Only a percentage of fungicide applied to plant surfaces is actually absorbed. Published research in this area is scarce and involves crop plants only, but available results suggest that, depending on the compound and environmental factors, 5–50% of the active ingredient is absorbed into plant tissues. The rate of absorption of azoxystrobin into wheat leaves is shown in Figure 1.3. Nearly 20% was absorbed in the first 24 hours, and after 8 days,

Fig. 1.3. Rate of azoxystrobin absorption in wheat. (Adapted from Godwin et al., 1999)

14  Chapter 1 45% of the applied active ingredient was detected in leaves. Active ingredients differ in the rate of uptake (especially in the first 24–48 hours) and the subsequent distribution in plants; however, most of the absorbed fungicide remains in the vicinity of the deposit. Since plants begin metabolizing foreign substances as they diffuse through the cuticle, the most effective fungicides are absorbed rapidly and remain intact for more than a few days. Some of the active ingredient that is not absorbed remains with the surface deposit where it may be effective (albeit briefly) against fungi on plant surfaces. Because they are more soluble and less tenacious than contact fungicides, most penetrants are more readily washed from leaves into thatch and perhaps the top fraction of soil where they may be absorbed by roots. Penetrant fungicides differ with regard to their solubility. Fungicides with greater solubility tend to be more effective against root pathogens. Almost all modern fungicides used for turf disease control are penetrants. However, there are important differences among penetrant fungicides involving their movement after getting through the plant’s outer barriers. Once active ingredients diffuse into the cuticle, compounds either move directly through cells with living protoplasts via pores in cell walls (symplastic transport) or they move around cells, between cell walls, and through

Fig. 1.4. Penetrant fungicides are capable of symplastic transport (A) or apoplastic transport (B).

Turf Fungicide Fundamentals  15

intercellular spaces and cells that do not contain living protoplasts (apoplastic transport) (Fig. 1.4). Only phosphonic acids move symplastically, while all other penetrants move in an apoplastic fashion (Table 1.3). Fungicides capable of apoplastic transport are further divided into those that are xylem mobile (acrope­tal penetrants) and those with limited migration across leaf tissues (local penetrants). In most cases, fungicides within a given class share a common phytomobility, such as local penetrant dicarboximides and xylem mobile DMIs. The notable exception is the QoI fungicide class, which includes both acropetal and local penetrants. The disease control advantage provided by penetrant fungicides lies in their ability to restrict the growth of pathogenic fungi inside the plant; i.e., they are chemotherapeutic. As long as fungitoxic concentrations persist in

Table 1.3. Phytomobility of active ingredients in turf fungicides Fungicide

Phytomobility classification

Movement throughout the plant

… … … … … …

Movement among cells

chlorothalonil mancozeb thiram PCNB chloroneb etridiazole

Contact Contact Contact Contact Contact Contact

… … … … … …

iprodione vinclozolin trifloxystrobin pyraclostrobin cyazofamid fludioxonil polyoxin D

Local penetrant Local penetrant Local penetrant Local penetrant Local penetrant Local penetrant Local penetrant

Translaminar Translaminar Translaminar Translaminar Translaminar Translaminar Translaminar

Uncertain Uncertain Apoplastic Apoplastic Apoplastic Apoplastic Apoplastic

azoxystrobin fluoxastrobin fenarimol metconazole myclobutanil propiconazole tebuconazole triadimefon triticonazole flutolanil boscalid mefenoxam thiophanate-methyl propamocarb fluopicolide

Acropetal penetrant Acropetal penetrant Acropetal penetrant Acropetal penetrant Acropetal penetrant Acropetal penetrant Acropetal penetrant Acropetal penetrant Acropetal penetrant Acropetal penetrant Acropetal penetrant Acropetal penetrant Acropetal penetrant Acropetal penetrant Acropetal penetrant

Xylem mobile Xylem mobile Xylem mobile Xylem mobile Xylem mobile Xylem mobile Xylem mobile Xylem mobile Xylem mobile Xylem mobile Xylem mobile Xylem mobile Xylem mobile Xylem mobile Xylem mobile

Apoplastic Apoplastic Apoplastic Apoplastic Apoplastic Apoplastic Apoplastic Apoplastic Apoplastic Apoplastic Apoplastic Apoplastic Apoplastic Apoplastic Apoplastic

fosetyl aluminum phosphonic acids

Systemic penetrant Systemic penetrant

Ambimobile Ambimobile

Symplastic Symplastic

16  Chapter 1 plant tissues, penetrant fungicides protect against new infections and suppress the development of existing infections. The result of this dual action is a considerable interruption of disease progress, extending the period of disease suppression, mitigating the effects of infection, and allowing damaged turf to regrow and recover. A disadvantage of penetrant fungicides is that, with rare exception, the active ingredients are site-­specific inhibitors. Hence, they are at risk for the development of fungicide-­resistant pathogen populations. Acropetal penetrants. Most modern fungicides are classified as acropetal penetrants. “Acropetal” is a botanical term that describes movement from the base toward the apex or tip. Acropetal penetrant fungicides therefore move upward in the plant after diffusing through the cuticle. Movement, or translocation, of fungicide occurs through the xylem, the water-­conducting tissues of plants. Before an active ingredient enters the xylem, it migrates past several layers of cells. By nature of their chemical structures, acropetal penetrant fungicides cannot pass through cells with living protoplasts. Instead, they are capable only of apoplastic transport, moving around individual cells, between cell walls, and through intercellular spaces. Eventually they filter into xylem cells, which are porous and do not contain living protoplasts (Fig. 1.5). Once in the xylem, active ingredients are subject to the same forces that move water through plants. Water potential determines the speed and direction of water movement through xylem. Water potential is greatest in soils

Fig. 1.5. Acropetal penetrant fungicides diffuse through the cuticle, move around and between plant cells, and enter the xylem, where they are transported upward to leaf tips and margins.

Turf Fungicide Fundamentals  17

with ample moisture and lowest in dry air. Different plant tissues vary with regard to water potential. Water, minerals, and other substances, including fungicides, that enter xylem cells always move down a gradient from high water potential to low water potential (Fig. 1.6). Therefore, although fungicide moves down the gradient, it moves up through the plant, acropetally, from the base to the leaf tips. Acropetal penetrant fungicides tend to accumulate at sites of high transpiration (leaf tips and margins), where water and oxygen are released into the atmosphere. In a discussion of fungicide movement in plants, it is worth noting from Figure 1.6 that water potential is greater in emerging leaves than in fully expanded leaves. The practical significance is that since active ingredients can move only down the gradient, they tend not to move toward new growth, perhaps increasing infection risk for newly emerging leaves. Also, they cannot be transported downward to roots. However, acropetal penetrant fungicides in soil and thatch may be absorbed by roots and translocated up through the plant, following the water potential gradient. (Published research concerning the delivery and mobility of fungicides in soil and thatch is scarce and dated at best.) Finally, terminal xylem cells in leaf tissues are similar to tiny capillaries in the human circulatory system. Therefore, all leaf cells are in close proximity to xylem, explaining how fungicides can be effectively distributed throughout leaf tissues. Extent of mobility varies with individual compounds and other factors, including age of plant tissues, ambient temperature, and moisture. Research on xylem-­mobile strobilurin fungicides estimates that only 8–20% of active ingredient entering the plant actually moves beyond the point of uptake after 8 days. The greatest fungicidal effect remains beneath the deposit; therefore, good application coverage helps optimize fungicide performance. There is some evidence that acropetal penetrant fungicides passively enter phloem cells, but because they are incompatible with the intracellular environment,

Fig. 1.6. Acropetal penetrant fungicides move down a water potential gradient. Water moves down a gradient from a site of high water potential to a site of lower (more negative) water potential.

