Compendium of Beet Diseases and Pests SECOND EDITION
Edited by Robert M. Harveson University of Nebraska Scottsbluff
Linda E. Hanson USDA ARS East Lansing, MI
Gary L. Hein University of Nebraska Lincoln
The American Phytopathological Society
Front cover photograph by Lee Panella and back cover photograph by Robert M. Harveson. 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 Control Number: 2009923020 International Standard Book Number: 978-0-89054-365-8 ď›™ 2009 by The American Phytopathological Society All rights reserved. No portion 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. Copyright is not claimed in any portion of this work written by U.S. government employees as a part of their official duties. Printed in China on acid-free paper. The American Phytopathological Society 3340 Pilot Knob Road St. Paul, Minnesota 55121, U.S.A.
Preface The purpose of this publication is to compile and organize beet (Beta vulgaris) production problems into one volume and be as comprehensive as possible. We hope it will be of value to all interested personnel—field workers, diagnosticians, extension specialists, agronomists, entomologists, and home gardeners. Although emphasizing sugar beet, the information often pertains to problems associated with other forms of beets, including fodder beet, table (red) beet, and Swiss chard. An extended effort was made to include images and descriptions of production issues affecting these crops as well. We also recognize and thank those authors of the first edition of the Compendium of Beet Diseases and Insects for their pioneering efforts to produce that landmark volume. We used their publication as a guide and significantly expanded and updated the information into the second edition. The second edition is organized into several major sections, including an expanded introduction with brief histories of beet production, botany, and breeding. The remainder of the compendium is divided into five major parts: Biotic Disorders, Abiotic Disorders, Postharvest Deterioration of Sugar Beet, Major Insect and Arthropod Pests, and Newly Emerging Issues Affecting Production. Special emphasis was placed on increasing the number of images of plant injury symptoms caused by herbicides, nutritional deficiencies, and pathogens and insects, along with their distinguishing characteristics. This revision was authored by 28 scientists affiliated with 14 different institutions or organizations and contains almost 400 images presented as more than 300 composite images, approximately 80% of which are new to this volume.
American Crystal Sugar Company, Moorhead, MN A. W. Anderson, North Dakota State University, Fargo M. A. Boetel, North Dakota State University, Fargo J. R. Brantner, University of Minnesota, Crookston P. R. Brown, Alf Christianson Seed Co., Mount Vernon, WA W. M. Bugbee (retired), USDA-ARS, North Dakota State University, Fargo P. S. Burange, North Dakota State University, Fargo P. Castillo, Institute of Sustainable Agriculture (IAS), Spanish Council for Scientific Research (CSIC), Córdoba, Spain A. Cattanach, American Crystal Sugar Company, Moorhead, MN M. Derie, Washington State University, Mount Vernon A. Dexter, North Dakota State University, Fargo J. Dolalie, American Crystal Sugar Company, Moorhead, MN R. J. Dregseth, North Dakota State University, Fargo J. E. Duffus (retired), USDA-ARS, Salinas, CA L. J. du Toit, Washington State University, Mount Vernon A. T. Dyer, Montana State University, Bozeman G. Fauske, North Dakota Sate University, Fargo L. D. Godfrey, University of California, Davis W. P. Gorenzel, University of California, Davis F. A. Gray, University of Wyoming, Laramie C. Guza, Michigan Sugar Company, Bay City, MI J. Hastings, American Crystal Sugar Company, Moorhead, MN F. J. Hills, University of California, Davis W. J. Hooker, Michigan State University, East Lansing B. J. Jacobsen, Montana State University, Bozeman R. Jones, Sidney Sugar Inc., Sidney, MT J. A. Kalisch, University of Nebraska–Lincoln, Lincoln D. L. Keith, University of Nebraska–Lincoln, Lincoln E. D. Kerr (retired), University of Nebraska–Lincoln, Scottsbluff J. O. Knott, North Dakota State University, Fargo C. Kritzberger, American Crystal Sugar Company, Moorhead, MN L. D. Leach, University of California, Davis R. T. Lewellen, USDA-ARS, Salinas, CA D. Lilleboe, Lilleboe Communications, Fargo, ND H.-Y. Liu, USDA-ARS, Salinas, CA R. E. Marsh, Great Western Sugar Company, Longmont, CO J. S. McFarlane,, USDA-ARS, Salinas, CA T. Newcomb, American Crystal Sugar Company, Moorhead, MN R. K. Oldemeyer, Great Western Sugar Company, Longmont, CO Oregon State University, Department of Entomology, Corvallis L. Panella, USDA-ARS, Fort Collins, CO C. S. Papp, California Department of Food and Agriculture, Sacramento F. B. Peairs, Colorado State University, Forth Collins P. A. Roberts, University of California, Riverside E. G. Ruppel (retired), USDA-ARS, Colorado State University, Fort Collins C. M. Rush, Texas A&M University, Amarillo
Authors of the first edition
W. M. Bugbee (retired), USDA-ARS, North Dakota State University, Fargo J. E. Duffus (retired), USDA-ARS, Salinas, CA B. B. Fischer, University of California, Fresno F. J. Hills, University of California, Davis L. D. Leach, University of California, Davis E. G. Ruppel (retired), USDA-ARS, Colorado State University, Fort Collins C. L. Schneider (retired), USDA-ARS, Michigan State University, East Lansing E. E. Schweizer, USDA-ARS, Colorado State University, Fort Collins A. E. Steele (retired), USDA-ARS, Salinas, CA A. Ulrich (retired), University of California, Berkeley E. D. Whitney (retired), USDA-ARS, Salinas, CA Y. M. Yun, Great Western Sugar Company; currently Mono-Hy Sugar Beet Seed Inc., Longmont, CO We gratefully acknowledge the following individuals who provided figures or images, ideas, manuscript reviews, or in general contributed some other form of assistance. We also are indebted to Senior Editor Carolee Bull and the two anonymous reviewers for their diligence, suggestions, and assistance throughout the course of this project. iii
Authors of the second edition
H. Russell, Michigan State University, East Lansing C. L. Schneider (retired), USDA-ARS, Michigan State University, East Lansing H. F. Schwartz, Colorado State University, Fort Collins E. E. Schweizer, USDA-ARS, Colorado State University, Fort Collins K. Sharpe, American Crystal Sugar Company, Moorhead, MN H. J. Smith, University of Wyoming, Laramie J. A. Smith, University of Nebraska–Lincoln, Lincoln M. E. Stanghellini, University of California, Riverside C. H. Starker, King City, OR A. E. Steele (retired), USDA-ARS, Salinas, CA C. A. Strausbaugh, USDA-ARS, Kimberly, ID I. J. Thomason (deceased), University of California, Riverside W. A. Thornhill, Brooms’ Barn Research Centre, Higham, Bury St. Edmunds, Suffolk, United Kingdom A. Ulrich (retired), University of California, Berkeley University of California, Statewide IPM Program, Davis C. Wardner, American Crystal Sugar Company, Moorhead, MN J. Weiland, USDA-ARS, Fargo, ND E. D. Whitney (retired), USDA-ARS, Salinas, CA W. Wildman, University of California, Davis R. G. Wilson, University of Nebraska–Lincoln, Scottsbluff C. E. Windels, University of Minnesota, Crookston W. M. Wintermantel, USDA-ARS, Salinas, CA J. Wood, West Coast Beet Seed, Salem, OR C. D. Yonts, University of Nebraska–Lincoln, Scottsbluff Y. M. Yun, Great Western Sugar Company; currently Mono-Hy Sugar Beet Seed Inc., Longmont, CO
