Management Options for Soybean Rust; Resistance and Fungicides. Monte R. Miles USDA-Agricultural Research Service Department of Crop Sciences National Soybean Research Center University of Illinois, Urbana, IL www.soydiseases.uiuc.edu

PHAKOSPORA PACHYRHIZI OBLIGATE PARASITE UREDINIOSPORES NO ALTERNATE HOST IS KNOWN DIRECT PENETRATION INFECTION CYCLES IN 5 TO 7 DAYS Introduction The identification of Asian soybean rust in Paraguay in 2001(Morel and Yorinori, 2002) and its spread to over 90% of the soybean production in Brazil through the 2003 season has heightened the awareness that this disease will soon be a threat to production on the continental USA. With the yield losses this disease can cause it will have a big impact on profitability of soybean production. Asian soybean rust, caused by Phakopsora pachyrhizi, is an obligate parasite; it needs living tissue to survive. Urediniospores are the main spore stage. Teliospores and basidiospores have been produced but are not part of the disease cycle, since there is no known alternate host for basidiospores to infect. The pathogen penetrates directly, unlike the pathogens that cause rusts of wheat and corn. The infection process is not influenced by host surface features, stomata are not important in infection. Most parts of the soybean plant are infected, including the coleoptiles, leaves, petioles, stems and seedpods. C. STONE

São Desidério, Roda Velha, BA, March 8, 2003 J. T. Yorinori

Photo: M. Assunção (Embrapa Soja/CTPA)/José Nunes Jr (CTPA); Campo Alegre, GO

Management of Soybean Rust Short-term solutions Fungicides Long-term solutions Host resistance Specific resistance Partial resistance Yield stability Combination of fungicides and resistance

RESISTANCE TO SOYBEAN RUST SPECIFIC OR SINGLE GENE RESISTANCE PARTIAL OR RATE REDUCING RESISTANCE YIELD STABILITY OR TOLERANCE

Initial Screening of Germplasm Initial studies 1961 ≈ 2,800 accessions screened in Taiwan (U.S collection) 1970 ≈ 4,000 accessions screened in India (U.S. collection) 1975 ≈ 1,675 accessions (MG V-X) screened in Taiwan (AVRDC) From these studies, sources of resistance were found and the inheritance of resistance was characterized

Specific Resistance Hartwig and Bromfield 1983 Showed that three soybean lines each carried a single dominant gene conferring specific resistance Each gene was found to be at a different locus Hartwig 1986 Identified a fourth major gene for resistance

Host Response Immune reaction - hypersensitive reaction with rapid cell death near the infection site without sporulation - rarely seen Resistant - red-brown (RB) reaction, lesions may or may not develop into sporulating pustules Susceptible - Tan lesions that develop into sporulating pustules C. STONE

GENE ACCESSION FOUND LOST Rpp1 PI200492 1960-62 1966 The resistance in Ankur, identified in the early 1970’s was lost in the late 1970’s , providing another example of the diversity in virulence seen in P. pachyrhizi populations overcoming single gene resistance. Only Bing Nang, the source of the Rpp4 gene, has not been reported to be defeated, although our observations both in the field in Paraguay and greenhouse inoculation tests indicate that it is susceptible to some isolates.

Virulence diversity of P. pachyrhizi In Australia, 8 isolates were separated into 6 races using wild Glycine species as the differentials. Native populations of wild Glycine spp show differential responses. In China, nine isolates that had a susceptible reaction on soybean were separated into 6 phenotypes using asparagus bean, kidney bean and short podded yam bean.

Virulence diversity of P. pachyrhizi In a screen of 42 single spore isolates from Taiwan, 9 races were identified using 11 G. max resistant sources. No resistant source was effective against all isolates

VIRULENCE IS DIVERSE AND COMPLEX PHYSIOLOGICAL SPECIALIZATION HAS BEEN SEEN ON MANY LEGUMES, THE WILD GLYCINE RELATIVES OF SOYBEAN, AS WELL AS ON SOYBEAN ACCESSIONS Physiological races of P. pachyrhizi were first described in 1966 when a set of nine single urediniospore isolates were inoculated onto six soybean and five legume accessions . The reactions of the nine isolates were similar on all six of the soybean genotypes, but six pathotypes were identified based upon their reactions on the legume accessions. The first example of virulence diversity on soybean cultivars was described in Queensland, Australia where one rust isolate was found to be virulent on the cultivar ‘Willis’ but avirulent on the accession PI 200492, while a second isolate was virulent on both soybean genotypes. Several other studies have also shown considerable variation in virulence among isolates from the same field, as well as isolates collected from wide geographical areas . The summary on virulence is that it is diverse and complex. Not only is there physiological specialization in the interaction with soybean but it is also known to occur within the other legume species as well.

