Soybean Rust: Lessons Learned from the Pandemic in Brazil

SOYBEAN RUST Lessons Learned from the Pandemic in Brazil

José Tadashi Yorinori Glen L. Hartman, Maurício C. Meyer, Ademir A. Henning, and Cláudia V. Godoy, editors

CHAPTER 1

Introduction

The soybean plant (Glycine max [L.] Merrill) is a host to more than 100 diseases caused by bacteria, fungi, viruses, and nematodes (Hartman et al., 1999); but none is as devastating as soybean rust. Soybean rust is caused by two species of fungi that belong to the genus Phakopsora: Phakopsora meibomiae (Arth.) Arth. (syn. Malupa vignae [Bres.] Y. Ono, Buriticá & J. F. Hennen) and Phakopsora pachyrhizi Syd. (syn. Malupa sojae [Henn.] Y. Ono, Buriticá & J. F. Hennen) (Ono et al., 1992).

For a long period after the first description of the pathogen and its first report in 1902 (Kitani & Inoue, 1960), the disease that was recorded worldwide was attributed to a single species, P. pachyrhizi (CMI, 1975). More recently, based on morphological features of the urediniospores and the telia, two species have been clearly distinguished: P. meibomiae and P. pachyrhizi (Hennen, 1996; Ono et al., 1992). The causal agent of soybean rust recorded in the Americas prior to 2001 was later identified as P. meibomiae. On the other hand, P. pachyrhizi is more widespread (traditionally throughout the Eastern Hemisphere) and destructive, and more is published about this species. In order to distinguish between the diseases caused by the two species of Phakopsora since 2001, when the first epidemic of P. pachyrhizi was recorded in South America, the disease caused by P. pachyrhizi was named as “Asian” rust and the one caused by P. meibomiae as “American” rust (Yorinori & Morel Paiva, 2002). In this book the disease caused by P. pachyrhizi will be referred to as soybean rust, unless noted as caused by P. meibomiae.

Soybean rust occurred in Asia (most soybean-­producing countries) and Australia and was confined to those areas until 1994, when it was detected in Hawaii (Killgore, 1996). The first detection on the African continent occurred in Uganda in 1996 in experimental plots where it caused severe damage. In 1998, soybean rust was found in Zambia and Zimbabwe where severe damage was recorded (Levy, 2004). In 2001 it caused damage of epidemic proportions in South Africa (Pretorius et al., 2001).

In the same year that it was identified in South Africa, the first outbreak of soybean rust occurred in South America where it was found in Paraguay on March 5, 2001 (Morel Paiva, 2001).

Shortly thereafter, on May 25, 2001, soybean rust was found in the west and north (Londrina) of Paraná state, Brazil, on several second plantings and volunteer soybeans (Yorinori et al., 2002a).

Currently, with the potential of both rust species occurring in the same region, the distinction between them is aided by using molecular techniques (DNA analysis) and by morphological comparisons of urediniospores and telia (Frederick

et al., 2002; Ono et al., 1992). The tan or light-­brown lesion type (TAN) refers to a susceptible reaction observed with P. pachyrhizi, and the reddish-­brown lesion type (RB) refers to a tolerant/resistant reaction observed with P. meibomiae, as well as soybean lines with a gene conferring incompatibility with P. pachyrhizi. The most accurate distinction between species is made through DNA analysis.

A comprehensive review of soybean rust in the world up to approximately 1982 was made by Bromfield (1984) in his monograph on soybean rust. At that time, the rusts occurring on soybean in the Americas and in Asia were considered to be caused by P. pachyrhizi.

The importance of P. pachyrhizi is shown by its rapid dissemination throughout a region and the amount of loss the disease caused in Brazil (Yorinori, 2004; Yorinori et al., 2005).

Individual farms had yield reductions above 80%, thus making harvest noneconomical in many parts of Brazil. The disease was more damaging in the central region. In 2001, the area affected by soybean rust in Brazil and Paraguay was estimated at 10,000 ha. In the 2001/02 crop season the disease had expanded to almost all soybean-­producing regions of Paraguay while in Brazil about 60% of the soybean acreage had rust.

Losses in Brazil that season were estimated at 0.6 million tons (US$133 million; US$221/t) (Yorinori et al., 2002b). In the 2002/03 crop season, soybean rust had expanded to more than 90% of the soybean acreage in Brazil, causing losses estimated at 3.4 million tons or the equivalent of US$750 million (US$221/t) (Yorinori et al., 2005). In the 2003/04 crop season, losses were estimated at 4.6 million tons or the equivalent of more than US$1.2 billion (US$261/t) (Yorinori, 2004). Yield loss estimates, costs of rust control, and revenue losses based on grain losses for the period 2002 to 2009 have amounted to US$14 billion. As much as 36 MMT (more than a half-­season’s harvest) were lost due to rust during that period.

In 2009/10, the yield loss due to soybean rust was estimated at 4.1 million tons (US$1.3 billion) and the average cost of three fungicide applications per hectare amounted to US$1.1 billion. By adding revenue losses of 13% taxes on lost grain (US$165 million), the total economic losses caused by soybean rust were estimated at US$2.5 billion. Thus, assessment of the economic importance of soybean rust incurred in Brazil since the 2001/02 crop season through the end of the 2009/10 crop season was estimated to be total grain losses of 40 million tons (US$10 billion with average soybean market prices varying from US$132 to US$370/t in the period); disease control cost of US$7.1 billion (annual average of two to three sprays); and revenue losses (13% taxes) on lost grain of 5.2 million tons • 1

2 • Chapter 1

(US$1.3 billion). Therefore, it is estimated that the total economic impact of soybean rust in Brazil during the period 2002 to 2010 reached US$18 billion. The northern state of Roraima is the only region in Brazil where soybean rust has not yet been recorded.