18  Chapter 1 they leak out rapidly. Therefore, some acropetal penetrants may show limited basipetal (downward from the apex toward the base) movement. The degree to which basipetal movement occurs depends on the extent of chemical incompatibility in phloem cells and the concentration of the fungicide. Downward movement is minimal and not practical in terms of facilitating control of crown and root diseases. Local penetrants. Local penetrant fungicides are mobile for only short distances in plants. They move through the apoplast but are not distributed through xylem or phloem cells (Fig. 1.7). For some older compounds, especially the dicarboximides (vinclozolin and iprodione), the extent of uptake and possible transport is uncertain. However, mobility is well defined for modern local penetrants such as trifloxystrobin and pyraclostrobin. As the active ingredients are absorbed, they adhere to lipid layers in the waxy cuticle, where they tend to accumulate. Since the cuticle protects both upper and lower leaf surfaces, some of the fungicide migrates in the apoplast around cells and through intercellular spaces toward lipid layers on the opposite side of the leaf. Migration through leaf tissues beneath the surface deposit is referred to as “translaminar movement.” Growth of fungal hyphae inside plants is arrested if fungitoxic concentrations of active ingredients are encountered during the compound’s transport across the leaf. Thus, local

Fig. 1.7. Local penetrant fungicides diffuse into the cuticle and accumulate in the waxy layers. Some fungicide may migrate through leaf tissues toward the cuticle on the opposite side of the leaf.

Turf Fungicide Fundamentals  19

penetrants possess some qualities of both acropetal penetrants and contact fungicides. Residual surface deposits and accumulations in the waxy cuticle protect against new infections; translaminar movement of fungicide can suppress existing infections beneath the site of the fungicide deposit. Mobility of local and acropetal penetrants is illustrated in Figure 1.8, where four QoI fungicides were applied to the base of wheat leaves prior to inoculation with the powdery mildew pathogen. Mildew infection occurred above the fungicide application site for local penetrants (trifloxystrobin and kresoxim-­methyl), but infection all the way to the leaf tip was prevented where acropetal penetrants (azoxystrobin and picoxystrobin) were applied. Systemic penetrants. Systemic penetrants can move upward (acropetally) and downward (basipetally) in the plant. They are transported through the symplast, the continuous network of cells with living protoplasts. Phloem cells and mesophyll cells contain living protoplasts; epidermal and xylem cells do not. When a systemic penetrant fungicide diffuses through the cuticle and past epidermal cells, it migrates into mesophyll cells where it follows the transport of sugars into the phloem and other parts of the plant (Fig. 1.9). Sugars are essential for providing the energy and structural components for growth of all plant parts. The transport is passive and follows a gradient from areas of high sugar concentration to areas of low sugar concentration, or from source to sink (Fig. 1.10). Fully expanded leaves manufacture the most sugar. They require some of it to sustain their own growth, but they export most of it to other parts of the plant for storage or to be utilized for growth. Roots do not produce their own sugars, but they still must grow and rely on a regular

Fig. 1.8. Movement of acropetal and local penetrant fungicides. Fungicides were applied to the bases of wheat leaves prior to inoculation with the powdery mildew pathogen. (Adapted from Bartlett et al., 2002)

20  Chapter 1

Fig. 1.9. Systemic penetrant fungicides diffuse into the cuticle and move through cells with living protoplasts. Upon reaching the phloem and xylem, they are transported upward and downward in the plant. In the phloem, materials follow a sugar gradient from source (expanded leaves) to sink (roots and emerging leaves).

Fig. 1.10. Fungicides transported through the network of cells with living protoplasts (symplast) follow a gradient from areas of high sugar concentration to those with low sugar concentration.

Turf Fungicide Fundamentals  21

supply from leaves, transported down the gradient through the phloem. New, rapidly expanding leaves cannot produce sufficient sugars to sustain their own growth; therefore, additional sugar must be imported from areas of production in expanded leaves. Since compounds moving through the symplast may be transported along the sugar gradient in phloem cells, they are “ambimobile,” capable of transport upward and downward in the plant. Along the journey through plant cells, some of the compound enters xylem cells and may be transported to leaf tips and margins. Currently, only phosphonic acid fungicides are ambimobile, or truly systemic. These include fosetyl aluminum, the active ingredient in Chipco Signature, and a variety of the phosphonic acid products. The movement of phosphonate into roots makes them ideal for root disease control, but, to date, the phosphonic acids are not active against root-­infecting fungi except Pythium species. Vapor Phase Activity Some fungicides exhibit vapor phase activity. Fungicide within the surface deposit volatilizes into a gaseous phase and moves and suppresses fungal growth beyond the immediate site of deposit. The vapor phase phenomenon is used to explain activity of trifloxystrobin beyond the site of fungicide application, as shown in Figure 1.8. Research shows that vapor phase activity is real, but its practical significance, especially with regard to turf disease control, remains uncertain. The Depot Effect “Depot effect” refers to situations where fungicide applied to turf is washed from the original site of deposit and accumulates in soil and thatch and on other areas of the plant such as leaf axils or around the base of individual plants. The extent to which the accumulation, or depot, contributes to disease control remains in question and differs with each type of fungicide and perhaps each disease. For example, a small amount of active ingredient of an acropetal penetrant fungicide may accumulate in thatch or in the top half inch of soil. Roots may absorb fungicide, which then may be translocated, possibly affecting root, crown, and leaf pathogens, provided fungicide concentrations are effective. This is the theory behind recommendations that target basal anthrac­nose and root diseases such as summer patch, necrotic ring spot, spring dead spot, and take-­a ll patch. Root absorption applies only to acropetal penetrants. Fungicides that remain bound to organic matter in the soil–thatch matrix may suppress pathogenic fungi growing through the root zone. This type of passive fungicide activity applies to all penetrant and contact fungicides, but the contribution to disease control is variable and is influenced by disease pressure and numerous environmental factors. The nature of turf growth influences the effect of fungicide accumulations at the base of an individual plant. Since new leaves emerge from the center of a growing plant, the oldest leaves and leaf sheaths are outermost at the base of the plant (Fig. 1.11). Therefore, fungicide accumulation close to the crown may protect against infection through the oldest leaves but is not likely to penetrate through successive leaf layers for translocation to newly emerging leaves. Accumulations higher on the plant, for example, in leaf axils, have a

22  Chapter 1

Fig. 1.11. “Depot effect” describes the activity of a fungicide that accumulates at the base of the plant or below.

better chance of protecting new growth from infection. However, since water potential of new growth is greater than that of expanded leaves, translocation of an active ingredient from a depot into emerging leaves through the xylem is weak at best. The depot effect is an interesting concept, but scientific investigations on plants are sparse and nonexistent on turf. From a practical perspective, because of the anatomy and physiology or turf plants, a reasonable case can be made for external protective action by fungicide accumulations, but their chemotherapeutic value remains unclear.

Fungicide Formulations Golf course superintendents should have a sound understanding of pesticide formulations in order to use turf chemicals proficiently and to prepare themselves for communication with inquiring administrators, golf patrons, and the public at large. Those who can explain the characteristics and advantages of products they apply instill greater confidence that pesticides are being used appropriately. Technically, the “formulation” represents the mixture of active and inert ingredients in the pesticide and describes the physical state (liquid or solid) of the product. A fungicide active ingredient is the molecule that provides biological activity to control the fungus. Chemical and physical properties of active ingredients prohibit their application in pure form. Therefore, active ingredients are combined, or “formulated,” with inert

Turf Fungicide Fundamentals  23

ingredients in modern fungicides. Although inert ingredients have no fungicidal activity, they are essential components of the finished product. Not only do they permit the active ingredient to be delivered in a usable form, they also improve fungicide performance, enhance safe handling characteristics, and lessen risk of phytotoxicity. The proportion of inert ingredients is listed on fungicide labels along with the description of active ingredients. Turf fungicides are manufactured in a variety of formulations designed to optimize the efficacy and applicability of the product. In general, turf fungicide formulations are classified as dry or liquid, with specific formulation types within each category (Table 1.4). Some fungicides may be formulated into both dry and liquid products to offer more flexibility in their use. For example, PCNB, used for snow mold control, is offered as Turfcide 400F (liquid) and Turfcide 10G (dry). Since fungicides for snow mold control are

Table 1.4. Fungicide formulations used for turf disease control Formulation


Dry Wettable powder (WP) Water-soluble packet (WSP)

WPs are among the earliest formulations. They are finely ground, solid particles containing active and inert ingredients. They are less expensive to manufacture and store well as long as they are kept dry. Constant agitation is essential, since WPs tend to separate out in the spray tank. They are particularly abrasive to nozzles and spray pumps. WPs are dusty and can be unpleasant to use. Improved packaging in WSPs greatly facilitates handling.