PARTIAL RESISTANCE REDUCES THE RATE OF AN EPIDEMIC BY SLOWING DOWN PATHOGEN USUALLY NOT A SINGLE GENE USUALLY NOT RACE SPECIFIC NOT A +/- TYPE OF EVALUATION EVALUATED OVER TIME GROWTH STAGE IMPORTANT

HOW DOES PARTIAL RESISTANCE OR “SLOW RUSTING” WORK? REDUCES INFECTION FREQUENCY- FEWER LESIONS INCREASES LATENT PERIOD - PATHOGEN NEEDS A LONGER TIME TO PRODUCE UREDINIA AND SPORES REDUCES SPORE PRODUCTION- FEWER UREDINIA AND FEWER SPORES / UREDINIA DIFFICULT TRAITS TO WORK WITH

EXAMPLE OF PARTIAL RESISTANCE - PUSTULE COUNTS Entry Pustules per plant Pustules per leaf Pustules at node 7 AGS 129 1,776 41 104 AGS 181 3,849 130 87 GC 82345-20-2 5,934 168 176 GC 82349-6-1 2,108 49 150 KS 8 2,715 76 107 SRE C-56A 803 23 25 SRE C-56E 709 19 29 SRE D-14C 2,159 58 17 SRE D-14D 2,100 54 51 G. L HARTMAN

HOW WILL PARTIAL OR “SLOW RUSTING” RESISTANCE BE EVALUATED ? DISEASE SEVERITY OVER TIME ESTIMATED PER PLOT AREA AFFECTED, DEFOLIATION, GREEN LEAF AREA PATHOGEN REPRODUCTION OVER TIME PUSTULE COUNTS, SPORE PRODUCTION, LATENT PERIOD GROWTH STAGE IS IMPORTANT RELATIVE LIFE TIME (0-100%) Partial resistance, or rate reducing resistance, is also known in soybean . Lines with partial resistance in field evaluations were rated as moderately resistant since fewer lesions developed on plants throughout the season. In greenhouse studies, host-pathogen combinations that resulted in RB reaction types tended to have longer latent periods, lower rates of increase in pustule number over time, and smaller lesions compared with susceptible interactions that resulted in a TAN reaction type .

Yield Stability Needs to be done with adapted germplasm Relative yielding ability of soybeans under stress from rust Compare yields between fungicide-protected plots and non-protected plots Yield stability assessment - Needs to be done with adapted germplasm

Yield Loss Differences 20 40 60 80 100 LOW YIELD STABILITY Yield loss (%) MOST YIELD STABILITY 1 2 3 4 5 6 7 8 9 10 11 12 Soybean entry

GOIAS Photo: Mauricio Assunção – Embrapa Soja/CTPA; Campo Alegre, GO

MATO GROSSO Primavera do Leste, MT: 21.02.03

Fungicides will be the primary tool to control Asian soybean rust in the near future. The primary tool in the control of the disease will be the use of fungicides. Single gene resistance has not been durable, partial resistance has been difficult to work with, leaving tolerance or yield stability as the selection method used in breeding programs. Tolerance is defined as yield stability in the presence of the disease compared to plots protected by fungicides (Hartman, 1995). Cultural practices have not been shown to be effective in control of the pathogen; recommendations were inconsistent and varied by location. The most effective practices were avoidance or were practices that maximized yields in the absence of the disease.