In addition to Brazil and Paraguay, soybean rust was found in experimental plots at Missiones, Argentina, at the end of 2001/02 (Rossi, 2003). By April 2004, it had reached late-­ planted fields in most of the important soybean regions in Argentina (R. Rossi, personal communication). In Bolivia the disease was first detected in July of 2003 and caused severe losses on unsprayed second-­crop soybeans (Navarro et al., 2004).

At present, P. pachyrhizi has been disseminated to all soybean-­producing countries in the Southern Hemisphere. In the Northern Hemisphere, rust was reported in Colombia in 2004 (Frederick, personal communication). On November 10, 2004, rust was first found in soybean plots at Louisiana State University, Baton Rouge, U.S.A., and in neighboring commercial fields (R. Schneider, personal communication; Rogers & Redding, 2004). In the U.S.A., the disease is mostly confined to regions along the Gulf of Mexico. The high temperatures and mostly dry weather common in the southern U.S.A. are not conducive for epidemics, and disease dispersal to central and northern regions also seems to be hindered at times by the north-­to-­south wind patterns during parts of the soybean season. Therefore, rust spores from the South have not reached soybeans in the Midwest early enough to cause any damage.

In 2005, soybean rust caused severe losses in Mexico (Terán Vargas et al., 2007). Rust spores may come into Mexico through winds blown southward from soybeans grown in the neighboring U.S. state of Texas or from kudzu (Pueraria mon­ tana [Lour.] Merr. var. lobata [Willd.] Sanjappa & Pradeep) along the U.S. Gulf Coast or from local susceptible sources that could infect soybeans and other hosts. For example, Mexico has the most susceptible natural host of soybean rust known: the yam bean (jicama, Pachyrhizus erosus [L.] Urban; syns.

P. angulatis, P. bulbosus). Yam bean is native to Mexico and grown commercially (Terán Vargas et al., 2007). Thus, the much-­feared soybean rust has become a global soybean disease as P. pachyrhizi has spread rapidly from Asia to Africa to South America and is now present in North America.

Phakopsora meibomiae: First Rust of Soybean Found in Brazil Referred to as the “American” Rust Geographical distribution

Phakopsora meibomiae occurs naturally in the Americas and possibly in Africa (CMI, 1975). In the Americas, it occurs from Puerto Rico in the Caribbean (Vakili & Bromfield, 1976) to the southern state of Paraná, Brazil (Ponta Grossa) (Deslandes, 1979; Yorinori, 1989; Yorinori & Deslandes, 1985). According to Bromfield (1984), “It is quite likely that the P. pachyrhizi in Africa represents a forma specialis different from that in eastern Asia and from that in the Americas.”

Prior to the detection of P. pachyrhizi in 2001, the rust occurring in the Americas was attributed to a mild race of P. pachyrhizi (Vakili, 1978; Vakili & Bromfield, 1976). Following comparative studies on American and Asian specimens conducted in 1992, the American species of Phakopsora was named P. meibomiae and recognized to cause a rust disease of

low impact on soybean yield (Hennen, 1996; Ono et al., 1992; Sinclair & Hartman, 1996; Vakili, 1978).

The American rust recorded in South America (Bromfield, 1976, 1984) first was found on soybeans in Brazil in 1979 at Lavras, state of Minas Gerais (Deslandes, 1979). In the beginning, news of the discovery of rust was restricted and could not be openly discussed as it was feared that the news of its presence in Brazil could affect the marketing of Brazilian soybeans. Following the identification of the disease on soybeans in the experimental plots of the Agricultural Research Corporation of Minas Gerais/Federal University of Lavras, the Brazilian Agricultural Research Corporation (Embrapa) Soybean (Soja) took control of the problem and implemented a National Soybean Rust Research Project (NSRRP) to be conducted at Lavras. Thus, a national survey was initiated to determine the geographical distribution of what was then considered soybean rust in Brazil.

Dr. Josué Deslandes was coordinator of the rust project at Lavras. In addition to surveying for the disease in most of the soybean-­growing areas, several tests were performed at Lavras to determine the susceptibility of cultivated and naturally growing legume species to rust. This determined if a possible natural host was more efficient in producing spores than were soybeans. At the same time, testing of advanced soybean lines from Embrapa Soja and commercial varieties was carried out at Lavras. The host range studies identified the legume species that were more susceptible and that could serve for production of inoculum for field studies. This was done only at Lavras in an attempt to restrict the dissemination of the fungus elsewhere. At that time there were no commercial soybeans grown at Lavras.

Soon after publication about the presence of a rust on soybean at Lavras (Deslandes, 1979), similar survey work and other important studies on epidemiology and screening for resistance were initiated by the plant pathologists at the Federal University of Viçosa.

Field surveys in many important soybean-­producing regions of the country showed that rust was widely disseminated in the uplands of south-­central and southern Brazil (Table 1.1).

Rust was occasionally found on commercial soybeans planted around the Federal District (Brasilia), state of Goiás (Cristalina), and in the state of Minas Gerais (Triângulo Mineiro region). In the southern region, it was commonly found on a perennial relative of soybean, Neonotonia wightii (Arnott) Lackey, which is widely disseminated as volunteer plants or grown in association with pasture for grazing. On soybean, rust occurred from mid to late season in southern Londrina, Tamarana, Mauá da Serra, Faxinal, and Ponta Grossa in the state of Paraná. As shown in Table 1.1, the rust that occurred before 2001 was generally located in the high elevations (above 800 m in the Cerrado) and in the cooler southern regions of Brazil where the climate was milder throughout the year, i.e., average temperature below 25°C and high relative humidity.