M. A. Boetel, North Dakota State University, Fargo C. A. Bradley, University of Illinois, Urbana L. Campbell, USDA-ARS, Fargo, ND A. Cattanach, American Crystal Sugar Company, Moorhead, MN A. Dexter, North Dakota State University, Fargo G. D. Franc, University of Wyoming, Laramie K. Fugate, USDA-ARS, Fargo, ND J. S. Gerik, USDA-ARS, Parlier, CA L. D. Godfrey, University of California, Davis F. A. Gray, University of Wyoming, Laramie N. C. Gudmestad, North Dakota State University, Fargo G. Hergert, University of Nebraska–Lincoln, Scottsbluff B. J. Jacobsen, Montana State University, Bozeman R. T. Lewellen, USDA-ARS, Salinas, CA H.-Y. Liu, USDA-ARS, Salinas, CA C. Ocamb, Oregon State University, Corvallis L. Panella, USDA-ARS, Fort Collins, CO V. V. Rivera, North Dakota State University, Fargo C. M. Rush, Texas A&M University, Amarillo G. A. Secor, North Dakota State University, Fargo J. Weiland, USDA-ARS, Fargo, ND R. G. Wilson, University of Nebraska–Lincoln, Scottsbluff C. E. Windels, University of Minnesota, Crookston W. M. Wintermantel, USDA-ARS, Salinas, CA C. D. Yonts, University of Nebraska–Lincoln, Scottsbluff R. M. Harveson L. E. Hanson G. L. Hein
50 51 53 53 54 55 55 57 57 58 58 59 60 61 61 62 62 62 63 63 64 64 67 68 69 70 70 72
1 History of Beet Production and Usage 2 Botany of the Beet Plant 3 Breeding for Disease and Insect Resistance
Part I. Biotic Disorders 6 Disease Development 6 Pathogens of Beet 7 Foliar Diseases Caused by Fungi and Oomycetes 7 Cercospora Leaf Spot 10 Ramularia Leaf Spot 11 Phoma Leaf Spot 12 Alternaria Leaf Spot 14 Rhizoctonia Foliar Blight 15 Powdery Mildew 17 Downy Mildew 19 Beet Tumor or Crown Wart 19 Beet Rust and Seedling Rust 20 Gray Mold or Botrytis Blight 21 Root Diseases Caused by Fungi and Oomycetes 21 Seedling Diseases 24 Aphanomyces Root Rot 27 Charcoal Rot 28 Fusarium Yellows 30 Fusarium Root Rot 31 Phoma Root Rot 32 Phytophthora Root Rot 33 Rhizoctonia Root and Crown Rot 36 Pythium Root Rot 37 Violet Root Rot 38 Phymatotrichum Root Rot 39 Rhizopus Root Rot 39 Southern Sclerotium Root Rot 40 Verticillium Wilt 41 Diseases Caused by Viruses and Viruslike Entities 41 Viruses Transmitted by Polymyxa betae 42 Beet necrotic yellow vein virus 44 Beet soilborne mosaic virus 45 Beet soilborne virus and Beet virus Q 46 Soilborne Virus Complex 46 Virus Yellows Complex 46 Beet Yellows 47 Beet Western Yellows 49 Beet Chlorosis 50 Beet Mild Yellowing
Beet Yellow Stunt Curly Top Cucumber Mosaic Beet Mosaic Beet Leaf Curl Beet Savoy Lettuce Infectious Yellows Beet Yellow Vein Beet Yellow Net Diseases Caused by Bacteria and Mollicutes Bacterial Vascular Necrosis and Rot Bacterial Leaf Spot Yellow Wilt Syndrome des Basses Richesses Beet Latent Rosette Scab Soft Rot Bacterial Pocket Silvering Disease Crown Gall Nematode Parasites of Sugar Beet Sugar Beet Cyst Nematode Root-Knot Nematodes False Root-Knot Nematodes Stem and Bulb Nematode and Potato Rot Nematode Clover Cyst Nematode Stubby-Root and Needle Nematodes Other Nematode Parasites of Beet
Part II. Abiotic Disorders 73 74 75 76 77 78 81 81 82 85
Nutritional Disorders Uniform Yellowing Stunted Greening Leaf Scorch Growing-Point Damage Yellowing with Green Veining Herbicide Issues in Beet Herbicide Injury Transgenic Sugar Beet Other Disorders
Part III. Postharvest Deterioration of Sugar Beet 92 93 93 94
Storage Rots Respiration Nonsucrose Carbohydrate Accumulation Minimizing Postharvest Losses
Part IV. Major Insect and Arthropod Pests 95 95 97 98 99 100 100 102 102 102 103 103 104 106 107 108 108 109 109 110 110 110 111
113 113 114 114 115 116 116
Root Feeders Sugarbeet Root Maggot Palestriped Flea Beetle Wireworms White Grubs Springtails (Subterranean) Sugarbeet Root Aphid Garden Symphylan Leaf and Crown Feeders Sugarbeet Crown Borer Beet Petiole Borer Webworms Cutworms Armyworms Flea Beetles Springtails (Foliar Feeding) Blister Beetles Carrion Beetles Grasshoppers Leaf-Feeding Weevil Thrips Leafminers Lygus Bugs
False Chinch Bug Spider Mites Aphids Beet Leafhopper Empoasca Leafhoppers Silverleaf Whitefly (Sweetpotato Whitefly) Yellow Wilt Leafhopper
Part V. Newly Emerging Issues Affecting Production 118 118 119 120 121 121 122
Fungicide Resistance in Cercospora beticola Central High Plains Perspective Red River Valley Perspective Multiple Root Disease Complexes New Diseases of Unknown Importance Other Fusarium-Associated Problems Black beet scorch virus
125 Appendix 131 Glossary 135 Index
Compendium of Beet Diseases and Pests SECOND EDITION
Introduction History of Beet Production and Usage Domesticated beet (Beta vulgaris) is said to get its name from the Greek letter beta because the swollen, turniplike root resembles a Greek “B”. The oldest known beet type, chard, was domesticated by at least 2000 b.c. and was grown by both the Greeks and Romans. The roots of the plant were originally used medicinally and later the leaves were used as a pot herb, much like spinach or some of the Chinese leaf vegetables. Beetroot, both red and white, was known in Italy during the second and third centuries a.d. and developed by selection from the wild beets native to the seacoasts of the Mediterranean. It was distributed throughout Europe and hybridized with leaf beet types (chard) to produce the multitude of colors and shapes found in table beet today. By the sixteenth century, it was known as the “Roman beet” and was boiled in stews, baked in tarts, and roasted whole. White beets appear to have been more common, but less desirable, than the red beets. During the eighteenth century, we begin to find accounts of large-rooted beets, known as mangel-wurzel, being fed to cattle. They were developed from early fodder beets in Germany and Holland as livestock feed and introduced into England in the 1770s. A mistranslation of the German mangold-wurzel (“beet-root”) as mangel-wurzel (“scarcity root”) resulted in the belief that this plant would be excellent food for the poor during periods of famine, but it was better suited for cows. American colonists brought beets to North America, but it is not known when for certain. Their cultivation was well established by the eighteenth century, since mention is made of chard and of red, white, and yellow beetroot being grown in U.S. gardens in the early 1800s. Experiments were conducted with them at Mount Vernon (home of George Washington) in Virginia, and by 1888, seven different types of mangel, twelve varieties of table beet, and one variety of chard were offered by Burpee’s Farm Annual. During the mid-1700s, the German chemist Andreas Margraff discovered that both white mangold and red beet contained sucrose, which was indistinguishable from that produced from cane. He foresaw that domestic use and the manufacture of sugar was possible in temperate climates, but these ideas would not be realized for another 50 years, when new ways of extraction could be developed. One of Margraff’s students, Franz Karl Achard, pursued this line of research with the help of a grant from Frederick William III of Prussia. Because of the success of his efforts to establish the beet as an economic source of sucrose, he is now considered to be the father of the sugar beet industry. Achard built the first sugar factory at Cunern in lower Silesia (modern-day Poland). He developed effective processing methods using crude plant material with poor concentrations of sucrose since the main source of germplasm for early sugar beet varieties came from the gene pool of the white fodder beet. He also freely shared the results of his research with others. From these humble beginnings, the development of the beet sugar industry of Germany, France, and other European countries can be traced.