Water-dispersible granule (WG)

WGs (also referred to as WDGs) are dry formulations (similar to WPs) dispersed in water. They can separate in the spray tank and also require constant agitation. The particles are much larger and much easier to handle (less dust and inhalation risk) than WPs.

Granule (G)

Granular products include active and inert ingredients on large particles designed for dry application with spreaders. Traditionally, granules have failed to provide the same uniformity of coverage achieved with sprayable fungicides.

Liquid Emulsifiable concentrate (EC) Emulsion in water (EW)

ECs are oil-based liquids. They form an oil-in-water emulsion (suspension of two liquids) in the spray tank. EW formulations are similar but with slightly different chemical properties. If several products are tank mixed, the EC or EW component should be added last.

Suspoemulsion (SE)

SEs contain suspended solids and emulsion droplets. They may be prone to incompatibility problems with several tank-mix partners.

Microemulsion (ME) Microemulsion concentrate (MEC)

MEs are liquids, similar to ECs, but their very small particle sizes prevent the oil and water phases from separating.

Flowable (F) Suspension concentrate (SC)

Fs and SCs are finely ground, dry particles suspended in water. Among liquid formulations, they are most likely to have problems with separation in the spray tank without careful attention to agitation. These liquids are very viscous (thick), and rinsing containers requires extra effort.

24  Chapter 1 normally applied in late fall, weather conditions may dictate the more appropriate formulation. For example, granular formulations of PCNB are particularly useful during cold weather, when liquid formulations or sprayable dry formulations run the risk of nonuniform distribution because of freezing water in spray nozzles. Although granular formulations are among the earliest of fungicide formulations, improved formulation technology and an interest in combining fungicides with fertilizers are prompting renewed efforts in granular fungicides. Dry flowable (DF) or wettable granule (WG or WDG) formulations are improvements over wettable powders (WP) in terms of handling and inhalation exposure to the applicator, but they are more expensive to produce. Liquid formulations involve either solids suspended in water as flowables (F) and suspension concentrates (SC) or emulsions (liquids suspended in water). Advances in liquid-­formulation technology have spawned improvements over the original emulsifiable concentrates (EC) in the form of microemulsions (ME) or suspoemulsions (SE) and emulsions in water (EW). Selected References Bartlett, D. W., Clough, J. M., Godwin, J. R., Hall, A. A., Hamer, M., and Parr-­Dobrzanski, B. 2002. The strobilurin fungicides. Pest Manag. Sci. 58:649-­662. Couch, H. B. 1995. Diseases of Turfgrasses, 3rd ed. Krieger Publishing, Malabar, FL. Crowdy, S. H. 1972. Translocation of systemic compounds. Pages 93-­114 in: Systemic Fungicides. R. W. Marsh, ed. Longman Group, London. Fungicide Resistance Action Committee. 2009. Godwin, J. R., Bartlett, D. W., and Heaney, S. P. 1999. Azoxystrobin: Implications of biochemical mode of action, pharmacokinetics and resistance management for spray programmes against Septoria diseases of wheat. Pages 299-­315 in: Septoria on Cereals: a Study of Pathosystems. J. A. Lucas, P. Bowyer, and H. M. Anderson, eds. CAB International. Wallingford, U.K. Gold, R. E., Ammerman, E., Koehl, H., Leinhos, G. M. E., Lorenz, G., Speakman, J. B., Stark-­ Urnau, M., and Sauter, H. 1996. The synthetic strobilurin BAS 490 F: Profile of a modern fungicide. Pages 79-­92 in: Modern Fungicides and Antifungal Compounds. H. Lyr, P. E. Russell, and H. D. Sisler, eds. Intercept, Andover, U.K. Hewitt, H. G. 1998. Fungicides in Crop Protection. CAB International, New York. Hisada, Y., Kato, T., and Kawase, Y. 1977. Systemic movements in cucumber plants and control of cucumber gray mould by a new fungicide, S-­7131. Neth. J. Plant Pathol. 83:71-­78. Kush, R. 2005. What are those other ingredients? Golf Course Manag. 73(5):99-­100. Kush, R. 2006. Back to basics: A review of pesticide formulation types. Golf Course Manag. 74(1):143-­145. McCallan, S. E. A. 1967. History of fungicides. Pages 1-­37 in: Fungicides: An Advanced Treatise. Vol. 1, Agricultural and Industrial Applications: Environmental Interactions. D. C. Torgeson, ed. Academic Press, New York. Morton, V., and Staub, T. 2008. A short history of fungicides. American Phytopathological Society. National Academy of Sciences. 2000. The Future Role of Pesticides in U.S. Agriculture. The Academy, Washington, DC. Neumann, St., and Jacob, F. 1995. Principles of uptake and systemic transport of fungicides within the plant. Pages 53-­73 in: Modern Selective Fungicides. H. Lyr, ed. Gustav Fischer Verlag, Jena, Germany. Russell, P. E. 2005. A century of fungicide evolution. J. Agric. Sci. 143:11-­25.

Turf Fungicide Fundamentals  25 Schumann, G. L., and D’Arcy, C. J. 2009. Essential Plant Pathology, 2nd ed. American Phytopathological Society, St. Paul, MN. Sharvelle, E. G. 1961. The Nature and Uses of Modern Fungicides. Burgess, Minneapolis, MN. Torgeson, D. C. 1967. Fungicides: An Advanced Treatise. Vol. 1, Agricultural and Industrial Applications: Environmental Interactions. Academic Press, New York. Torgeson, D. C. 1969. Fungicides: An Advanced Treatise. Vol. 2, Chemistry and Physiology. Academic Press, New York. Whitford, F. 2002. The Complete Book of Pesticide Management, Science, Regulation, Stewardship, and Communication. John Wiley & Sons, New York. Ypema, H. L., and Gold, R. E. 1999. Kresoxim-­methyl: Modification of a naturally occurring compound to produce a new fungicide. Plant Dis. 83:4-­19.

Mode of Action Fungal Growth Cellular Targets Selectivity and Spectrum of Activity Mode of Action Classification

Modes of Action of Fungicides



Mode of Action The mode of action of a fungicide describes how the active ingredient affects the fungal pathogen. Depending on the fungicide, mode of action may be described at several different physiological levels including morphological changes, affected cellular components or biochemical processes, and sites of molecular activity. The extent of our understanding of mode of action varies with different active ingredients. Where knowledge is limited, such as with the dicarboximide fungicides (iprodione and vinclozolin), mode of action is most often described in terms of the observed changes in fungal morphology and growth in laboratory cultures. In other cases, such as the benzimidazole fungicides (thiophanate-­methyl), research has uncovered the exact molecular site of activity. Because mode of action is related to other issues (especially fungicide resistance), researchers continue to explore the fundamentals of how fungicides affect target pathogens. A more thorough understanding of fungicide mode of action will help prepare turf managers to deal with issues such as efficacy against new or emerging diseases and complications brought on by the development of fungicide-­resistant strains in pathogen populations. The objective of this chapter is to describe modes of action for active ingredients used for turfgrass disease control. Understanding the nature of a fungicide’s mode of action may not be essential for controlling turf diseases, but it can lead to a more informed approach to controlling diseases with available chemical assets. A working knowledge of fungicide mode of action helps explain the selectivity of certain fungicides, i.e., why they are effective against some fungi and not others and, more importantly, why they do not kill plant or animal cells. It also forms the foundation for developing sound resistance-­management strategies. At the very least, a review of fungicide mode of action provides an appreciation for the incredibly small scale at which fungicides interact with their targets and an awareness that minute changes in the active ingredient or its target site can explain the difference


28  Chapter 2 between effective and ineffective molecules, safe and phytotoxic compounds, and sensitive and resistant pathogen strains. The first part of this chapter describes how fungal cells grow, identifies the cellular sites targeted by fungicides, and addresses the issue of selectivity. The second part details, to the extent that current knowledge allows, physiological and metabolic sites of action of individual fungicides used for turf disease control.