In the state of São Paulo, P. meibomiae was found on N. wightii at Campinas, Jau, Aguai, and on the hillsides of Águas da Prata. In Minas Gerais, it occurred in the high elevations of Viçosa, Poços de Caldas, Águas da Prata, Monte Carmelo, São Gotardo, Uberlândia, and Lavras (Yorinori & Deslandes, 1984) (Table 1.1).

Host range

Phakopsora meibomiae infects a wide range of legume species: 42 species in 19 genera of leguminous hosts and 18 additional species in 12 genera by artificial inoculation (Hennen,

Introduction • 3

Table 1.1. Locations in Brazil where soybean rust caused by Phakopsora meibomiae was found before the discovery of P. pachyrhizi in 2001a State

County

Espirito Santo Federal District (Brasilia) Federal District (Brasilia) Mato Grosso do Sul Minas Gerais Minas Gerais Minas Gerais Minas Gerais Paraná Paraná Paraná Paraná Paraná Paraná Paraná Paraná São Paulo São Paulo

Guaçui Brasilia Brasilia Ponta Porã Lavras Poços de Caldas São Gotardo Viçosa Castro Cianorte Guarapuava Londrina Mauá da Serra Palmeira Ponta Grossa Tamarana Águas da Prata Campinas

Year found

Soybean

Other legumes

Altitude (m)

1979 1980 1980 1984 1979 1982 1982 1979 1983 1980 1983 1980 1983 1983 1983 1983 1982 1980

No Yes Yes Yes Yes No Yes Yes Yes No Yes No Yes Yes Yes Yes No No

Yes No No No Yes Yes Yes No No Yes No Yes No No No No Yes Yes

800 1,172 850 600 801 1,200 1,150 1,200 550 1,020 567 1,100 880 880 800 800 1,100 696

Data from Yorinori & Deslandes, 1985. Table courtesy J. T. Yorinori—© APS.

a

1996). The most common hosts are soybean, N. wightii, and several varieties and species of common bean (Phaseolus vul­ garis L.), lima bean, (P. lunatus L.), and hyacinth bean (Lablab purpureus [L.] Sweet, syn. Dolichos lablab) (Yorinori & Deslandes, 1984). Almost all legume species listed as a host for P. meibomiae are also considered a host for P. pachyrhizi.

Nevertheless, preliminary tests have shown that quite significant differences in reaction (susceptible and resistant) to both species of Phakopsora exist among the legume species (J. T. Yorinori, unpublished). Since both species may occur in the same area under mild climatic conditions, the differentiation of the two species of Phakopsora may be further evaluated by reaction types and tests on differential legume species. Nonetheless, the most conclusive proof is with DNA testing.

To further support this assumption, spores collected from rust lesions on soybeans and on N. wightii in March 2003 at Castro County, state of Paraná, by Dr. Reid D. Frederick of the USDA Agricultural Research Service (ARS) Foreign Disease-­ Weed Science Research Unit (FDWSRU) at Fort Detrick, Frederick, Maryland, were subjected to DNA analysis. He found that the causal agent of rust on soybeans was P. pachyrhizi and on N. wightii was P. meibomiae (R. Frederick, personal communication). Both species could also be occurring on soybeans, but only P. meibomiae was found on N. wightii. Thus, although N. wightii is listed as a host to P. pachyrhizi, it may not be a good source of inoculum of P. pachyrhizi.

In 1981, before the establishment of the distinction between P. meibomiae and P. pachyrhizi, Dr. Ken R. Bromfield, from the USDA/ARS FDWSRU at Frederick, Maryland, was invited to visit Brazil to discuss and update Brazilian plant pathologists on soybean rust (Fig. 1.1). During his visits, Dr. Bromfield collected rust samples from different legume species found at Lavras, Minas Gerais. One of these samples was instrumental

in differentiating the causal agent of the rust epidemic that occurred in Paraguay and Brazil in 2001.

A study on host range carried out by Cassetari Neto (1984) at Lavras in 1982–1983 (Fig. 1.2) showed that in addition to soybeans, P. meibomiae infection was more severe on several other legume species. This was especially true for certain varieties of common dry beans, broad beans (lima bean and Hyacinth bean), and N. wightii (Table 1.2). The latter is widely grown in association with grass for cattle grazing and has also become well established in many parts of south-­central Brazil as perennial volunteer plants. Phakopsora meibomiae has been most common on N. wightii in the south-­central Paraná state and in the hilly regions of Águas da Prata (São Paulo) and Poços de Caldas (Minas Gerais) (border between the states of

Fig. 1.1. Dr. Kenneth R. Bromfield (left) and Dr. Josué A. Deslandes (right) at

Lavras, Minas Gerais, 1981. (Courtesy J. T. Yorinori—­© APS)

4 • Chapter 1

Fig. 1.2. Experimental plots at Lavras, Minas Gerais used for resistance screening (left) and a resistant cultivar (right). (Courtesy J. T. Yorinori—­© APS)

Table 1.2. Legume species infected by Phakopsora meibomiae based on field inoculations: number of lesions/cm2; number of uredinia per lesion; sporulating uredinia; and latent perioda Species

Calopogonium mucunoides C. juncea Desmodium discolor Dolichos axilares Glycine max Lablab purpureus Macroptilium atropurpureum M. lathyroides Macroptiloma sp.