During the early 1800s, most European sugar was obtained from the West Indies, originating from cane. After supplies were cut off by the English blockade of continental Europe during the Napoleonic Wars, the demand for sugar grew throughout Europe. Between 1810 and 1815, more than 79,000 acres were in production and more than 300 small factories were built in France. After Napoleon���s demise, sugar again was readily available, and prices collapsed because of excess supplies. The majority of the factories were closed, and new development proceeded slowly. However, with the decline of slavery in the West Indies, the European industry was better positioned to compete with the tropical source of sucrose, and by the 1850s, the industry was well established and operating over most of the continent. After gaining a place in Europe, many attempts were made to introduce sugar beet production in the United States. The first effort to grow sugar beet was in 1830 in Philadelphia, but no factory was ever built and the idea was abandoned. The first factory built in the United States was at Northampton, Massachusetts, in 1838, but it never operated after 1840. Other unsuccessful attempts were made to establish factories in Wisconsin, Illinois, and Michigan. In the early 1850s, Mormon pioneers began to establish home industries to make themselves more independent. One of these was the effort to produce and extract sucrose from locally grown sugar beet crops. From machinery brought from England and transported from Kansas by covered wagon to Utah, they established a factory near Salt Lake City, Utah, in 1852. Because of a lack of knowledge of chemical processing, this attempt also was unsuccessful for producing crystallized sucrose; however, it paved the way for the future development of sugar beet culture and processing in the western United States. The first successful commercial production of beet sugar in the United States began in central California in 1870. By 1890, two factories were operating, in Alvarado (now Union City) and Watsonville. Throughout the history of the sugar beet industry in the United States, many factories were started but operated only for a short period of time. These start-up efforts often were done on a trial-and-error basis, moving around frequently from place to place, trying to find that right combination of factors that would result in more long-term success. Many of the problems encountered were due to the sugar beet seeds that were being imported from Europe. Researchers with the Department of Agriculture learned early on that superior results were obtained when using home-produced cultivars, yet the industry continued to insist on using imported products. This way of thinking inhibited continual success for producing beet sugar in certain areas. Sugar beet as it is known today is unique among food plants in use throughout the world in that it is a product of breeding research, and it also became a prime example of improving plant performance through genetics and breeding (discussed below). The sugar beet plant is also unique in history by its role as a catalyst in revolutionizing agriculture. Growing sugar beet introduced the system of crop rotation, changing from the 1
previous small-grain monoculture in effect in Europe at that time. This allowed manuring and better soil fertility and reduced weed problems, while also supplying a source of food for livestock from beet tops, crowns, and pulp. Of the current world production of more than 130 million metric tons of sugar, about 35% comes from sugar beet and 65% comes from sugar cane. In the United States, about 50– 55% of the domestic production of about 8.4 million metric tons derives from sugar beet. Sugar beet is grown mostly in the temperate zone from plantings made in April and harvested in the fall. In subtropical areas, sugar beet is grown also as a winter crop with spring/summer harvest. In the temperate zone and in terms of economic product, sugar beet is one of the most efficient crops. Yields up to 23,500 kg of sugar per hectare have been produced in California’s Imperial Valley. Today, 11 states and two provinces within four diverse regions are involved with sugar beet production in North America (Fig. 1). These areas include the upper Midwest (Minnesota and North Dakota [United States]), the far west (California, Idaho, Oregon, and Washington [United States]), the Great Plains (Colorado, Nebraska, Montana, and Wyoming [United States] and Alberta [Canada]), and the Great Lakes (Michigan [United States] and Ontario [Canada]; Ohio [United States] ceased production in 2005). The methods of producing cultivars that are adapted to these specific geographic regions and specific production and pest issues continue to this day. These efforts are largely responsible for the continued success of the industry in the United States today. Selected References Anonymous. 1959. The Beet Sugar Story. United States Beet Sugar Association, Washington, DC. Arrington, L. J. 1966. Beet Sugar in the West. University of Washington Press, Seattle. Bennett, C. W., and Leach, L. D. 1971. Diseases and their control. Pages 223-285 in: Advances in Sugarbeet Production. R. T. Johnson, J. T. Alexander, G. E. Rush, and G. R. Hawkes, eds. Iowa State University Press, Ames. Coons, G. H., Owen, F. V., and Stewart, D. 1955. Improvement of the sugar beet in the United States. Adv. Agron. 8:89-135. Harris, F. S. 1919. The Sugar-Beet in America. Macmillan, New York. Rupp, R. 1987. Blue Corn and Square Tomatoes: Unusual Facts About Common Garden Vegetables. Storey Communications, Pownal, VT. Sauer, J. D. 1994. Historical Geography of Crop Plants. CRC Press, Boca Raton, FL. Theis, T. 1971. A food resource. Pages 3-18 in: Advances in Sugarbeet Production. R. T. Johnson, J. T. Alexander, G. E. Rush, and G. R. Hawkes, eds. Iowa State University Press, Ames. Winner, C. 1993. History of the crop. Pages 1-35 in: The Sugar Beet Crop: Science into Practice. D. A. Cooke and R. K. Scott, eds. Chapman & Hall, London.
(Prepared by R. M. Harveson, L. Panella, and R. T. Lewellen)
Fig. 1. Sugar crop acreage (beet [green], cane [yellow]) planted in the United States in 2004. (Courtesy D. Lilleboe)
Botany of the Beet Plant Beet is classified as class Dicotyledoneae, subclass Caryophyllidae, order Caryophyllales, family Chenopodiaceae, Beta vulgaris. There are very few Chenopodiaceae crop plants, beet, spinach (Spinacia oleracea), and quinoa (Chenopodium quinoa), but a number of noxious weeds are also important, including fireweed (Kochia scoparia), Russian thistle (Salsola kali), and lambsquarters (Chenopodium album). Like many of the other members of the family Chenopodiaceae, beets are halophytes. All of the cultivated beets and their ancestral forms are classified as B. vulgaris and have 2n = 2x = 18 chromosomes. Because of the continuous variation that exists between members of B. vulgaris, it has been divided into subspecies. Formerly, and still casually, the ancestral form was classed as Beta maritima but now is classified as B. vulgaris subsp. mari tima, the wild sea beet. The genus Beta is divided into four sections. The centers of diversity of the sections are shown in Figure 2. As four groups, the species relationships agree well with the morphological differences and crossability observed by geneticists and plant breeders. The four sections of the genus Beta are Beta (formerly Vulgares), Corollinae, Nanae, and Procumbentes (formerly Patellares). The species within these sections and their geographic distribution are shown in Table 1 and Figure 2. Section Beta comprises the cultivated beets and the wild maritima forms that are cross-compatible. Section Beta is indigenous to the Mediterranean Basin and extends west to the Canary Islands, east to India, and north to Scandinavia. Section Beta was revised recently by Letschert et al. (Table 1), and the noncultivated forms of section Beta have become an important germplasm resource for plant breeding, particularly for genes conferring disease resistance. Section Corollinae is centered in Asia Minor. Member species are known to possess resistance to curly top, Cercospora leaf spot, and other diseases and to have monogerm seeds and apomictic reproduction. However, as yet, no traits or genes for resistance have been moved into cultivated beets from these species. Section Nanae has only one species and is confined to several mountainous areas in Greece. Section Procumbentes is found in the far western Mediterranean Basin, the Iberian Peninsula, and the islands west of Africa. Member species of section Procumbentes are known to possess high levels of resistance to the sugar beet cyst nematode, Beet necrotic yellow vein virus and its vector (Polymyxa betae), and other pests and pathogens of cultivated beets and promise to be an important source of disease resistance in the future. Cultivated beets are separated into four groups based upon morphology and end use. Leaf Beet Group. This group consists of cultivars in which the leaves and petioles are used as vegetables and pot herbs.