Fungal Growth All turf managers should be familiar with the term “mycelium,” which is the part of the fungal pathogen that is often used for identifying certain diseases in the field. The mycelium, such as that observed with symptoms and signs of dollar spot and Pythium blight (Fig. 2.1), is composed of numerous filaments, or threads, of the pathogen. A single mycelial thread is called a hypha and is the basic unit of growth and structure of almost all fungi, and certainly of all important turf pathogens. The plural of hypha is hyphae, and the mycelium is a mass of hyphae. The hypha is shaped like a cylinder or tube and is often compartmentalized into distinct cells by cross walls called “septations” or “septa.” The septa are porous, so the cytoplasm (cell fluid) is more or less continuous throughout the growing filament. Hyphal cells may be compared to cars on a commuter train with doors at each end to allow passage from one car to another (Fig. 2.2). Suspended within the cytoplasm are organelles, the various structural and Fig. 2.1. Mycelium (a visible mass of hyphal threads) is a diagnostic functional components that support fungal growth aid for identifying Pythium blight in the field.

Fig. 2.2. A single thread of mycelium is called a hypha. It is composed of individual cells that often are separated by porous cell walls. Cellular fluids and components are able to flow from one cell to another.

Modes of Action of Fungicides  29

and the ability to parasitize turf leaves, stems, and roots. Included among these organelles are the nucleus, mitochondria, ribosomes, and cell membranes. The fluid substance of the cytoplasm is rich with assorted proteins that regulate chemical reactions that are absolutely essential for the function of the cell components. A cytoskeleton composed of fibers and microtubules helps maintain the organization of organelles within each cell. The most active part of the hypha is its tip, or apex. Fungi grow or extend only at the apex. Individual filaments grow longer but not wider. For that reason, the length of hyphae may be unlimited, but the width remains fairly constant. In fact, because the width of hyphal filaments remains constant, it is a trait that can be measured microscopically and used to describe and identify different species of fungi. Hyphae regularly branch in response to various physical and chemical stimuli. Branches also have apexes, and further growth results in the characteristic radial expansion of the fungus often demonstrated in culture plates (Fig. 2.3). The importance of apical growth cannot be overstated and is essential to an understanding of fungal development and the efficacy of fungicides. The apex is rich in enzymes that are secreted by the fungus into its substrate in order to break down complex food sources into simple nutrients needed for growth. Most of the energy that drives mycelial expansion is produced at the apex, and it is where cell wall and membrane components are manufactured and arranged into functional parts. All essential components (the secreted enzymes, the energy-­production units, and the cell wall-­ and membrane-­assembly systems) represent potential target sites for fungicides. Interference with the function of even a single component results in metabolic problems throughout the cell, leading to abnormal development and often cell death. The fact that the majority of actions responsible for fungal growth and development occur at actively growing hyphal tips reinforces the notion that fungicides are most effective when the pathogen is actively growing and their targets are exposed and vulnerable. Once the active ingredient enters hyphal tips, mycelial growth slows as fungal metabolism begins to fail. Fungal cells at or near the leading edge of the colony collapse and die as the fungicide takes effect. Cells at the advancing edge are killed, but it is unlikely that the fungicide will reach all cells in the fungal thallus (entire fungal body). Pathogen growth and development resumes when toxic concentrations of fungicide are depleted from the pathogen’s immediate environment. For that reason, the effects of a fungicide are often referred to as being “fungistatic” (inhibiting fungal growth) rather than “fungicidal” (capable of killing fungi). The fungistatic nature of fungicides is an important reason that they must often be reapplied during the season. Spores play an important role in the disease cycle of many turf pathogens. They are agents of infection, dispersal, and in some cases survival. Some spores are genetically identical to the parent mycelium—they are called “asexual” spores or “clonal” spores. Other spores result from genetic recombination or sexual reproduction. They are called “sexual” spores and have attributes of both types of parent mycelium. Although they are structurally and functionally different from the fungal mycelium, once spore germination begins and the germ tube develops into a growing hypha,

Fig. 2.3. A fungal colony growing in a laboratory culture plate (A) represents a network of branching hyphae (B). Microscopic examination of the advancing edge of the colony reveals individual hyphal strands (C).

30  Chapter 2 most of the metabolic processes are identical. An important difference is that spores contain high concentrations of energy-­storage materials such as lipids and complex carbohydrates that fuel most of the hyphal growth prior to invasion of plant tissues. In order to sustain mycelial growth in otherwise actively growing hyphae, essential lipids and carbohydrate compounds must be manufactured as plant tissues are colonized. Because germinating spores draw the essentials from their own storage, fungicides that normally suppress mycelial growth by blocking production of such compounds may not be effective against spores.

Cellular Targets Fungicidal mode of action can be described with regard to six major cellular target sites. Within each major target, there may be several distinct biochemical targets. Many target sites are simply unknown. A diagram of a hyphal tip, presented in Figure 2.4, illustrates various cell components and identifies the major cellular targets as discussed below.

Fig. 2.4. The six major cellular targets of fungicides within the hyphal tip and the fungicides effective at each in controlling turfgrass disease.

Modes of Action of Fungicides  31 Cell Wall The cell wall provides structure and protection to fungal cells. Cell wall components are manufactured in actively growing hyphal tips where they are transported to the leading edge for assembly. During construction, the leading edge of the hyphal tip is porous and permits transport of materials into and out of the cell. Cell walls of most fungi contain chitin, a compound not produced by plants or animals. Because of this rather unique feature, enzymes that produce chitin are inviting targets for fungicides. Without chitin, cell wall construction is not completed, collapsing hyphal tips and severely interfering with fungal growth. Polyoxin fungicides inhibit chitin production in fungal cells. Cell Membrane The cell membrane separates the cytoplasm from the cell wall. It is an extremely complex structure that regulates which compounds exit and enter the cell. Enzymes released through the cell membrane at the hyphal tip begin the attack on plant cells, breaking down complex plant parts into simple nutrients. At the same time, transporter proteins embedded in the cell membrane ferry the nutrients back into the fungal cell. Any disruption of membrane function causes unregulated release of essential compounds, resulting in cell leakage and a cessation of hyphal growth. Sterols are essential components of cell membranes. For many fungi, the fabric of the cell membrane contains ergosterol, a particular sterol that is not produced by plants and animals. The demethylation inhibitors (DMI fungicides) (fenarimol, myclobutanil, metconazole, propiconazole, tebuconazole, triadimefon, and triticonazole) inhibit the production of ergosterol, rendering cell membranes incomplete and nonfunctional. Evidence shows that several other fungicides (chloroneb, quintozene [PCNB], etridiazole, and propamocarb) disturb membrane function by attacking associated proteins and enzymes. Cytoskeleton (Microtubules) The cytoskeleton represents a scaffolding or framework within the cytoplasm and contributes to cell function as well as cell structure. It is composed of microtubules and a variety of filaments. The microtubules play important roles in the transport of organelles and other components within the cell, especially to the growing hyphal tip. They also form the mitotic spindles that are essential for cell division. Microtubules are located in the cell nucleus and at the region of elongation behind the leading edge of the hyphal tip. In the nucleus, they facilitate cell division (mitosis). In the fungal tips, they help transport enzymes and other compounds to the apical area during cell growth. Benzimidazole fungicides disrupt microtubule function by interfering with a molecule called beta-­tubulin, thereby limiting growth and preventing cell division. Mitochondria The mitochondria are cellular organelles that produce and distribute energy for cell growth and development. Compounds from the breakdown of simple nutrients enter the mitochondria, where they are transformed into

32  Chapter 2 stored energy molecules of adenosine triphosphate (ATP). Energy is required to drive all metabolic functions, especially active absorption and expulsion of cellular substances. Interference with energy production leads to a rapid depletion of stored ATP and stalled growth. Several fungicides target energy production at different sites within mitochondria. For example, the QoI (quinone outside inhibitor) fungicides (strobilurins including azoxystrobin, fluoxastrobin, pyraclostrobin, and trifloxystrobin) and a QiI (quinone inside inhibitor) compound (cyazofamid) affect Complex III of the mitochondrial electron transport chain at two different sites (Qo and Qi), whereas flutolanil and boscalid inhibit a different protein complex termed Complex II or succinate dehydrogenase.