Neonotonia wightii Phaseolus sp.

Phaseolus bracteolatus P. lunatus P. lunatus var. macrocarpus P. vulgaris Rhincozia minima Teramnus uncinatus Vigna sp.

Vigna mungo V. marina a

Lesions per cm2

54 6 19 26 17 15 20 14 23 7 11 26 20 23 ND 13 3 8 94 26

Uredinia per lesion

b fg c–e bc c–f c–f c–e c–f c–e e–g c–g bc c–e cd c–g g d–g a bc

0.4 2.5 1.1 1.7 1.6 2.2 2.6 1.3 2.1 2.0 1.5 1.2 1.6 2.1 1.8 1.9 0.3 0.2 2.6 2.8

fg ab ef b–e b–e a–c ab c–e a–e a–e b–e d–f b–e a–d b–e a–e g g ab a

Sporulating uredinia (%)

66 68 63 77 99 89 92 39 89 96 77 78 84 88 86 72 32 13 82 78

d–f c–e d–f b–d a a–d a–c e–g a–d ab b–d b–d a–d a–d a–d b–d fg g b–d b–d

Latent period (days)

10 10 15 15 10 10 ND 10 10 15 10 10 10 10 10 10 20 10 10 10

Data from Cassetari Neto, 1984. Table courtesy J. T. Yorinori—© APS.

São Paulo and Minas Gerais) where it is also grown in association with grass for cattle grazing.

Soybean response to P. meibomiae

Lesions produced by P. meibomiae on soybean are characteristically of the RB type, even on more sensitive varieties (Figs. 1.3 and 1.4). When caused by P. pachyrhizi, these same RB lesions represent a resistant reaction. Thus, distinguishing between the two species of rusts based on lesion types, when

the variety is tolerant or resistant to P. pachyrhizi, becomes difficult or impossible in the field.

Since the outbreak of rust in all soybean-­producing regions of Brazil, it has become impossible to differentiate between the two rusts in the field based on foliar symptoms alone because of the similarity of lesion types of both rusts. Phakopsora mei­ bomiae infects and sporulates abundantly on susceptible soybeans, but it produces lesions that vary in color from light to dark RB. Typical TAN lesions are rarely seen. Phakopsora meibomiae is more pathogenic and sporulates better on most

Introduction • 5

Fig. 1.3. Leaflets infected by Phakopsora meibomiae showing RB-­type lesions. (Courtesy J. T. Yorinori—­© APS)

Fig. 1.4. Lesions of RB-­type reaction (left) and limited sporulation of Phakopsora meibomiae on soybean (right). (Courtesy J. T. Yorinori—­© APS)

dry beans and broad beans than on soybeans and is widely disseminated on N. wightii. On the other hand, TAN and RB lesions on the same variety may be caused by simultaneous infection by different races of P. pachyrhizi or by a mixed infection of the two species.

Disease severity and economic impact of P. meibomiae

Conspicuous amounts of defoliation were occasionally observed but never repeated on soybeans over two consecutive seasons. Most often the severe foliar symptoms and damage were caused by other diseases, especially brown spot (Septo­ ria glycines Hemmi) and Cercospora leaf blight (Cercospora kikuchii [T. Matsumoto & Tomoy.] M. W. Gardner). These additional diseases were responsible for important early leaf blighting and defoliation. Phakopsora meibomiae, similar to brown spot and Cercospora leaf blight, is more common at the end of the season on second crop soybeans (fall/winter) and on volunteer plants.

From its first report by Deslandes (1979), rust caused by P. meibomiae was most conspicuous in southern Paraná (Ponta Grossa and Tamarana) in March, 1983. In 1985, it was quite severe on experimental plots and some commercial varieties grown at the Estação Experimental Trigo Muniz maintained by

the former Cooperativa Agricola de Cotia–CC at São Gotardo, state of Minas Gerais (Yorinori & Deslandes, 1984). Again, in the 1987/88 crop season, the first measurable yield loss occurred at the same experimental station and in some commercial fields in the vicinity. Local estimates placed yield losses in the 1987/88 season as high as 40% (Yorinori, 1989) (Fig. 1.5).

During this period, the occurrence of severe P. meibomiae rust in one year and total absence in the next was intriguing.

In several of the recorded regions its occurrence was erratic.

Following the severe outbreak at São Gotardo, Minas Gerais, in 1985 and 1987/88, rust surveys carried out the following year did not show its presence in any of the fields. Apparently, weather conditions alone could not have been responsible for the dramatic change in the presence/absence of the disease from one year to the next; however, the reason was never elucidated.

Telia and teliospore formation by P. meibomiae

Teliospores were frequently found on most susceptible hosts (hyacinth bean, soybean, N. wightii, lima bean, common bean, and Rhynchosia minima [L.] DC.) at Lavras during the winter.

Telia were produced in old lesions mixed with the uredinia and developed like hardened light-­brown to reddish-­brown jelly (Figs. 1.6 and 1.7). Cross sections of the telia showed a compact

6 • Chapter 1

Fig. 1.5. Defoliation caused by Phakopsora meibomiae at São Gotardo, Minas Gerais, on experimental plots (left) and in the field (Cultivar FT-­Seriema) (right), 1987/88 crop season. (Courtesy J. T. Yorinori—­© APS)

Fig. 1.6. Telia (left) and teliospores (right) of Phakopsora meibomiae on soybean. (Courtesy J. T. Yorinori—­© APS)

Fig. 1.7. Telia (dark) (left) and teliospores (right) of Phakopsora meibomiae on Dolichos lablab. (Courtesy J. T. Yorinori—­© APS)

Introduction • 7 mass of cells forming three to five layers of teliospores (Figs.