Fig. 2. Geographic distribution of wild species in the four sections of the genus Beta. (Courtesy Central Intelligence Agency)
Leaf beets have also been called spinach beet, Swiss chard, and chard and have been grown since ancient times. Garden Beet Group. This group consists of cultivars with swollen hypocotyls that, along with the leaves, are used as a vegetable. These have also been known as table beet, red beet, beet root, and beet. Young leaves can be included in the “baby leaf” category. Coloration is usually intense red but white, yellow, orange, and pinkish cultivars occur, just as within the leaf beet and fodder beet groups. Garden beet cultivars may be grown to produce a natural, betacyanidine dye for food coloring. Both leaf beet and garden beet leaves have received renewed interest and use in the packaged, mixed-salad industry. Garden beet forms have been known for more than 1,000 years but have been in common use for considerably less time. Fodder Beet Group. This group consists of cultivars that are used as fodder for livestock. The plants have a large, swollen root that consists of both hypocotyl and root. These have also been called mangel or mangel-wurzel. Fodder beets have been grown for 300–400 years and consist of cultivars of various colors. Sugar Beet Group. This group consists of cultivars used for the production of sucrose. They are usually white. The sugar beet root consists of about 90% true root and 10% hypocotyl as contrasted to garden beet, which is 85–90% hypocotyl. Sugar beet cultivars were largely selected from fodder beet germ plasm for higher sucrose concentration and good sugar extraction qualities and have been cultivated as an agricultural crop for about 200 years. Typically, the sucrose concentration in garden, fodder, and sugar beets ranges from 3 to 6%, 6 to 12%, and 14 to 20%, respectively. Sugar beet is a biennial plant, growing as a rosette and accumulating sucrose until the plant becomes vernalized, followed by long-day conditions. This stimulates bolting and the production of flowers and seeds. Vernalization is optimal near 6°C, and the bolting process can vary from less than 1 month to more than 4 months, depending upon the genetic background of the germplasm. Commercial seed production is usually in northwestern marine climates from 40 to 50 degrees latitude (for example, in the Po Valley of Italy, southern France, and the Willamette Valley of Oregon [United States]), where fall-
lanted cultivars receive adequate vernalization under moderp ate winter conditions followed by long days. Sugar beet is a C3 plant and fixes carbon dioxide by the Calvin cycle. Sucrose is stored in the taproot. The root enlarges as a result of the development of cambial rings and expanding parenchyma cells to form a conspicuous ringed structure of eight or more rings. The inner six or so rings account for most of the root size and sucrose storage. Sucrose enters the root via the phloem and is ultimately stored in the vacuoles of parenchyma cells. Among root cells, there is a sucrose concentration gradient, with the highest being in the small cells nearest the vascular zones. Within the whole root, the sucrose concentration is highest near the center of gravity and decreases above, below, and outside this point. Sucrose is removed from sugar beet by hot-water diffusion from sliced (cossetted) roots. The sucrose is refined from the juice by a series of treatments with lime and carbonization and by filtration to precipitate and remove most of the nonsucrose solubles. Following purification, most of the water is removed in heated vacuum pans, and crystallized white sugar is produced after molasses is driven off by centrifugation. Molasses is composed of noncrystallized sucrose and the so-called impurities. These impurities prevent the crystallization of sucrose in a 1.5:1.0 sucrose/impurities ratio by weight. Impurities are natural cellular constituents and include sodium and potassium cations, amino acids, and betaine. Normally, healthy, well-grown sugar beet has a purity that allows 84–90% of the sucrose to be extracted during refining without supplemental ion exchange procedures. Diseases, pests, and environmental stresses usually increase the relative level of impurities and decrease the root yield and sucrose content, leading to inefficiency and potential economic losses for the grower and processor. Selected References de Bock, T. S. M. 1986. The genus Beta: Domestication, taxonomy and interspecific hybridization for plant breeding. Acta Hortic. 182:335-343. Elliott, M. C., and Weston, G. D. 1993. Biology and physiology of the sugar-beet plant. Pages 37-66 in: The Sugar Beet Crop: Science into Practice. D. A. Cooke and R. K. Scott, eds. Chapman & Hall, London. Ford-Lloyd, B. V., Williams, A. L. S., and Williams, J. T. 1975. A revision of Beta section Vulgares (Chenopodiaceae), with new light on the origin of cultivated beets. Bot. J. Linn. Soc. 71:89-102. Lange, W., Brandenburg, W. A., and de Bock, T. S. M. 1999. Taxonomy and cultonomy of beet (Beta vulgaris L.). Bot. J. Linn. Soc. 130:81-96. Letschert, J. P. W., Lange, W., Frese, L., and van den Berg, R. G. 1994. Taxonomy of Beta section Beta. J. Sugar Beet Res. 31:69-85.
(Prepared by R. T. Lewellen, L. Panella, and R. M. Harveson)
Breeding for Disease and Insect Resistance As mentioned above, sugar beet is a relatively new crop, developed after the ability to adequately measure sucrose concentration allowed for mass and progeny selection based on this criterion. Early sugar beet varieties, most likely, came from the gene pool of fodder beet (the white Silesian fodder beet), which had a low sucrose content by today’s standards. Genetic improvement in sugar beet is complicated by its breeding system. The sugar beet plant is biennial and flowering requires a long-day photoperiod and vernalization at 10°C or lower for 80–120 days. After vernalization, the rosette from the previous year produces a flower stalk (bolts) with indeterminate inflorescences. 3
Flowers of sugar beet are perfect but incomplete, containing five stamens and one ovary with usually one embryo, and are mainly wind pollinated with some insect pollination possible. Both genetic (chromosomal, inherited in Mendelian fashion) and genetic-cytoplasmic (cytoplasmic male sterility [CMS], caused by an interaction of the cytoplasmic and mitochondrial genomes) types of male sterility occur, which makes hybrid cultivar production practical. In the wild type, two or more flowers occur as fused clusters to produce multigerm seed balls. Modern agriculture is dependentuponsingle-seededcultivarsbecauseoftheneedfor precision sowing. This trait is known as monogermity and is recessively inherited. Because hybrid cultivars are grown, the seed-bearing parent is always monogerm and the pollinator parent is usually multigerm, producing a seed ball with monogerm maternal traits but a true seed and a subsequent plant that is genotypically multigerm. Wild-type beet is also highly allogamous, enforced by a complex self-incompatibility system that allows almost any two plants to interpollinate while preventing self-pollination. A dominant gene for self-fertility, S f, can circumvent this outcrossing behavior of beet and is widely used by breeders to managepopulationimprovementprogramsbaseduponselfedprogeny performance and to develop inbred lines for hybrids. Hybrids are composed of two or more parental components. Today most cultivars are three-way hybrids with two inbred monogerm lines and a multigerm pollinator that may be inbred or a closely bred derivative from a sib family, e.g., from a fullsib progeny. Hybrids may be either diploid (2n = 18) or triploid (2n = 27). Triploids are made from autotetraploid (2n = 36) pollinators, which are developed using colchicine to double the chromosomes of a diploid plant. Unlike the highly uniform, pure line cultivars of self-fertile crops, such as lettuce, soybean, or wheat, considerable genetic variability may still occur within sugar beet hybrid cultivars. Because most of the known resistance to sugar beet diseases is quantitative (polygenic, i.e., controlled by more than one gene), more experimental efforts are needed to identify those traits required for qualitative resistance (monogenic). The early development of sugar beet was in a temperate northern European climate. This region is still relatively free of disease and environmental stresses and may explain why so few qualitative resistance genes are present in the sugar beet gene pool. Additionally, this lack of selection pressure to maintain high levels of resistance to pathogens, pests, and environmental stresses could have led to a loss of genetic variability. Although the main source of germplasm for early sugar beet varieties was narrow, there is speculation that early sugar beet cultivars contained wild sea beet (Beta vulgaris subsp. maritima) germ plasm from unintentional cross-pollination during seed production. Nonetheless, sugar beet breeding in the United States has primarily concentrated on developing resistance to biotic and abiotic stresses. As sugar beet production spread out of northern Europe, a host of production-limiting, endemic diseases, for which there were few known sources of resistance, was encountered. This was particularly noticed in North America since most sugar beet seeds used in the United States prior to World War I were imported from Europe. After the war, a domestic seed production industry was begun and, by the end of the 1930s, domestic sugar beetseedproductionaccountedforaboutone-thirdoftheUnited State’sseedrequirements.Becausedevelopingdisease-resistant cultivars became a top priority, the U.S. Department of Agriculture (USDA) began making collection trips to look for sources of resistance to diseases such as Cercospora leaf spot and curly top in wild sea beet, as well as in the other species in the genus Beta.Thedevelopmentofdisease-andpest-resistantgermplasm was a collaborative effort among USDA Agricultural Research Service (ARS) researchers, university researchers, sugar company agriculturists, and commercial plant breeders. 4
One of the first successful attempts at breeding for disease resistance was by Italian Ottavio Munerati, who looked to the wild sea beet growing in the Po estuary of Italy as a source of host plant resistance to leaf spot (caused by Cercospora beticola). The germplasm that came out of this program, Cesena, Mezzano, and the Rovigo series (e.g., R 148), has been used worldwide and forms the basis of much of the Cercosporaresistant germplasm in use today. Another example of success from North America was from the viral disease curly top. Because of successive crop failures throughout the Intermountain West of the United States, USDA efforts began focusing on developing resistance from wild sugar beet relatives in 1925. By 1929, about 100 lb of seeds had been produced from vigorously growing plants collected from severely infested fields in Utah. These seeds were tested in 1930 under heavy disease conditions and were later designated ‘US 1’. This cultivar was quickly replaced by more resistant cultivars, but the process likely saved the fledgling sugar beet industry at that time. It was also significant by reversing the previous insistence on utilizing European products and by highlighting the importance of producing locally adapted cultivars with a domestic seed industry. The 1960s saw a large number of changes in sugar beet breeding. The CMS system was developed and used with monogerm females (CMS) to produce and market monogerm, CMS hybrid varieties. The use of a single source of CMS and limited sources for the monogerm trait led to a shrinking of genetic diversity, which, coupled with shortened rotations and increased cultivated acreage, increased disease pressure on the world sugar beet crop. There was a reluctance to use sea beet germplasm, perhaps because of the earlier introgression of so many undesirable traits from the exotic germplasm. By the 1980s, the need for increased pest resistance and greater productivity reawakened interest in using sea beet and other exotic sources of germplasm in public and private breeding programs. Today, the Sugar Beet Germplasm Committee, affiliated with the American Society of Sugar Beet Technologists, coordinates a national evaluation of sugar beet germplasm in the United States, and the Beta collection of the USDA-ARS’s National Plant Germplasm System (NPGS) is one of the bestcharacterized collections that the NPGS holds. Over the past 25 years, evaluations by numerous investigators have been made for resistance to 13 important diseases and insect pests, as well as for more than 26 botanical characteristics and more than 15 important agronomic traits. In Europe, the EU GENRES CT95 42 project screened between 300 and 700 accessions for resistance to eight important diseases and for drought tolerance. Worldwide, commercial and public plant breeders are taking the results of these evaluations and beginning to introgress these new sources of disease resistance into the sugar beet gene pool. Selected References Biancardi, E., Campbell, L. G., de Biaggi, M., and Skaracis, G. N., eds. 2005. The Genetics and Breeding of Sugar Beet. Science Publishers, Plymouth, United Kingdom. Bosemark, N. O. 1993. Genetics and breeding. Pages 66-119 in: The Sugar Beet Crop: Science into Practice. D. A. Cooke and R. K. Scott, eds. Chapman & Hall, London. Coons, G. H., Owen, F. V., and Stewart, D. 1955. Improvement of the sugar beet in the United States. Adv. Agron. 8:89-135. Fischer, H. E. 1989. Origin of the ‘Weisse Schlisische Rübe’ (white Silesian beet) and resynthesis of sugar beet. Euphytica 41:75-80. Frese, L. 2002. Combining static and dynamic management of PGR: A case study of Beta genetic resources. Pages 133-147 in: Managing Plant Genetic Diversity. J. M. M. Engels, V. R. Rao, A. H. D. Brown, and M. T. Jackson, eds. CABI Publishing, Oxon, United Kingdom. Frese, L., Desprez, B., and Ziegler, D. 2001. Potential of genetic resourcesandbreedingstrategiesforbase-broadening.Pages295-309 in: Broadening the Genetic Base of Crop Production. H. D. Cooper,
C. Spillane, and T. Hodgkin, eds. International Plant Genetic Resources Institute (IPGRI), Food and Agriculture Organization of the United Nations (FAO), and CABI Publishing, Oxon, United Kingdom. Lewellen, R. T. 1992. Use of plant introductions to improve populations and hybrids of sugarbeet. Pages 117-Â136 in: Use of Plant
Introductions in Cultivar Development, Part 2. H. L. Shands and L.Â E. Weisner, eds. CSSA Spec. Publ. No. 20. Crop Science Society of America, Madison, WI.