Several fungicides target energy production at different sites within mitochondria.

Nucleic Acids Nucleic acids carry the genetic information that determines the structure and function of all cell components. Because they are so fundamental to all living organisms and all living organisms contain the same basic DNA structure, there are very few potential targets in nucleic acid biosynthesis that are specific to plant-­pathogenic fungi. Hence, only a few fungicides act directly on the manufacture of nucleic acids. Mefenoxam, used for Pythium blight control, inhibits the ribonucleic acid (RNA) polymerase I enzyme in the nucleus of sensitive fungi. It blocks production of a type of RNA—ribosomal RNA (rRNA)—­that is an essential component of the cell’s protein-­ manufacturing machinery. Proteins are essential to all parts of cell function and structure, so a compound that interferes with protein synthesis has deleterious effects on cell growth and development. General Cell Constituents Carbohydrates, proteins, and lipids (fats) are essential cellular constituents of all organisms. Proteins are essential to the structure and function of all living cells. Some proteins regulate cell functions; others add to the structural framework of each cell; and enzymes (special types of proteins) catalyze all metabolic processes. Most protein molecules contain a certain arrangement of sulfur and hydrogen atoms called a sulfhydryl (SH) group. Virtually every metabolic process involves proteins with functional sulfhydryl groups. They exist in the cytoplasm and in all organelles. In order for a pathogen to remain healthy enough to grow and parasitize turf roots, stems, or leaves, all of the sulfydryl groups must be intact. Even if only one step in a metabolic process is blocked through the inactivation of a functional group, a bottleneck occurs in the cascade of events that lead to active growth. As a result, further growth is retarded, and in many cases cell death occurs. Although there are various types of functional groups, it appears sulfhydryl groups in any of the thousands of possible sites within each cell provide abundant targets for appropriately named multi-­site fungicides such as chlorothalonil.

Selectivity and Spectrum of Activity Fungicides used for turf disease control must be selective. That is, the active ingredient must attack the intended pathogen without detrimental effects to

Modes of Action of Fungicides  33

turf or other plants or to animals and humans. Selectivity is ultimately determined by the mode of action of the toxic ingredient and its fate in the target species. In some cases, fungicides are selective because their biochemical targets are not present in other organisms. For example, chitin in cell walls and ergosterol in membranes are nearly unique to fungi. Fungicides that interfere with biosynthesis of those compounds pose a reduced risk to other organisms. In most other cases, metabolic processes targeted by fungicides are actually present in nontarget organisms, but the nontarget organisms are either insensitive to ambient concentrations of the toxic agent or they are able to metabolically break down, detoxify, or discharge the active ingredient. For example, humans and plants also have mitochondria, but humans detoxify the fungicide and plants turn on alternative respiration processes. Factors that determine selectivity also account for some of the differences in the spectrum of activity against various turf diseases. The spectrum of activity defines the specific diseases against which the fungicide is effective. It is reasonable to expect that fungicides or fungicide classes will have activity against related pathogens, although individual compounds are likely to differ in their degree of efficacy against specific diseases. A multi-­site compound such as chlorothalonil has a very broad spectrum of activity (effective against many diseases) because most fungi offer a plentiful supply of metabolic targets (sulfhydryl groups) inside the cell. Alternatively, the spectrum of activity of polyoxin D is limited and, for example, does not include Pythium blight. Polyoxins inhibit the synthesis of chitin, an essential cell wall component of many fungi. Since cell walls of Pythium species do not contain chitin, the fungicide is ineffective. There are a variety of reasons that a given fungicide may not be effective against some diseases, including the natural variability among groups of plant pathogens. Figure 2.5 provides a general illustration of the activity of modern fungicides against common turf diseases grouped according to relatedness of their pathogens. Most turf pathogens may be sorted into three groups: oomycetes, ascomycetes, and basidiomycetes. Oomycetes are in a different taxonomical kingdom than true fungi and are actually classified as “fungus-­like organisms,” although they were once described as true fungi. Important oomycetes include pathogens that cause Pythium blight, Pythium root dysfunction, and yellow tuft (downy mildew). From an evolutionary perspective, they are believed to be more primitive than other turf pathogens. Biologically, they are remarkably similar to true fungi in that their hyphae exhibit apical growth and they penetrate plant cells by producing cell wall-­degrading enzymes. However, their cell membranes do not contain ergosterol, and, in most cases, their hyphae have no cross walls (septa). Their sexual spore is an oospore. Modern fungicides for Pythium blight tend to have a very narrow spectrum of activity and, with few exceptions, are generally effective only against oomycete pathogens (Fig. 2.5). Ascomycetes and basidiomycetes are classified in the kingdom Fungi. The common feature of pathogens classified as ascomycetes is the ascus, a structure that gives rise to specialized sexual spores called ascospores. For some ascomycete pathogens, the ascus is extremely rare in nature, and therefore their classification is determined by modern molecular analysis of the fungal DNA sequence. Most ascomycetes (the dollar spot pathogen is an important

It is reasonable to expect that fungicides or fungicide classes will have activity against related pathogens…

34  Chapter 2 exception) also produce abundant asexual spores called conidia. Note that pathogens of common root diseases (summer patch, necrotic ring spot, take-­a ll patch, and spring dead spot) are included among the ascomycetes (Fig. 2.5). The reason that a broad-­spectrum fungicide such as chlorothalonil lacks efficacy against these diseases has more to do with the difficulty in delivering the fungicide to roots than its inactivity against those pathogens. Basidiomycetes represent the most diverse group of fungi in nature. All basidiomyctes are characterized by a developmental structure called a basidium that functions in sexual reproduction. The basidium gives rise to basidiospores, which provide genetic diversity among populations of basidiomycetous fungi. Many basidiomycetes also produce asexual spores. From a turf pathology perspective, basidiomycetes cause a very broad range of disease problems, from fairy ring to rust diseases. A fungicide’s spectrum of activity defines the range of pathogens against which the compound is effective. It is reasonable to expect that if a given fungicide has activity against one member of a genus or group of pathogens, then it may some have activity against related pathogens. Figure 2.5 profiles

Fig. 2.5. Spectrum of activity of fungicides. Turf diseases are arranged in three groups based on the pathogens that cause them: oomycetes, ascomycetes, and basidiomycetes. Selected registered fungicides are listed in the bottom part of the chart along with horizontal lines that span the diseases they control. Dashed lines show inactivity or weak activity at best.

Modes of Action of Fungicides  35

the spectrum of activity of selected compounds in a general sense. From a practical perspective, the spectrum of activity of each fungicide is described in the “Applications” section on each fungicide product label.

Mode of Action Classification Classification of fungicides according to their modes of action changes as research continues to reveal how active ingredients affect fungal metabolism. Because mode of action is intimately associated with the phenomenon of fungicide resistance, a classification scheme based on the mode of action (MOA) was advanced by the Fungicide Resistance Action Committee in 1980. Fungicides for turf disease control are classified according to their MOA groups in Table 2.1 and addressed individually in further detail in the narrative below. MOA Group A Target: Nucleic Acid Synthesis The phenylamide fungicides include mefenoxam, an important active ingredient used to control Pythium blight and other diseases caused by Pythium species. Within the fungal nucleus, mefenoxam interferes with the function of an RNA polymerase enzyme and severely limits the production of rRNA. In healthy cells, rRNA migrates from the nucleus to the cytoplasm where it is integrated into ribosomes, the cellular factories for protein production. Deficiencies in rRNA deprive the cell of ribosomes and ultimately disrupt the synthesis of proteins essential to the structure of fungal cells and the regulation of their metabolism. Consequently, cells die and fungal growth is inhibited. Phenylamide fungicides do not affect all developmental stages in the pathogen. For example, they inhibit mycelial growth but are not effective against germinating spores, because spores possess a reservoir of ribosomes. MOA Group B Target: Microtubules, Mitosis, and Cell Growth Subgroup B1. Beta-­tubulin assembly in mitosis. Benzimidazoles, the first truly noncontact (penetrant) fungicides, were introduced in the late 1960s. They generally control diseases caused by a wide range of fungal pathogens, but they lack activity against Pythium species and other oomycetes. The active ingredient benomyl (no longer registered for use on turf) is historically important in that it nearly revolutionized turf disease control after the use of heavy metal-­based compounds was restricted and later banned. Interestingly, benomyl was the first fungicide to which resistance in pathogen populations evolved. Currently, the only benzimidazole fungicide used against turf diseases is thiophanate-­methyl. Once inside the plant, it is transformed to methyl benzimidazole carbamate (MBC), a metabolite that binds to tubulins in the fungal cell. Tubulins are the building blocks for microtubules, important structures that help transport cellular components. Because microtubules serve an essential function during mitosis (cell division), interruption of the process leads to cell death. Also, within the cytoplasm, microtubules convey components for cell growth to the hyphal apex.