1.6 and 1.7).

In addition to the predominant RB lesion types, P. meibo­ miae also differed from P. pachyrhizi in the requirement of milder temperatures for disease development, in some morphological features of the urediniospores, and by its telia and teliospore configuration. Telia of P. meibomiae have one to four and, rarely, five layers of teliospores. The spore wall has a light brown to cinnamon color with walls 1.5 to 2.0 µm thick; the apical wall of the outer layer reaches up to 6 µm. In contrast, P. pachyrhizi telia have two to seven teliospore layers; spore walls are a pale brownish-­yellow color and are of more uniform thickness and with an outer apical spore wall that varies from 1 to 3 µm (Bonde & Peterson, 1996; Hennen, 1996).

The Payback from Investment in Training and Research Fearing that the soybean rust found at Lavras could cause severe losses in soybean production in Brazil, the NSRRP was established by Embrapa Soja in 1980. While most research work was to be confined at Lavras in order to prevent the spread of the disease to other regions, a national survey program was initiated. In the same year, while finishing the requirements for the PhD degree in plant pathology at the University of Illinois, I obtained permission from the Brazilian government to spend 1 week in training under Dr. Bromfield at the USDA/ ARS FDWSRU at Fort Detrick, Frederick, Maryland. The 1 week spent with Dr. Bromfield and the staff at Fort Detrick was most valuable for the establishment of the rust project in Brazil.

In a very short time, I could conceptualize the magnitude of the challenge represented by P. pachyrhizi. The damage it caused on inoculated plants in the containment facility was unparalleled to any other foliar disease of soybean. Besides the techniques learned on handling the rust fungus, the information on the genetic variabilities, both of the soybean germplasm and of the pathogen, were most valuable. In addition, the information on epidemiology of P. pachyrhizi kindly provided by Dr. Morris R. Bonde, Dr. J. S. Melching, and Dr. Gary L. Peterson became invaluable for establishing guidelines for management of soybean rust in Brazil. Upon completion of studies at the University of Illinois, I returned to Brazil and was assigned to coordinate the NSRRP. In 1981, Dr. Bromfield was invited to Brazil to do an extensive survey. He visited several locations where both soybeans and other legumes were grown, especially in the high elevations where rust was most likely to be found (Table 1.1). The places visited included Campinas (Agronomic Institute), Caxambú, Águas da Prata, Poços de Caldas, Lavras, São Gotardo, and Viçosa. Dr. Bromfield collected several leaf samples from various locations with the required permits. He performed greenhouse tests at Fort Detrick and compared Asian isolates from Taiwan and the Philippines with the Brazilian isolates to show that these isolates from Brazil were not P. pachyrhizi.

These samples were kept and preserved in liquid nitrogen to become instrumental in distinguishing and ensuring that the new outbreak of rust that occurred in Paraguay and in Brazil in 2001 was due to P. pachyrhizi and not P. meibomiae. Comparative molecular studies were done on two samples kept at Fort Detrick: one from Dr. Bromfield’s collection from Brazil, 1981, and the other collected by Dr. Reid Frederick of USDA/ARS

FDWSRU, Fort Detrick, Maryland, in 2001, from fields that had rust in Paraguay and Brazil. These studies left no doubt that the new rust epidemic was caused by P. pachyrhizi.

Soybean Rust Caused by Phakopsora pachyrhizi The importance of being prepared

Long before P. pachyrhizi hit the first soybean fields in the Americas, I had gathered a large amount of information about the disease from the literature, from personal contacts with international experts in their day-­to-­day work, and from many years of experience working with P. meibomiae.

Soybean rust had been a major concern since the early studies of soybean diseases in Brazil. In 1974, when I had the responsibility to establish and coordinate the soybean research program at the most modern research facility (under construction), the Agronomic Institute of the State of Paraná (IAPAR), two major soybean diseases were included as potential threats to the future of soybean production in Brazil: soybean rust (P. pachyrhizi) and soybean cyst nematode (SCN) (Heterodera glycines). Neither pathogen was present in Brazil at the time, but seeds of resistant germplasm were needed for the future germplasm bank. SCN was first found in central Brazil in 1992 and P. pachyrhizi was found in 2001.

In 1974, IAPAR did not have a single seed to start the program, but by the end of the year we had one of the most renowned soybean breeders, Dr. Romeu A. S. Kiihl, leading the breeding program. A reasonable collection of varieties and germplasm to start the program was received from Instituto Agronômico de Campinas (Campinas Agronomic Institute) from the state of São Paulo. In 1982, together with Embrapa Soja breeder Dr. Leones Alves de Almeida, we had the opportunity to travel to Japan, Taiwan, and Thailand in order to see soybean rust in action at its place of origin.

In Japan, soybean rust was quite severe at Shizuoka Prefecture on soybeans planted after rice (Fig. 1.8). In a later visit to Japan in 1987, we were told that the soybean rust fungus does not survive in the winter, and in order to cause damage to soybeans, the inoculum must be blown by the typhoon wind early in the season from more tropical or subtropical regions in Asia. If the inoculum reached the soybean fields by June or July, then epidemics of rust were likely. Thus, as the occurrence of the disease in Japan depended on early arrival of inoculum coming from more tropical or subtropical regions in Asia that was blown by a typhoon, soybean rust was a problem only once every 8-­10 years (Ishii, personal communication).