(Prepared by L. Panella, R. T. Lewellen, and R. M. Harveson)
Part I. Biotic Disorders Disease Development Disease is the result of an interaction between a host, one or more pathogens, the environment, and in some cases a vector that results in abnormal growth, development, or functioning of the host. Symptoms are the visible expression by the host of such interactions. Disease severity usually is related to environmental conditions during pathogenesis, susceptibility of the host, and virulence of the pathogen. If any critical disease-producing element is lacking, symptoms do not occur; if conditions are less than favorable for disease development, some infection may take place, but an epidemic does not occur. Signs are another means of disease detection. A sign is any indication of disease on the host from direct observation of the pathogen or its associated parts and products, such as spores, mycelium, exudate, fruiting bodies, or rhizomorphs. Integrated pest management takes advantage of these requirements for disease and attempts to manage the pathogen, the vector (if any), the type of crop and the cropping order, the environment favoring disease development, or a combination of these factors. Biotic disease occurs when pathogens or infectious organisms interact with a host plant and have a negative impact on the host. Pathogens affecting beet include bacteria, fungi, viruses, nematodes, rickettsias, phytoplasmas, oomycetes, and parasitic plants. Many of these pathogens affect plants in different stages of development. For example, Phoma betae can attack seedlings, leaves or roots of mature plants, and beets in storage. Vectors, such as aphids, leafhoppers, nematodes, and fungi, also are important in disseminating disease-causing entities. While a fair amount of research has been done on problems in sugar beet, less is known about some of the diseases and abiotic stressors on other types of beet, such as table, leaf, and fodder beets. In part, this probably is due to the amount of acreage of the different crops and the number of researchers investigating problems on these different crops. In most cases, even for diseases that have not been widely reported on other types of beet, when plants have been screened, lines in all beet types have been susceptible to the diseases. This can be examined by looking at the results for disease screenings with the national Beta collection, for which information is made available on the Germplasm Resources Information Network (GRIN) for the National Genetic Resources Program (NGRP) (www.ars-grin.gov/). For most of the sections in this compendium, unless specifically stated, symptoms and control measures on other beet types are either similar to those described or not known. (Prepared by L. E. Hanson) 6
Pathogens of Beet Bacteria
Bacterial pathogens of beet are generally single celled, rod shaped, microscopic, and non-spore-forming. The exception is a Streptomyces species that is a nonseptate, branched filament that produces conidia on aerial hyphae. Bacteria enter a host through wounds or natural openings, such as stomata and hydathodes. They are disseminated by insects, splashing rain, irrigation water, contaminated equipment, and pruning. Plant-pathogenic bacteria survive from one season to another in soil, plant debris, seeds, or insects or they overwinter on perennial hosts.
Fungi that attack beet are usually branched, filamentous, and either septate or nonseptate. Reproduction is either sexual or asexual and is achieved by the production of spores or resting bodies (e.g., sclerotia, chlamydospores, cystosori, and conidia), some of which resist desiccation and survive for long periods in soil or organic debris or on living plants. Under favorable environmental conditions (temperature and moisture), these structures germinate and, if they are in contact with a susceptible host, cause disease. Infection can be accomplished by direct penetration of the host or by entry through wounds or natural openings, such as stomata, hydathodes, and lenticels. Some fungi, known as obligate parasites, can live and reproduce only in intimate contact with a susceptible host. Infectious entities are disseminated by splashing rain, running water, wind, insects, forcible ejection from the pathogen, or a combination of these means.
Viruses are submicroscopic nucleic acids enclosed by a protein coat. Most plant-pathogenic viruses have coding material that consists of ribonucleic acid (RNA); a few, such as curly top viruses and Cauliflower mosaic virus, consist of deoxyribonucleic acid (DNA). Plant-pathogenic viruses generally are flexuous or rigid rods or polyhedrons. Most are transmitted and disseminated by vectors, such as aphids, leafhoppers, whiteflies, lace bugs, fungi, and nematodes. However, some are transmitted in seeds or mechanically by operations in which a host is injured by contaminated equipment. Viruses are obligate parasites that multiply only in a host or, in some cases, in a vector. In a vector, some viruses are short-lived, or nonpersistent, and some exist in a persistent or semipersistent manner, either for the life of the vector or for an extended period of time. The host range of a virus may be limited to a few species or may include many, which serve as reservoirs of the pathogen. Infected plants may be symptomless or may express symptoms,
such as yellowing, mosaics, ring spots, stunting, veinclearing, and hypertrophy of tissue (root proliferation).
Plant-parasitic nematodes are small (0.3–10 mm long), worm-shaped, stylet-bearing animals. They are usually soilborne. A few to several hundred eggs per female are either laid, singly or in masses, or retained within the body of the female, which develops into a cyst. The larvae go through four molts to reach the adult stage. Different nematode species are infectious at different stages. The length of the life cycle depends on the environmental conditions; under optimum conditions, it is usually 3–4 weeks. Nematodes are disseminated by water and wind, in infested soil, and on plants and machinery. Nematodesmaybeclassifiedaseitherendoparasiticorectoparasitic, according to whether they feed internally or externally, respectively, on the host. Root symptoms of nematode infection include hypertrophy, necrosis, and proliferation of fibrous roots. Foliar symptoms include yellowing, wilting, and stunting.
Rickettsias are organisms that resemble bacteria and measure 0.2–0.5 × 1.0–4.0 µm. They may be confined to certain tissues. They are transmitted by grafting and by insects and are suppressed by antibiotics. Rickettsias can be observed with an optical microscope. They cannot be cultured on common bacterial media, although some have been cultured on defined media.
Oomycetes are filamentous pathogens that appear similar to fungi. They reproduce asexually or sexually by sporangia, zoospores, and oospores. Some are obligate parasites that require living host tissue for growth.
Some parasitic plants are pathogens of higher plants. The only seed-bearing plant known to affect beet is dodder (Cuscuta spp.), which also acts as a vector of many viruses. Dodder has slender, threadlike, leafless, yellowish or orange stems (Fig. 3). When a susceptible crop is planted, dodder plants parasitize their hosts by attaching to them with haustoria, or rootlike organs. Through this association, the dodder receives its nutrition and moisture from the host, while simultaneously reducing the health and vigor of the host. Dodder is a true seed plant and spreads from plant to plant if not managed. It is capable of surviving in the soil from year to year by seeds. The infection center should be burned or controlled by herbicides, and seeds of the parasite should never be allowed to be produced.