36  Chapter 2 Table 2.1. Fungicide Resistance Action Committee (FRAC) designations for fungicide mode of action (MOA) codes and resistance groups for active ingredients used for turf disease control FRAC MOA codea

Fungicide active ingredient

Basic manufacturer product

FRAC resistance group

Nucleic acid synthesis



Subdue Maxx


Microtubules, mitosis, and cell growth

B B1


Cleary 3336







boscalid flutolanil

Emerald Prostar

7 7


azoxystrobin fluoxastrobin pyraclostrobin trifloxystrobin

Heritage Disarm Insignia Compass

11 11 11 11










iprodione vinclozolin

Chipco 26GT Curalan

2 2


chloroneb PCNB etridiazole

Chloroneb Turfcide Koban

14 14 14





Metabolic or cellular target

Respiration processes (mitochondria)

Signal transduction—cell wall and cell membrane components

Lipids and cell membrane systems




Ergosterol biosynthesis (cell membrane)


cyproconazole fenarimol metconazole myclobutanil propiconazole tebuconazole triadimefon triticonazole

Sentinel Rubigan Tourney Eagle Banner Maxx Torque Bayleton Trinity/Triton

3 3 3 3 3 3 3 3

Glucan (chitin) synthesis in cell walls


polyoxin D



Multi-site activity…nonselective inhibition of enzyme function reactions with cellular constituents.


chlorothalonil mancozeb thiram

Daconil Fore Spotrete


copper sulfur

Assorted prod­ucts

fosetyl Al phosphonic acids

Chipco Signa­ture

Uncertain mode of action a


See for an explanation of FRAC codes.


Modes of Action of Fungicides  37

Cells with impaired or deficient microtubules suffer interrupted transport of essential growth elements, thereby suppressing hyphal growth. Selectivity of benzimidazole fungicides seems to be explained by the strength of binding by MBC to target site. Although tubulins are important to the structure and function of plant and animal cells, strong binding by MBC occurs only in sensitive fungi. Since oomycetes such as Pythium species lack the target tubulin, benzimidazoles are not effective against them. Subgroup B5. Delocalization of spectrin-­ like protein. Spectrin-­like protein is thought to provide a bridge between the cytoskeleton and the cell membrane. It is important to membrane integrity in mammalian cells. In oomycete pathogens (such as the Pythium blight pathogen), spectrin-­like protein is thought to play a role in the elongation of hyphal tips. Fluopicolide interferes with the localization or collection of spectrin-­like protein growing cells, thereby disturbing membrane structure and function. Germinating spores and hyphal tips swell and burst after treatment with fluopicolide. The fungicide has a high degree of specificity and is not cross-­resistant with other fungicides used to control oomycete pathogens. MOA Group C Target: Mitochondrial Respiration Respiration is a metabolic process that generates energy for all other cell functions. As the pathogen parasitizes plant cells, it nourishes itself with simple sugars, such as glucose, derived from the breakdown of plant proteins, lipids, and complex carbohydrates. Through the process of glycolysis in the cell cytoplasm, glucose is broken down into a variety of compounds that provide the building blocks for fungal growth. Among the breakdown products is pyruvic acid, a compound that filters through the cytoplasm and into mitochondria, where it is transformed to acetyl coenzyme A, an essential constituent of the tricarboxylic acid cycle. Metabolites from the tricarboxylic acid cycle are used in the respiratory electron transport chain to generate ATP, the ultimate source of cell energy (Fig. 2.6). The electron transport chain is composed of four linked complexes, each representing a potential fungicide target. Carboxamide fungicides (flutolanil and boscalid) disrupt respiration at Complex II; QoI fungicides and QiI fungicides attack Complex III, but at different locations (Fig. 2.7). Cross-­resistance does not occur between fungicides that attack at different sites along the electron transport chain. Subgroup C2. Complex II: Succinate dehydogenase. Several different sites of activity apparently exist within Complex II of the electron transport chain. Flutolanil and boscalid are both carboxamides that disrupt respiratory electron transport at Complex II, but they are active against a very different range of fungal pathogens. Among turf diseases, flutolanil is used almost exclusively against basidiomycetes, such as those that cause Rhizoctonia diseases (e.g., brown patch and zoysia patch) and to some extent against fairy ring. Boscalid is used specifically against one disease, dollar spot. Boscalid interferes with fungal respiration and growth by inhibiting the succinate ubiquinone reductase enzyme. The target site of flutolanil, the active ingredient in ProStar, also is located at Complex II, but flutolanil inhibits activity of the succinate dehydrogenase enzyme. Although the two fungicides are classified as carboxamides and target the same electron transport complex, each

38  Chapter 2 fungicide binds to a unique target site, explaining why the spectra of activity of boscalid and flutolanil are so different. Subgroup C3. Complex III: Cytochrome bc1 at Qo site. QoI fungicides (often called strobilurin fungicides) include azoxystrobin, fluoxastrobin,

Fig. 2.6. The respiratory process begins with the breakdown of glucose in cell cytoplasm. Pyruvic acid, a by-product of glucose digestion, migrates into mitochondria, where it is transformed into acetyl coenzyme A and enters the tricarboxylic acid (TCA) cycle. The electron transport chain releases energy-rich adenosine triphosphate (ATP) after accepting products released from the TCA cycle.

Modes of Action of Fungicides  39

pyraclostrobin, and trifloxystrobin and interfere with electron transport at Complex III. Specifically, they inactivate the ubiquinol oxidase enzyme at the cytochrome bc1 site (Fig. 2.7). QoI compounds are recognized for their broad spectrum of activity and are effective against most turf diseases, with the exception of dollar spot. They inhibit spore germination and mycelial growth and reduce spore production in sensitive fungal pathogens. Although QoI fungicides differ in their movement within the plant, they all have some level of chemotherapeutic activity. Beyond their efficacy against many fungal species, the promise of QoI fungicides is associated with the fact that they were derived from naturally occurring compounds originally isolated from mushrooms (Strobilulus tenacellus, source of the name strobilurin) that grow on decaying forest plants. They have low mammalian toxicity and a relatively small ecological impact. Subgroup C4. Complex III: Cytochrome bc1 at Qi site. Cyazofamid also targets cytochrome bc1 in Complex III, but at the inside (Qi center) rather than the outside (Qo center) location. Cyazofamid activity is limited to oomycete pathogens. MOA Group E Target: Signal Transduction Fungicides that interfere with signal transduction defeat the pathogen’s environmental sensory systems. In healthy cells, osmotic-­regulation mechanisms keep pressure inside the hyphae in equilibrium with its environment.

Fig. 2.7. The respiratory electron transport chain occurs within mitochondria. It generates energy in the form of adenosine triphosphate (ATP) to fuel other cell functions. Two of the four complexes in the chain are targeted by fungicides used for turf disease control. Carboxamide fungicides (boscalid and flutolanil) disrupt electron transport at Complex II. QiI (quinone inside inhibitor) fungicide (cyazofamid) and QoI (quinone outside inhibitor) fungicides (azoxystrobin, fluoxastrobin, pyraclostrobin, and trifloxystrobin) interrupt the chain at Complex III.

40  Chapter 2

Dicarboximides also are effective in inhibiting several steps that lead to infection by fungal conidia.