In Taiwan, we visited the Asian Vegetable Research and Development Center (AVRDC) at Shanwai (Fig. 1.9) and met with Dr. C. C. Yeh (Fig. 1.10), an acquaintance from the University of Illinois who also pursued his PhD degree with Dr. James Sinclair. Dr. Yeh showed us his work on the pathogenic variability of P. pachyrhizi for which he used the detached leaf technique. It was amazing to see the great pathogenic variability of the fungus (Table 1.3).

Dr. Arnold Tschanz, a USDA expert who was screening for rust resistance at AVRDC, showed us the extent of damage rust could cause to a susceptible soybean. Unsprayed plots had practically no pods (Fig. 1.11). Dr. Tschanz showed us his plots where there was a large collection of germplasm and advanced breeding lines under screening for resistance. He mentioned

8 • Chapter 1

Fig. 1.8. Soybean plants with severe rust growing after paddy rice at Shizuoka Prefecture (left) and yellow leaves with severe rust (right), Sept., 1982. (Courtesy J. T. Yorinori—­© APS)

Fig. 1.9. Entrance to the Asian Vegetable Research and Development Center (left) and the main administration building (right), Taiwan. (Courtesy J. T. Yorinori—­© APS)

Fig. 1.10. Drs. C. C. Yeh, Leones A. de Almeida, and Tadashi Yorinori (left) and a detached leaf technique (right) for race identification of Phakopsora pachyrhizi at the Asian Vegetable Research and Development Center, 1982. (Courtesy J. T. Yorinori—­© APS)

how difficult it was to find a reliable source of resistance that could withstand the variability of the pathogen.

Dr. Shanmugasundaram (Sundar), principal breeder, soybean project leader at AVRDC and responsible for the international cooperative program, showed us his research efforts on the development of vegetable soybeans. He was successful in developing high-­yielding varieties grown in succession/rotation

with rice in the paddy fields but had not been successful in developing long-­lasting soybean rust resistant varieties (Fig. 1.12).

In addition to the year-­round production of legume crops, several climbing legume plants were grown around fences of the experimental field (Fig. 1.12) to contribute continued sources of inoculum for germplasm and breeding line evaluations for soybean rust.

Introduction • 9

Fig. 1.11. Severely affected plot between two healthy looking plots at the Asian Vegetable Research and Development Center (left); Drs. Leones A. de Almeida and

Arnie Tschanz (right) looking for viable seeds in a plot badly affected by Phakopsora pachyrhizi. (Courtesy J. T. Yorinori—­© APS)

Fig. 1.12. Dr. Sundar showing Dr. Leones A. de Almeida one of his recently released varieties under continuous soybean cropping system (left); several legume species surrounding the experimental plots (right) at the Asian Vegetable Research and Development Center, 1982. (Courtesy J. T. Yorinori—­© APS)

Table 1.3. Races of Phakopsora pachyrhizi identified in Taiwan in 1982a Reactions of differential soybean linesb Race

1 2 3

ANKUR

TN4

TK 5

PI 230971

PI 200482

TAN TAN RB

TAN TAN RB

TAN TAN RB

TAN RB RB

TAN TAN TAN

Data from Yeh, 1985. Table courtesy J. T. Yorinori—© APS. TAN (tan colored) = susceptible reaction; RB (reddish-brown) = resistant reaction.

a

b

A most amazing experience was to see a few plants of a recently released variety growing at the entrance of the main building surrounded by concrete pavement. It was surprising that the soybean rust was doing well but the plants were suffering both from the heat and the rust (Fig. 1.13).

From Taiwan, the trip extended to Thailand. In Bangkok we first visited with Dr. Udom Pupipat, plant pathologist and professor at Kasetsart University, who introduced us to the plant pathology staff. We had the opportunity to visit the university’s

experiment station about a 1 hour drive from Bangkok. Many breeding lines and commercial varieties were being tested for yield performance and disease reaction. No rust was found on soybeans, but there was severe defoliation due to bacterial pustule (Xanthomonas citri pv. glycines) and wild fire (Pseudo­ monas savastanoi pv. glycinea) which was mistakenly attributed to anthracnose. The effect on yield was devastating, being comparable to a severe case of soybean rust. The absence of rust at the university’s experiment station could be attributed to the almost unbearable heat at the time.

From Bangkok, we flew to Chiang Mai where we spent a week with Dr. Montha Nuntapunt, the pathologist in charge of testing the advanced breeding lines developed by the breeders from Kasetsart University (Fig. 1.14). She also cooperated with Drs. Sundar and Tschanz from AVRDC to test their advanced lines and germplasm. The rust outbreak at Chiang Mai was not yet at its peak, but most plots were yellowing from the midportion of the canopy to the bottom. Therefore, the severity of rust was very high and showed significant potential damage at Chiang Mai. Compared to Bangkok, which is almost at sea level, Chiang Mai is located in the higher elevations (more than 1,000 m above sea level) in northern Thailand. Besides being grown under high moisture of the paddy fields following the rice crop, the climate was more favorable for rust development.

10 • Chapter 1

Fig. 1.13. Front (left) and side view (right) of soybean plants severely infected by rust in front of the Asian Vegetable Research and Development Center administrative building. (Courtesy J. T. Yorinori—­© APS)

Fig. 1.14. Dr. Montha Nuntapunt showing a rust resistant plot to Dr. Leones A. de Almeida (left); severe rust on a susceptible plot (right). (Courtesy J. T.

Yorinori—­© APS)

Some of the soybean germplasm showed good resistance to rust.

The visits to Japan, Taiwan, and Thailand in 1982 were most useful and gave us a lasting impression about the severity of the disease and that high yield losses would render soybean production unfeasible if proper care was not taken to control it.