Fig. 3. Dodder growing on sugar beet. (Courtesy E. D. Whitney)
Spiders, insects, and centipedes are invertebrate animals that may be pests of plants or vectors of pathogens. They are characterized by jointed appendages and segmented bodies. All of these animals reproduce sexually. In addition, aphids, for example, may reproduce parthenogenetically under favorable environmental conditions. Depending on the species, the life cycle may take as little as a few days or as long as a year or more. The abundance of a species depends on climate, available food, predators, and many other factors. Selected References Agrios, G. N. 2005. Plant Pathology, 5th ed. Academic Press, New York. Cooke, D. A., and Scott, R. K., eds. 1993. The Sugar Beet Crop: Science into Practice. Chapman & Hall, London. Dunning, A., and Byford, W., eds. 1982. Pests, Diseases and Disorders of Sugar Beet. (Translated from French.) B.M. Press, Sartrouville, France. Johnson, R. T., Alexander, J. T., Rush, G. E., and Hawkes. G. R., eds. 1971. Advances in Sugarbeet Production: Principles and Practices. Iowa State University Press, Ames. Maxson, A. C. 1948. Insects and Diseases of the Sugar Beet. Beet Sugar Development Foundation, Fort Collins, CO. Whitney, E. D., and Duffus, J. E., eds. 1986. Compendium of Beet Diseases and Insects. American Phytopathological Society, St. Paul, MN. Wilson, R. G., Smith, J. A., and Miller, S. D., eds. 2001. Sugarbeet Production Guide. Univ. Nebr. Coop. Ext. EC01-156.
(Prepared by L. E. Hanson)
Foliar Diseases Caused by Fungi and Oomycetes Foliar diseases typically are observed as damage to aerial portions of the plant. Many foliar diseases cause leaf spots of various types (Fig. 4). In some cases, these may be difficult to differentiate or to separate from foliar damage from other causes, such as nutrient deficiency, leaf scorch, or herbicide damage. With the advent of the use of table beet leaves in the “baby leaf” market, there is an increased interest in some of these problems.
Cercospora Leaf Spot Cercospora leaf spot, caused by the fungus Cercospora beticola, is the most important and destructive foliar disease of
sugar beet, table beet, and Swiss chard wherever these crops are grown. In addition, safflower (Carthamus tinctorius) was recently reported as an alternate host in Montana (United States). The reported distribution of C. beticola on sugar beet, table beet, fodder beet, spinach, and Beta vulgaris subsp. maritima is given in Figure 5. Wild hosts also include species of the genera Amaranthus, Atriplex, Chenopodium, Cycloloma, and Plantago. This disease is most destructive where warm, humid summers occur in regions of North America and Europe. Losses can approach 40% or more. On sugar beet, losses in the field are manifested by reductions in harvest weight and in the percentage of sugar in the roots. Losses in storage result from increased storage decay, and processing yield is reduced by greater levels of impurities and increased loss to molasses. Losses are attributable to both the destruction of leaf tissue and 7
the effects of the pathotoxins cercosporin and beticolin produced by C. beticola.
Individual leaf spots are most commonly found initially on older leaves and the disease progressively moves to younger leaves. Individual leaf spots are 3–5 mm in diameter at maturity and are nearly circular (Fig. 6 left). Lesion centers are tan to light brown. Signs of the pathogen typically include black fungal stroma scattered within mature lesions, and under conditions of high humidity, the lesion center may have a grayish cast due to the production of conidiophores and conidia on the stroma. Lesion borders are dark brown to reddish purple, depending on the level of anthocyanin production of the host. With the progression of the disease, the individual spots coalesce (Fig. 6 right) and heavily infected leaves initially turn yellow (Fig. 6 left) and then brown and remain attached to the plant. Yellowing and rapid leaf death are caused by pathotoxins produced by the fungus. Lesions also form on petioles and appear elongated rather than circular. Sunken, circular lesions have also been reported on root crown not covered by soil. Reduced beet root yields and sucrose content typically result from foliar infection. Beet roots with low sucrose content do not store as well as those with high sucrose content.
Fig. 4. Comparison of common foliar diseases (left to right): Cercospora leaf spot, Alternaria leaf spot, Phoma leaf spot, and bacterial leaf spot. (Courtesy R. M. Harveson)
C. beticola (phylum Ascomycota, class Dothideomycetes, order Capnodiales, family Mycosphaerellaceae) hyphae are hyaline to pale olivaceous brown, are septate, and vary from 2 to 4 µm in diameter. Mycelia are intercellular in the host and formpseudostromatainthesubstomatalcavities.Conidiophores originate from these stromata (Fig. 7 left) and emerge through host stomates or cracks in the plant surface. Conidiophores are unbranched, measure 3–5.5 × 10–100 (mostly 40–60) µm, and have conspicuous conidial scars at geniculations and at the apex (Fig. 7 right). Conidial ontogeny is holoblastic and conidial secession is schizolytic. Conidia are hyaline, needle shaped, smooth, straight to slightly curved with 3 to 14 or more septa in culture, and typically 2–3 × 36–107 µm (Fig. 8). Environmental conditions can affect conidial morphology; there are some reports of spores up to 400 µm long and with up to 27 septa. Each conidial cell may have one to eight nuclei. No teleomorph stage is known, although considerable genetic variability exists in the fungal population with respect to fungicide resistance. However, there are no reports of physiologic races with respect to genetic sugar beet host resistance. The fungus can be grown on several media, including potato dextrose agar, V8 agar, and beet leaf juice agar. In vitro sporu-
Fig. 6. Cercospora leaf spot symptoms on sugar beet. Left, Ad vanced lesions causing yellowing and death of the leaf. (Courtesy R. M. Harveson) Right, Blighted foliage of sugar beet showing coalescing of lesions. (Courtesy L. E. Hanson)
Fig. 5. Areas delimited by a blue line indicate the reported distribution of Cercospora beticola. (Courtesy B. J. Jacobsen)
lation is facilitated by exposure to light, with light and temperature interacting to determine the degree of sporulation.
Disease Cycle and Epidemiology
C. beticola primarily survives between seasons in infected leaves and petioles as conidia and pseudostroma. Conidia persist 1–4 months on infected leaf debris, while the fungus survives in pseudostroma for 1–2 years. Other reported sources of inocula include infested seeds, conidia or pseudostroma in or on wild hosts, or infected plant tissues buried in soil that allow for root infection. Conidial development and release are conditioned by water films or by very high humidity levels (greater than 98% relative humidity) and temperatures between 20 and 26°C. Under favorable conditions, conidia are most commonly spread by splashing water, although they are readily spread short distances (less than 100 m) by wind. Conidia also may be spread by irrigation water, insects, and equipment or workers under wet conditions. Infection can take place via appressoria when stomates are closed or directly by hyphae when stomates are open. Infection through stomates occurs at temperatures between 12 and 40°C and when relative humidity exceeds 90% for 1–22 h, depending on temperatures. Conidia are produced from primary infections in 7–21 days, depending on temperature, light, leaf age, and host resistance. Generally, this time is shortened as temperature or susceptibility increases. However, at temperatures above 37°C, disease production and spread are reduced. Several models based on environmental and yield loss threshold parameters that describe conditions for sporulation, spore germination, infection, and disease development are available. Environmental conditions used in monitoring include tempera ture and relative humidity, with no sporulation or infection at temperatures less than 10°C and very little at temperatures less than 15°C. Optimal temperatures for sporulation, germination, and infection are 25–35°C. These critical processes all require extended periods of relative humidity greater than 90–95% or of free moisture on leaf surfaces. Approximately 5–8 h of relative humidity greater than 90–95% or of free moisture on leaf surfaces are required at temperatures within the optimal temperature range. Longer periods of free moisture are required at higher or lower temperatures. At 16°C, 22–24 h of favorable humidity are required for infection. Generally, there is little disease development before row closure, and yield loss potential is generally greater with earlier infections. Disease progress is slower for varieties with some degree of genetic resistance (Fig. 9). Environmental monitoring to determine daily potential infection values and disease severity monitoring are used successfully in all areas where Cercospora leaf spot is important.