Fungicides such as iprodione, vinclozolin, and fludioxonil deceive the pathogen into overproducing substances that increase osmotic pressure (Leroux et al., 1992). Sustained exposure to the fungicide results in swelling and eventual bursting of hyphal tips, effectively suppressing fungal growth. The exact target location is unknown, but some evidence shows that affected sites are at, or very near, the cell membrane. It is suspected that phenylpyrroles (fludioxonil) and dicarboximides (iprodione and vinclozolin) affect different parts of the same osmoregulation mechanism. Subgroup E2 includes fludioxonil, the active ingredient of Medallion. Evidence shows that exposure to the fungicide results in an increase in osmotic pressure inside the cell, causing hyphal tips to burst. The E3 subgroup includes the dicarboximide fungicides iprodione and vinclozolin. The familiar basic manufacturer trade names for these compounds are Chipco 26 GT (for iprodione) and Curalan (for vinclozolin). There are several post-­ patent generic iprodione products. The dicarboximides were originally classified in MOA Group F1, but recent research with several fungal pathogens that affect agricultural crops suggests different target sites including glutathione synthase and a protein kinase enzyme. At effective concentrations, growth of sensitive fungi is completely suppressed by iprodione, but the effect is reversible and fungal growth resumes with the depletion of the toxic ingredient. This is an interesting and practical example of the fungistatic rather than fungicidal nature of these compounds. Dicarboximides also are effective in inhibiting several steps that lead to infection by fungal conidia (spore germination, germ tube elongation, and appressorium formation). Conclusions regarding dicarboximide mode of action are supported by research on fungicidal effects of iprodione on Drechslera sorokiniana, the causal agent of leaf spot of Kentucky bluegrass and annual bluegrass. Iprodione has shown a limited ability to prevent germination but is strongly effective in limiting germ tube elongation and development of appressoria (preinfection structures produced by surface hyphae). Conidial germ tubes tend to swell and burst in the presence of the fungicide. MOA Group F Target: Lipids and Membrane Synthesis Group F contains five (F1–F5) subgroups, two of which (F3 and F4) contain important fungicides for turf disease control. For each of the subgroups, the exact biochemical mechanisms that are targeted by the fungicides remain unclear. As a result, the mode of action of these fungicides is described largely in terms of the fungicide effects on fungal growth and development at the cellular level. Most of the research on mode of action of fungicides in this group has been conducted with species of non-­plant-­pathogenic fungi in the laboratory. Subgroup F3. Lipid peroxidation (proposed). The aromatic hydrocarbon fungicides used for turf disease control include chloroneb, etridiazole, and quintozine (PCNB) and were the subjects of early investigations on the modes of action of fungicides. Chloroneb and etridiazole are somewhat effective against oomycete pathogens and were traditionally used to protect against Pythium blight. They have good contact activity, and they are rather weak penetrants with low chemotherapeutic activity compared with modern

Modes of Action of Fungicides  41

penetrant compounds. Aromatic hydrocarbon fungicides restrict the growth of mycelium in sensitive fungi but have little or no effect on spore germination. Their specific mode of action is not precisely defined, but apparently it involves a degradation of lipids found in mitochondrial membranes (resulting in the failure of membrane function). Other investigations suggest different modes of action, including the inhibition of mitochondrial respiration by ethazole (closely related to etridiazole). However, in early research, cells treated with aromatic hydrocarbons exhibited abnormally thick cell walls with reduced plasticity, indicating effects on the production or function of enzymes involved in cell wall synthesis. Chemical and microbial stability of PCNB is quite strong, making it much less vulnerable to breakdown by microorganisms. The stability and longevity in nature is an advantage that permits its use as an effective soil fungicide against crop pathogens and perhaps its long-­lasting efficacy against snow molds on cool-­season turf. Subgroup F4. Alterations in fatty acid composition (proposed). Pro­ pamocarb, the active ingredient in Banol, induces membrane leakage and inhibits growth in sensitive fungi. It is suspected that the active ingredient alters certain functional groups in membrane phospholipids, thereby disturbing membrane function. The spectrum of activity of propamocarb is limited to Pythium species and related fungi and is quite effective against Pythium blight on turf. Like other carbamates, propamocarb uptake and acropetal movement is reportedly weak. MOA Group G Target: Sterol Biosynthesis The sterol biosynthesis inhibitors represent the largest group of modern fungicides. Among fungicides used for turf disease control, this group includes fenarimol, metconazole, myclobutanil, propiconazole, tebuconazole, triadimefon, and triticonazole. They are broad-­spectrum fungicides and are also used on a variety of grain, fruit, and vegetable crops and have many uses in the treatment of human fungal diseases such as athlete’s foot. As the name implies, the fungicides inhibit production of certain sterols inside fungal cells. Sterols are important components of almost all living cells, plant and animal. But one sterol, ergosterol, is unique to many fungi. That uniqueness is the target of the sterol biosynthesis fungicides. Ergosterol is synthesized by a complex chemical pathway that actually begins with the breakdown of simple sugar substrates in the cytoplasm of each cell. It is transported to the hyphal tip, where it becomes part of the fabric of the cell membrane. Functional membranes allow the selective absorption and expulsion of certain substances at appropriate rates and concentrations. Once membrane function is disrupted, the entrance and exit of chemical compounds becomes confused, electrolytes leak from cells, growth is suppressed, and, in the case of sustained effects, fungal cells may be killed. Sterol biosynthesis-­inhibitor fungicides are not effective against all turf pathogens because not all fungal pathogens produce their own ergosterol. Pythium blight and yellow tuft are two diseases whose pathogens (oomycetes) acquire sterols directly from the plant tissues that they are parasitizing through mycelial uptake. Thus, they are not affected by the sterol biosynthesis-­inhibiting fungicides. Also, these fungicides cannot be used to inhibit spore germination, a process that relies

The sterol biosynthesis inhibitors represent the largest group of modern fungicides.

42  Chapter 2 Box 2.1. Classification of fungicides that inhibit ergosterol biosynthesis MOA (Mode of Action) Group G: Sterol biosynthesis inhibitors Subgroup G1: DMI fungicides (C-14 demethylation inhibitors) Active ingredient fenarimol metconzole myclobutanil propiconazole tebuconazole triadimefon

Trade name, basic manufacturer Rubigan, Gowan Tourney, Valent Eagle, Dow Banner Maxx, Syngenta Torque, Cleary Bayleton, Bayer


Trinity, BASF Triton, Bayer

Subgroup G2: Morpholines (δ8,7 isomerase and δ14 reductase inhibitors)

(no fungicides registered for use on turf)

Fig. 2.8. Target site of demethylation inhibitors (DMI fungicides).

on stored products for sterol components, and therefore can proceed in the absence of sterol biosynthesis, even in fungal species that are sensitive. The sterol biosynthesis inhibitors are organized into two groups. Group G1 contains the C-­14 demethylation inhibitors (DMI fungicides). Group G2 includes the morpholines, compounds that inhibit isomerase and reductase enzymes in the ergosterol biosynthesis pathway. All of the sterol biosynthesis inhibitors used for turf disease control are classified as DMI fungicides (Group G1) (Box 2.1). Hence, in this text, they will be referred to as DMI fungicides, but they are occasionally referred to as SBI (sterol biosynthesis inhibitor) or SI (sterol inhibitor) compounds in other