Upon returning to Brazil, our contacts with experts met during the trip were continued and became most valuable when the real P. pachyrhizi appeared in 2001.

Development of P. pachyrhizi in the world

Originally from Asia (China) and traditionally present in most Asian countries and Australia, soybean rust was always considered the most serious disease that could affect soybeans (Bromfield, 1976).

In 1994, P. pachyrhizi was first found outside the Asian countries on small plantations in Hawaii (Bonde & Peterson, 1996; Killgore, 1996). Just 2 years later (1996) it was found in the African Continent where it caused severe damage on experimental plots in Uganda (Kawuki et al., 2003). The next countries to be affected were Zambia and Zimbabwe in 1998. In both countries the disease was devastating from the first year of de-

tection (Levy, 2004). In 2001 it was found in South Africa, causing severe damage the first year (Caldwell & McLaren, 2004; Pretorius et al., 2001). In the same year it was found in Paraguay and southern Brazil in March and May, respectively (Morel Paiva, 2001; Yorinori & Morel Paiva, 2002). Since then most soybean-­producing countries of the Americas, including Argentina in 2003 (Rossi, 2003), Bolivia in July 2004 (Navarro et al., 2004), and the U.S.A. in November 2004 (Rogers & Redding, 2004; Schneider et al., 2005), have reported soybean rust.

Soybean rust was found in the U.S.A. in experimental plots at Louisiana State University and in neighboring commercial fields in Baton Rouge, Louisiana. In 2005 (January 24 through December 31), soybean rust was found at 139 locations on soybean and kudzu hosts in eight states (www.sbrusa.net, 2.27.2006). In 2006, 231 soybean fields were found with rust and the disease was discovered at an additional 43 sites on kudzu in 15 states; in 2007, rust was detected in 324 counties in 19 states in the U.S.A. and one province of Canada; in 2008, soybean rust was found in 392 counties; and in 2009, a record number of counties (564) in 16 states had soybean rust (sbr.ipmpipe.org/, 11.30.2009).

Storms and tornadoes in the southern U.S.A. and high temperatures and little rain in the main U.S. soybean production

Introduction • 11

Fig. 1.15. Dew on soybean leaves at Pesotum, Champaign County, Illinois, following almost 1 month of drought, July 23, 2005. (Courtesy J. T. Yorinori—­© APS)

areas may have limited distribution of the disease in the 2005 crop season, as there was little movement of rust to the northern states. Perhaps the most important weather factors reducing rust dispersal into the main soybean production areas of the Midwest in the U.S.A. are drought conditions, either locally in areas where rust occurs or more regionally, or because of wind direction. Thus, although rust is present year-round on kudzu and/or volunteer soybeans along the Gulf of Mexico from Texas to Florida, the patterns of drought and possible wind direction may prevent the rust spores from reaching the corn/soybean belt region early enough (before late August) to cause significant damage. Nevertheless, farmers must keep monitoring for rust and follow the weather forecast continuously until the crop reaches a safe growth stage. A weather pattern that blows south to north from mid-­July to late August could have the potential to favor the development of a soybean rust epidemic in the Midwest. In July 2005, following a long period of drought in Champaign County, Illinois, I observed dew formation that was more than adequate for rust establishment, even under these drier conditions (Fig. 1.15).

Great effort and considerable money were invested in research, training, and education with regards to soybean rust.

Investments also were made for enforcement of very strict regulations, almost as tight as military discipline, regarding procedures for actions at newly identified sites of infection. A most efficient alert system was developed for quick access to follow the annual development of soybean rust through a joint effort of all private and public offices related to soybeans as never previously seen in the U.S.A. Nevertheless, as the severe threat did not materialize in the initial 2 years after introduction, enthusiasm abated, and financial support and research efforts dwindled. However, the site that monitors observation of soybean rust in the U.S.A. is still active (https://soybean.ipmpipe. org/soybeanrust/).

Soybean rust was first found in Mexico in 2005 (Terán Vargas et al., 2007) and caused severe damage in the states of Tamaulipas and Vera Cruz, where 80% of the soybeans are grown.

According to Dr. J. Avila Valdez (CIRNE-­INIFAP, Mexico) (personal communication), rust spores are blown toward Tamaulipas by southward wind from kudzu growing along the Gulf of Mexico and early planted soybeans with rust in Texas. In 2005, soybean rust caused severe yield losses, but no rust was found the following year (2006) when about 70% of soybean

production was lost to severe drought. In 2007, rust was found in two states: Tamaulipas (Altamira County) and Veracruz (Tampico County) (www.sbrusa.net, 19.12.2007). In 2009, rust was found in the states of Tamaulipas (Gonzales, Velle Hermoso, Altamira, El Mante, and Rio Bravo counties), Chiapas (Mazatan and Tapachula counties), and Veracruz–Llave (Papantha and Tampico Alto counties). The disease occurred late in the 2009 season and no losses were recorded (sbr.ipmpipe.org/, 11.30.2009).

The worldwide dissemination of P. pachyrhizi shows that as soybean cultivation expanded from the eastern (Asian) to the western (American) continents, after more or less time, P. pachyrhizi followed the movement of the crop. Being disseminated by wind, the fungus is able to overcome hurdles to long-­ distance spread. All it requires for establishment is a suitable host, adequate environment, and urediniospores (inoculum) to move with the wind. The closer the source of inoculum is to the cultivated soybean, the faster the disease develops on the crop.