Fig. 7. Left, Geniculate conidiophores of Cercospora beticola. Right, Individual pseudothecium of C. beticola. (Courtesy R. M. Harveson)
Crop rotations of 2–3 years or more that allow for the decay and destruction of infected crop or weed residues are recommended to reduce disease. Separation of the new crop from infected residues by 100 m helps reduce early-season infections. Timely foliar fungicide application is essential for management. Several fungicides are registered for different beet types. Resistant or tolerant cultivars should be used where available. Disease forecasting programs adapted for the growing region should be used where available. In table beet and Swiss chard, thorough removal or deep plowing of crop residues is recommended. Selected References Carlson, L. W. 1967. Relation of weather factors to dispersal of conidia of Cercospora beticola (Sacc.). J. Am. Soc. Sugar Beet Technol. 14:319-323. Lartey, R. T., Caesar-TonThat, T. C., Caesar, A. J., Shelver, W. L., Sol, N. I., and Bergman, J. W. 2005. Safflower: A new host of Cercospora beticola. Plant Dis. 89:797-801. McKay, M. B., and Pool, V. W. 1918. Field studies of Cercospora beticola. Phytopathology 8:119-136. Pool, V. W., and McKay, M. B. 1916. Climatic conditions as related to Cercospora beticola. J. Agric. Res. 6:21-60. Vereijssen, J. 2004. Cercospora leaf spot in sugar beet. epidemiology, life cycle components and disease management. Ph.D. thesis. Wageningen University, Wageningen, the Netherlands. Windels, C. E., Lamey, H. A., Hilde, D., Widner, J., and Knudsen, T. 1998. A Cercospora leaf spot model for sugar beet: In practice by an industry. Plant Dis. 82:716-726.
Fig. 8. Multicelled conidia of Cercospora beticola. (Courtesy R. M. Harveson)
Fig. 9. Field infection of a susceptible cultivar (right) showing severe blighting compared with that of a resistant cultivar (left). (Courtesy R. M. Harveson)
Wolf, P. F. J., and Verreet, J. A. 2002. An integrated pest management system in Germany for the control of fungal leaf diseases of sugar beet: The IPM sugar beet model. Plant Dis. 86:336-344.
(Prepared by B. J. Jacobsen and G. D. Franc)
Ramularia Leaf Spot Ramularia leaf spot affects sugar beet, table beet, fodder beet, and rarely Swiss chard under cool, damp conditions and has been reported in North America from Oregon, Washington, northern California, and Colorado (United States) and from British Columbia (Canada). In Europe, the disease is found in Ireland, the United Kingdom, the Scandinavian countries, and parts of Belgium, France, Germany, and Russia. It occurs less frequently in central Europe. In the United States, it is most prevalent in sugar beet seed crops, which are usually grown when climatic conditions favor development of the disease.
The fungus attacks older and middle-aged leaves of beet (Fig. 10). Typical leaf spots (Fig. 11) are light brown, and they are larger (4–7 mm in diameter) and more angular than
those caused by Cercospora beticola but may appear similar. Mature lesions may have a dark brown to reddish brown margin, and the necrotic centers of the leaf spots become silvery gray to white upon sporulation of the fungus (Fig. 11 inset). Affected leaves turn yellow, become necrotic, and die, often when less than 30% of the leaf surface is covered with lesions. Symptoms are similar to those of Cercospora leaf spot (see Cercospora Leaf Spot), but these diseases can be clearly differentiated when the pathogens sporulate. C. beticola produces black stromata, seen as black spots in the lesion, while Ramularia beticola produces clusters of conidiophores that are gray or white.
Conidiophores of R. beticola are clustered, short, and subhyaline to hyaline, with prominent conidial scars, and emerge through leaf stomata. Conidia (1.5 × 8.2 µm) are hyaline and cylindric and are frequently formed in short chains. The conidia are typically two celled but also may be one or three celled.
Disease Cycle and Epidemiology
Lack of economic importance has precluded extensive studies of Ramularia leaf spot. Some evidence indicates that the fungus is seedborne and that conidia and mycelium probably overseason in infected crop residues. Spores are dispersed primarily by wind but also can be spread by splash dispersal. Under conditions of high relative humidity and low temperature (17–20°C), conidia germinate on leaf surfaces, and hyphae subsequently penetrate the leaves through the stomata only. At 17°C, the incubation period for disease development is 16–18 days. High plant density and sulfur deficiency tend to increase disease intensity and damage. Significant defoliation can occur if climatic conditions favoring disease development persist for extended periods, but plants frequently recover with the onset of warm, dry weather.
Fig. 10. Ramularia leaf spot lesions on older leaves of sugar beet. (Courtesy J. Wood)
Ramularia leaf spot rarely causes enough damage on sugar beet to warrant management measures in the United States, except in seed production. If management is needed, there are some recommendations. Plant density should be reduced since high plant density tends to increase disease intensity and damage. The presence of sufficient sulfur should be ensured since sulfur deficiency increases disease severity. Some fungicides are effective against Ramularia leaf spot and are registered for use on sugar, table, and fodder beets in Europe but are not registered for use on this disease in the United States. An integrated pest management model has been developed for several leaf diseases on sugar beet in Germany and includes Ramularia leaf spot. Selected References Bennett, C. W., and Leach, L. D. 1971. Diseases and their control. Pages 223-285 in: Advances in Sugarbeet Production: Principles and Practices. R. T. Johnson, J. T. Alexander, G. E. Rush, and G. R. Hawkes, eds. Iowa State University Press, Ames. Byford, W. J. 1975. Ramularia beticola in sugar-beet seed crops in England. J. Agric. Sci. 85:369-375. Byford, W. J. 1976. Experiments with fungicide sprays to control Ram ularia beticola in sugar-beet seed crops. Ann. Appl. Biol. 82:291297. Byford, W. J. 1996. A survey of foliar diseases of sugar beet and their control in Europe. Pages 1-10 in: Proc. IIRB Congr., 59th. International Institute for Sugar Beet Research, Brussels, Belgium. Wolf, P. F. J., and Verreet, J. A. 2002. An integrated pest management system in Germany for the control of fungal leaf diseases in sugar beet: The IPM sugar beet model. Plant Dis. 86:336-344.
Fig. 11. Fungal sporulation on Ramularia leaf spot lesions on sugar beet. Inset, Close-up of lesions. (Courtesy J. Wood)
(Prepared by L. E. Hanson and C. Ocamb)
Phoma Leaf Spot Phoma leaf spot is caused by the seedborne pathogen Phoma betae and commonly affects sugar beet (Fig. 12), table beet (Fig. 13), fodder beet, and chard, in addition to oat and Cheno podium album (lambsquarters). The same fungus also induces seedling disease problems in sugar beet and table beet. It also can persist in the crowns, and it may cause root rot and sugar beet storage rot in harvest piles later in the season and a type of crown rot of mature roots. Although occurring almost everywhere these different beet types are grown, Phoma leaf spot is of little economic importance, except as a source of inoculum for infections of seed stalks and seed clusters.
Individual leaf spots are usually light brown and round to oval (1–2 cm in diameter) and have dark, concentric rings near the perimeter (Fig. 14) as opposed to the smaller lesions with solid centers associated with Cercospora leaf spot (see Foliar Diseases Caused by Fungi and Oomycetes; Fig. 4). Small, spherical, black pycnidia develop in the dark rings, and conidia are produced within the pycnidia. On seed stalks, brown to
black necrotic streaks form and develop grayish, pycnidiabearing centers.
P. betae is an imperfect fungus and is the most commonly found form in nature. P. betae produces pycnidiospores (conidia) in black, ostiolate, lenticular to globose pycnidia that are immersed in host tissue. The conidia (2.6–4.9 × 3.8–9.3 µm; sizes vary greatly because of environmental influences) are hyaline, one celled, and oblong. The perfect stage, Pleospora bjoerlingii (Fig. 15), develops in the autumn under lesion surfaces. Perithecia (160–205 × 230–340 µm) are black and somewhat hemispherical. Asco spores (8.5–10 × 19.5–25 µm) are pale yellow-green and usually muriform. Further descriptions of the pathogen are found in other sections (see Seedling Diseases, Phoma Root Rot, and Postharvest Deterioration of Sugar Beet).
Disease Cycle and Epidemiology
The fungus is seedborne and can survive as conidia in pyc nidia and as mycelium in soil and crop residue for up to 26 months after a beet crop has been harvested. During moist weather, the pycnidia exude a cirrhus (gelatinous mass of spores) from which spores are then dispersed mainly by splashing rain (Fig. 16). When the fungus is present in its perfect stage, ascospores produced in the perithecia are primarily carried to beet foliage by wind. The disease is most severe during periods of high humidity and temperatures of 15–32°C (Fig. 12).