Modes of Action of Fungicides  43

discussions of turf fungicides. They are acropetal penetrant fungicides whose mode of action has been studied in great detail. The toxic agent obstructs the action of certain enzymes (demethylase enzymes) in the pathway from acetyl coenzyme A to ergosterol in the cytoplasm (Fig. 2.8). This creates a deleterious bottleneck that allows the precursors to accumulate but severely limits ergosterol production. As a result of the ergosterol deficiency, membranes are not able to properly regulate the compounds that enter and exit the cell; leakage occurs and growth essentially stops. The morpholine group (G2) contains a very small number of commercial fungicides and currently no products for use on turfgrass. However, because their biochemical target is different from that of the DMI fungicides, morpholines may provide future effective sterol biosynthesis-­inhibiting fungicides. Morpholines have been used effectively in a few cases involving crop diseases where DMI fungicides began to fail because of the development of predominantly resistant populations. MOA Group H Target: Glucan (Chitin) Synthesis Polyoxins inhibit the production of chitin, an essential component of cell walls in most fungi. Among turf pathogens, only a few (oomycetes—­ Pythium species and yellow tuft pathogens) do not have chitin in their cell walls. Chitin is produced in arthropod exoskeletons but not in other organisms, and therefore polyoxins have no effect on plants or mammals. Chitin is important because it provides structure and integrity to the growing fungal hyphae. Without the support provided by the chitin component, cell walls collapse and hyphae swell and eventually burst. The same process occurs in the germ tube of a germinating spore. Polyoxins inhibit activity of the chitin synthase enzyme responsible for synthesis of chitin in the hyphal tip. Polyoxins are actually antibiotics produced by a bacterium (Streptomyces cacao var. asoensis). There are several variants of polyoxins (polyoxin A–polyoxin L). Polyoxin D is the metabolically active compound that serves as the active ingredient of Endorse, a fungicide registered for control of anthrac­nose and diseases caused by Rhizoctonia species. MOA Group U Unknown Mode of Action The mode of action of phosphonate fungicides is not clearly defined, although recent advances in pesticide research provide some explanation. As explained in a later chapter, phosphonate fungicides are incorporated into plants as phosphite ions (HPO32–). The ions have a chemical structure different from that of phosphate (PO4–3), so the same effect on plant nutrition (as phosphate fertilizers) is not realized. Instead, phosphonates actually interfere with phosphate metabolism in sensitive fungi. The interference diverts energy-­rich ATP away from other metabolic pathways, resulting in decreased fungal growth. Results of more recent research demonstrate that the phosphonate fungicides also inhibit several enzymes that are important in glucose metabolism, suggesting that more than a single metabolic site is affected by the phosphite ions. Furthermore, there is evidence that, at certain concentrations in the plant, phosphite ions stimulate host plant defense mechanisms,

44  Chapter 2 further contributing to fungicide efficacy. These fungicides have a very narrow spectrum of activity. It has been suggested that, among other reasons, insensitive fungi are able to distinguish between phosphite and phosphate ions, transporting only the phosphate ion or excluding the phosphite in the presence of phosphate. The differences appear very small, but they have a substantial effect on the spectrum of activity of the fungicide. MOA Group M Target: Multi-­Site Functional Groups Group M contains contact fungicides with a variety of active ingredients, including copper, sulfur, mancozeb, thiram, and chlorothalonil. A common target site attacked by these compounds is the sulfhydryl functional group associated with numerous cellular proteins. Proteins with sulfhydryl functional groups exist in all parts of the cell. For example, they regulate chemical reactions in the cytoplasm, break down nutrients in the cell membrane, and generate energy in mitochondria. Those are only a few examples of literally thousands of metabolic processes that depend on proteins with sulfhydryl groups, hence the “multi-­site” designation. Although they represent the oldest and the most important group of fungicides in a historical sense (especially against crop diseases), their mode of action is not well understood, perhaps because of the very fact that their targets are so abundant throughout the fungal cell. Chlorothalonil deserves special mention because it is arguably the most important fungicide available for turf disease control and one of the more widely utilized fungicides for crop disease management. Also, because it is the most contemporary of the multi-­site compounds, its mode of action has been more thoroughly investigated. Chlorothalonil, classified as a benzonitrile, is a very broad-­spectrum contact fungicide. The most significant target of chlorothalonil is the sulfhydryl group of the compound glutathione (Fig. 2.9). Glutathione flows freely throughout the cytoplasm and is an essential regulator of normal cell metabolism. Enzymes that are necessary for breaking down complex molecules into simple nutrients and energy rely on an ample supply of glutathione in the cellular fluid. Chlorothalonil readily reacts with glutathione, rendering it inactive. Without glutathione, enzyme function at several sites within the cell is irreversibly impaired and cell metabolism is severely disturbed, leading to cell death. Chlorothalonil also is reported to

Fig. 2.9. Chemical structure of glutathione, whose sulfhydryl (SH) group is the target of several multi-site fungicides, including chlorothalonil.

Modes of Action of Fungicides  45

obstruct energy production in the cell by reacting with the sulfur-­containing compound acetyl coenzyme A. Selected References Australian Pesticides and Veterinary Medicine Authority. 2004. Evaluation of the new active boscalid in the product Filan fungicide. The Authority, Kingston, Australia. Baldwin, B. C., Clough, J. M., Godfrey, C. R. A., Godwin, J. R., and Wiggins, T. E. 1995. The discovery and mode of action of ICIA5504. Pages 69-­76 in: Modern Fungicides and Antifungal Compounds. H. Lyr, P. E. Russell, and H. D. Sisler, eds. Intercept, Andover, U.K. Bartlett, D. W., Clough, J. M., Godwin, J. R., Hall, A. A., Hamer, M., and Parr-­Dobrzanski, B. 2002. The strobilurin fungicides. Pest Manag. Sci. 58:649-­662. Brown, I. F., and Hall, H. R. 1981. Certain biological properties of fenarimol applicable to its field use. Pages 573-­578 in: Pests and Diseases. Proc. Br. Crop Prot. Conf. British Crop Protection Council, Farnham, U.K. Buchenauer, H. 1977. Mode of action and selectivity of fungicides which interfere with ergosterol biosynthesis. Pages 699-­711 in: Proc. Br. Crop Prot. Conf. British Crop Protection Council, Farnham, U.K. Burden, R. S., Carter, G. A., James, C. S., Clark, T., and Holloway, P. J. 1988. Selective effects of propamocarb and prothiocarb on the fatty acid composition of some Oomycetes. Pages 403-­410 in: Proc. Br. Crop Prot. Conf. British Crop Protection Council, Farnham, U.K. Burden, R. S., Cooke, D. T., and Carter, G. A. 1989. Inhibition of sterol biosynthesis and growth in plants and fungi. Phytochemistry 28:1791-­1804. Copping, L. G., and Hewitt, H. G. 1998. Fungicides. Pages 74-­113 in: Chemistry and Mode of Action of Crop Protection Agents. Royal Society of Chemistry, Cambridge, U.K. Danneberger, T. K., and Vargas, J. M. 1982. Systemic activity of iprodione in Poa annua and post infection activity for Drechslera sorokiniana. Plant Dis. 66:914-­915. Davidse, L. C. 1995. Phenylamide fungicides: Biochemical action and resistance. Pages 347-­ 354 in: Modern Selective Fungicides. H. Lyr, ed. Gustav Fischer Verlag, Jena, Germany. Edgington, L. V. 1981. Structural requirements for systemic fungicides. Ann. Rev. Phytopathol. 19:107-­124. Edlich, W., and Lyr, H. 1995. Mechanism of action of dicarboximide fungicides. Pages 119-­ 131 in: Modern Selective Fungicides. H. Lyr, ed. Gustav Fischer Verlag, Jena, Germany. Ellner, F. M. 1995. The glutathione system, a novel target of dicarboximides in Botrytis cinerea. Pages 133-­140 in: Modern Fungicides and Antifungal Compounds. H. Lyr, P. E. Russell, and H. D. Sisler, eds. Intercept, Andover, U.K. Fungicide Resistance Action Committee. 2006. FRAC Code List 2: Fungicides sorted by modes of action. The Committee, Brussels. Gisi, U., and Cohen, Y. 1996. Resistance to phenylamide fungicides: A case study with Phy­ tophthora infestans. Ann. Rev. Phytopathol. 34:549-­572. Gisi, U., Sierotzki, H., Cook, A., and McCaffery, A. 2002. Mechanisms influencing the evolution of resistance to Qo inhibitor fungicides. Pest Manag. Sci. 58:859-­867. Guest, D., and Grant, B. 1991. The complex action of phosphonates as antifungal agents. Biol. Rev. 66:159-­187. Hagan, A., and Larsen, P. O. 1979. Effect of fungicides on conidium germination, germ tube elongation, and appressorium formation by Bipolaris sorokiniana on Kentucky bluegrass. Plant Dis. Rep. 63:474-­478. Halos, P. M., and Huisman, O. C. 1976. Inhibition of respiration in Pythium species by ethazole. Phytopathology 66:158-­164. Hector, R. F. 1993. Compounds active against cell walls of medically important fungi. Clin. Microbiol. Rev. 6(1):1-­21.

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