Conclusion Since the much-­feared disaster expected for soybean production in Brazil did not materialize from the rust on soybean found at Lavras in 1979, because of its erratic behavior from year to year, and the high cost of running the NSRRP, Embrapa Soja decided to terminate the program in 1989. This action was also followed at other research centers. But payback for those 10 years of often unappreciated effort to learn more about soybean rust, which included money spent at Lavras and on international travel to observe and learn about soybean rust, came when P. pachyrhizi was identified in Brazil in 2001. It then became evident that the knowledge and experience gained in handling P. meibomiae at Lavras and the exchange of information abroad was a great investment made in anticipation of the real problem that was now present.

The situation changed dramatically in 2000/01 with confirmation that the rust found in Paraguay and in southern Brazil was caused by P. pachyrhizi. This discovery changed the course of history. The devastation it caused initially and is still causing, in addition to its adaptability to a wide range of environmental conditions, reassured that what had occurred before 2000/01 did not have anything to do with P. pachyrhizi. The

12 • Chapter 1

Fig. 1.16. Dr. Kenneth R. Bromfield with a trainee student (Jean) from the Philippines (left) in the containment facility at Frederick, Maryland (right), Sept., 1980. (Courtesy J. T. Yorinori—­© APS)

Fig. 1.17. Lesion types TAN (isolate from Taiwan) and RB (isolate of Phakopsora meibomiae from Brazil) (left). RB and TAN-­type lesions of germplasm PI 230971

(left) and variety BRS 154 (right), April 27, 2005. (Left, Courtesy K. R. Bromfield—­Reproduced by permission. Right, Courtesy J. T. Yorinori—­© APS)

Table 1.4. Pathogenic variability among isolates of Phakopsora pachyrhizi from Taiwan, the Philippines, Australia, and India and isolates of probable P. meibomiae from Puerto Rico and Brazila Reactions of differential soybean linesc Raceb

Origin of isolate

Wayne

PI 200492

Ankur

PI 230970

PDRL – 1 PDRL – 1 PDRL – 2 PDRL – 2 PDRL – 2 PDRL – 3d PDRL – 3d PDRL – 4

Taiwan – 72 – 1 Philippines – 77 –1 Australia –72 – 1 Australia – 79 – 1 India – 73 – 1 Puerto Rico, Comp.

Brazil – 80 – IA Taiwan – 80 – 2A

TAN TAN TAN TAN TAN RB RB TAN

TAN TAN 0 0 0 RB RB TAN

TAN TAN RB RB RB RB RB TAN

RB RB RB RB RB RB RB TAN

Data from Bromfield, 1984. Table courtesy J. T. Yorinori—© APS. Race designation given before causal agents of soybean rust had been distinguished into two currently known species: P. pachyrhizi and P. meibomiae. c TAN (tan colored) = susceptible reaction; RB (reddish-brown) = resistant reaction; 0 = immune. d Puerto Rican and Brazilian isolates must have been P. meibomiae. a

b

Introduction • 13 newly found pathogen expressed the full potential for damage foreseen by specialists that dealt with the disease in Asia and in Africa. So, despite the fact that a large sum of public money had been spent on a disease problem that was not a real challenge at the time, the investments yielded great dividends later when it was realized that this new introduction was P. pachyrhizi.

The development and extent of damage caused by soybean rust in the Americas was probably far beyond what the most experienced researchers, such as Dr. Bromfield, Dr. Edgar E. Hartwig, Dr. Tschanz, and many others, could have ever imagined. From the first detection of the disease in Paraguay and southern Brazil, it took just 3 years (March 2001 to November 2004) to expand throughout the entire South American continent and reach the United States. The effort and expenditures of more than 40 years of rust research in Asian countries, and particularly at the USDA/ARS FDWSRU in Frederick, Maryland (Fig. 1.16), were certainly to great avail in providing background information for better understanding the disease epidemiology, pathogenic variability of P. pachyrhizi, and sources of host resistance to the pathogen (Fig. 1.17; Table 1.4).

Pathogenic variability of P. pachyrhizi had been shown by several researchers in different parts of the world (Bromfield, 1984; Poonpogul, 2004; Yamaoka et al., 2002; Yeh, 1985) (Fig. 1.18; Table 1.4). This variability may be the main reason that resistant soybean varieties developed in the past lasted for only a short time.

This book is an account of the various facets of soybean rust (P. pachyrhizi) in Brazil from its introduction in 2001 to the crop season of 2009–2010. Included in these pages are its evolution and economic impact; the difficulties encountered in controlling the disease, either by chemical means or by crop management; and the importance of volunteer soybeans and multiple cropping to the survival of the fungus from one crop season to the next, i.e. the green bridge. Also included are the events leading to the enactment of regulatory measures (state

Fig. 1.18. Distinct RB-­type lesions caused by Phakopsora meibomiae (isolate BR-­80-­1 from Brazil) and TAN-­type lesions caused by Phakopsora pachyrhizi (isolate from Taiwan) on the same leaf. (Courtesy K. R. Bromfield—­Reproduced by permission)

and federal law) to establish a 90-­day host/rust free period (vazio sanitário) before the first sowing of each summer crop; the importance of climatic condition and its impact on the irregularity of rust development from year to year; the efficacy and failure of chemical control due to excess rain and the use of reduced fungicide dosage and inadequate (cheaper and unreliable) products in an attempt to reduce cost; and the establishment of volunteer cooperative programs such as the Antirust Consortium for rust alert (www.consorcioantiferrugem.net). Finally, uniform fungicide trials and recommendations, current disease management procedures, and state-­of-­the-­art strategies for developing rust-­resistant varieties are also discussed.