Fig. 12. Severe Phoma leaf spot infection in a sugar beet field. (Courtesy R. M. Harveson)
Fig. 14. Phoma leaf spot of sugar beet showing a circular lesion with concentric rings. (Courtesy L. E. Hanson)
Fig. 13. Phoma leaf spot of table beet. (Courtesy L. J. du Toit)
Fig. 15. Ascus and ascospores of Pleospora bjoerlingii. (Courtesy W. M. Bugbee)
Fig. 16. Discharge of pycnidiospores from pycnidium of Phoma betae on a sugar beet seedling. (Courtesy L. D. Leach)
Fig. 17. Alternaria leaf spot of sugar beet. (Courtesy E. D. Kerr; reprinted, by permission, from Franc et al., 2001)
Cultivars have not been developed with resistance to any of the diseases caused by P. betae. Susceptible beet crops should be planted in a 4-year rotation with nonhost crops. Weed populations, particularly C. album, should be properly managed. Fungicide seed treatments help reduce disease incidence. Processing seeds to remove cortical tissues assists in eliminating the pathogen from this often localized area of the seed. Selected References Bugbee, W. M., and Soine, O. C. 1974. Survival of Phoma betae in soil. Phytopathology 64:1258-1260. du Toit, L. 2004. Diseases of vegetable seed crops: Identification, biology and management. Proc. Organic Seed Growers Conf., 2004. Organic Seed Alliance, Port Townsend, WA. www.seedalliance. org/uploads/pdf/VegSeedDiseases.pdf. Nyvall, R. F. 1979. Diseases of sugar beets (Beta vulgaris L.). Pages 295-314 in: Field Crop Diseases Handbook. AVI Publishing, Westport, CT. Pool, V. W., and McKay, M. B. 1915. Phoma betae on the leaves of sugar beet. J. Agric. Res. 4:169-177. Walker, J. C. 1952. Diseases of Vegetable Crops. McGraw-Hill, New York.
(Prepared by R. M. Harveson)
Alternaria Leaf Spot Alternaria brassicae and A. alternata (syn. A. tenuis) cause leaf lesions in Beta spp. Both A. brassicae and A. alternata are globally distributed and are common wherever sugar beet is grown, especially where cruciferous crops are grown in close association with sugar beet. Alternaria leaf spot also can affect table beet and Swiss chard.
Both fungi are necrotrophic pathogens and may cause conspicuous spotting of all aerial plant parts in an interaction dependent on host reaction and environmental conditions. These spots start as pinheadlike structures that expand into uniform or concentrically zonate lesions of various sizes. On sugar beet, lesions caused by either fungus are circular to irregular (usually 2–10 mm in diameter), are gray (Fig. 17) to dark brown to almost black, and may be surrounded by a chlorotic area. Lesions can develop a velvety black appearance with heavy sporulation. Foliar infection may cause loss of photosynthetic area, accelerated senescence, and defoliation. Infection by A. alternata 12
Fig. 18. Alternaria leaf spot symptoms on sugar beet infected with Beet western yellows virus. (Courtesy R. T. Lewellen)
is believed to be secondary in nature, with symptoms only occurring on old leaves already weakened by senescence, poor nutritional status, or other plant stressors. The presence of A. alternata is also commonly observed in association with Beet western yellows virus (Fig. 18) or Fusarium yellows infections. Although A. brassicae also infects weakened or stressed leaves, this fungus is a primary pathogen able to initiate infection of otherwise healthy leaves. Infection by A. brassicae may cause an incipient green-island effect in the foliar lesions, presumably because of the production of cytokinins by the fungus. Differential diagnosis is further aided by the fact that conidia are usually present on field-infected material. If not present, sporulation can be induced by incubating infected material for 24 h in a moist chamber at 20°C.
Sporulation of A. brassicae is sparse to moderate on the host plant, with conidia usually solitary and found near the center of the lesions. However, chains of two to four conidia are common in culture. Primary conidiophores are single or in groups of 2 to 10 or more emerging through stomata; they are brown, usually simple, frequently geniculate, smooth, and 5–11 × 140–170 µm, and they have zero to seven septa and bear one to several small but prominent conidial scars. Conidia are acropleurogenous, straight or slightly curved, obclavate, beaked with 5–19 transverse and 0–8 longitudinal or oblique septa (Fig. 19), light to medium olivaceous brown, usually smooth, rarely very inconspicuously warted, and 11–42 µm wide in the broadest part and 75–350 µm long. Beaks are one-quarter to one-half of the mature conidium length, 4–9 µm wide, sturdy, never fragile or
Fig. 20. Catenulate conidia of Alternaria alternata in vitro. (Cour tesy E. G. Ruppel)
Fig. 19. Beaked conidia of Alternaria brassicae. (Courtesy J. S. McFarlane; reprinted, by permission, from McFarlane et al., 1954)
filamentous, and usually without transverse septa and may be replaced by simple or geniculate secondary conidiophores, especially in culture. Sporulation of A. alternata on foliar lesions under conditions of high humidity reveals abundant small conidia growing in long chains throughout the lesion. These conidia, characterized as approximately 6–16 × 9–42 µm, are readily distinguished from those of A. brassicae by their smaller size and growth in long chains (Fig. 20), some of which may be branched. Conidia of A. alternata are obclavate to elliptic or ovoid and dark, with both cross septa and longitudinal septa but little or no apical beak. The literature reveals that A. alternata is morphologically variable and taxonomically inconsistent, with the placement of many isolates under the common epithet alternata, incorrectly leading to a “collective species” concept.
Disease Cycle and Epidemiology
The disease cycle and epidemiology of Alternaria leaf spot has not been studied in sugar beet. However, inocula of both A. alternata and A. brassicae persist in debris of other diseased hosts and, thus, likely overwinter in sugar beet debris. Chlamydospore and microsclerotium formation in A. brassicae also may prolong survival, and seed transmission is known to occur for other hosts. Spores of both fungi are produced on foliar lesions and are readily dispersed by air currents. Periods of high humidity favor sporulation and, when followed by periods of reduced humidity, are likely to favor spore release from lesions. Sporulation and secondary spread also are favored by reduced sugar content in leaves. Cool, humid conditions favor infection, and wounding may enhance infection by A. alternata. Older plants are typically more susceptible to infection by Alternaria spp., with older leavesdeveloping lesionsbeforeyoungerleaves. Alternaria leaf spot development is most severe under field con-
ditions where beet yellows viruses, including Beet western yellows virus, Beet chlorosis virus, and Beet mild yellowing virus, have already weakened plants. Under these conditions, lesions usually first appear in interveinal areas of affected leaves. In addition to infecting sugar, leaf, and table beets, both Alternaria species have hosts in the family Brassicaceae (cruciferous crops and weeds) as well as in the families Solanaceae and Alliaceae. In addition, A. brassicae has a wide host range, including hosts in the families Fabaceae (legumes), Chenopodiaceae, Cucurbitaceae, Papaveraceae, and Poaceae (grasses), as well as others. There is a need to reexamine and confirm the identity and pathology of A. brassicae-like and A. alternata-like fungi that seemingly occur on such a great diversity of plants.
Management in sugar beet usually is not necessary because disease starts late in the season on foliage already senescent because of other factors. Proper irrigation and fertility practices reduce plant stress and the potential for disease development. Increased sugar yields have resulted from fungicide applications made to virus-infected plants. Comprehensive disease forecasting systems have not yet been developed, but models for predicting the sporulation of A. brassicae have been developed for other cropsandmay aidin developingdiseaseforecastingstrategies for sugar beet. There are fungicides registered for treating Alternaria spp. on leafy vegetables, including Swiss chard. Selected References CABI/EPPO. 1999. Alternaria brassicae. Distribution Maps of Plant Diseases, Map No. 353. CAB International, Wallingford, United Kingdom. Franc, G. D., Harveson, R. M., Kerr, E. D., and Jacobsen, B. J. 2001. Disease management. Pages 131-160 in: Sugarbeet Production Guide. R. G. Wilson, J. A. Smith, and S. D. Miller, eds. Univ. Nebr. Coop. Ext. EC01-156. McFarlane, J. S., Bardin, R., and Snyder, W. C. 1954. An Alternaria leaf spot of the sugar beet. Proc. Am. Soc. Sugar Beet Technol. 8(1):241-246. Rotem, J. 1994. The Genus Alternaria: Biology, Epidemiology, and Pathogenicity. American Phytopathological Society, St. Paul, MN. Simmons, E. G. 1992. Alternaria taxonomy: Current status, viewpoint, challenge. Pages 1-35 in: Alternaria: Biology, Plant Diseases and Metabolites—Topics in Secondary Metabolism, Vol. 3. J. Chelkowski and A. Visconti, eds. Elsevier Science Publishers, Amsterdam, the Netherlands. Simmons, E. G. 1999. Alternaria themes and variations (236-243) host specific toxin producers. Mycotaxon 70:325-369.
(Prepared by G. D. Franc) 13