FUNGICIDES REGISTERED FOR USE ON SOYBEAN AND LABLED FOR CONTROL OF SOYBEAN RUST CHLOROTHALONIL BRAVO (SYNGENTA) ECHO ( SIPCAM AGRO) AZOXYSTROBIN QUADRIS (SYNGENTA)

FUNGICIDES ON THE SECTION 18 EMERGENCY EXEMPTION REQUEST MYCOBUTANIL * PROPICONAZOLE * PYRACLOSTROBIN PYRACLOSTROBIN + BOSCALID ** TEBUCONAZOLE TETRACONAZOLE TRIFLOXYSTROBIN + PROPOCONIZOLE * APPROVED BY EPA, ** BOSCALID IS REGISTERED

ALL FUNGICIDES ARE NOT THE SAME CURATIVE ABSORBED TRANSLOCATES KILLS FUNGAL TISSUE USE AFTER INFECTION TRIAZOLES PROTECTANT +/-ABSORBED +/-TRANSLOCATE PREVENTS INFECTION OR SPORULATION USE BEFORE INFECTION STROBALURINS AND CHLOROTHALONILS

FUNGICIDE EFFICACY TRIALS IN SOUTHERN AFRICA AND SOUTH AMERICA EVALUATE FUNGICIDES THAT ARE LABLED OR ON THE SECTION 18 REQUEST COMPARISON OF 2 AND 3 APPLICATIONS WITH FIRST APPLICATION SOON AFTER FLOWERING Fungicide Efficacy. Many fungicides have been evaluated to control soybean rust. Early research from Asia indicated that mancozeb was effective (Hartman et al., 1992). Other compounds available at the time were compared to mancozeb and were effective, but results varied by test (Table 1). More recently, fungicide trials in India (Patil and Anahosur, 1998) and Southern Africa (Levy et al., 2002) have identified several triazole compounds and triazole mixes. Among the more effective were flusilazole + carbendazim, difenoconazole, and triadimenol. M. Miles

RECCOMENDATIONS FOR CHEMICAL CONTROL BRAZIL AND SOUTHERN AFRICA ARE THE SOURCES OF INFORMATION FORMULATIONS WE WILL HAVE WILL DIFFER FROM BRAZIL AND AFRICA NOT ALL FUNGICIDES WILL BE AVALIABLE IN THE U.S.

RECOMMENDATIONS FOR CHEMICAL CONTROL FIRST APPLICATION NEEDS TO BE AT OR SOON AFTER FIRST FLOWER - IN ZIMBABWE THIS WAS 50 DAYS AFTER PLANTING. 2 OR 3 APPLICATIONS ARE NEEDED 14 - 20 DAYS BETWEEN APPLICATIONS THE FUNGICIDE NEEDS TO PENETRATE THE CANOPY

ADDITIONAL RECCOMENDATIONS- STROBALURIN FUNGICIDES NEED TO BE USED AS A PROTECTANT, ONCE RUST IS AT 5-10% THEY DO NOT ALWAYS PROTECT YIELD STROBALURINS ARE SINGLE SITE MODE OF ACTION - USED ONLY ONCE PER SEASON MANY TRIAZOLES MAY NOT HAVE THE RESIDUAL NEEDED FOR 20+ DAY INTERVALS ENVIRONMENT WILL HAVE AN EFFECT MIXES OF TRIAZOLES AND STROBALURINS ROTATE THE FUNGICIDES

OK, SO WHAT DO I USE? THERE ARE MANY QUESTIONS THAT NEED TO BE AWNSERED FIRST THE SECTION 18 EMERGENCY EXEMPTION REQUESTS HAVE 3 OR 4 SENARIOS WITH RECCOMENDATIONS THAT DEPEND ON PRESENCE OR PREDICTION OF RUST IS THE RUST PRESENT? HOW SEVERE? DO YOU NEED CURATIVE FUNGICIDE OR WILL A PROTECTANT FUNGICIDE WORK? ECONOMICS AND TIME OF SEASON? WHAT IS THE PRE HARVEST INTERVAL OF THE FUNGICIDE YOU WANT TO USE?

HOWCAN WE PENETRATE THE CANOPY? AERIAL AND GROUND NORMAL AND HIGH VOLUME TYPE OF NOZZLE FOR GROUND APPLICATION Application methods. One of the more critical application challenges for protecting the soybean crop from yield losses due to soybean rust is to penetrate the canopy and deliver the fungicide into the middle third of the canopy. Fungicides are not used in most soybean production areas, so little work has been done to develop fungicide application programs for the crop. Both aerial and ground applications are used in South America. Multiple application methods are being used in Southern Africa, with the most effective methods being those where penetration and canopy coverage are the greatest. Examples of effective methods include air assist and high pressure lateral discharge equipment, increased pressure delivery and increased water volume per hectare. Currently, there is a multi-state project to evaluate high and low volume application in aerial and ground systems using predominantly 30-inch row spacing. Within the ground application program are different nozzle types that would be available on a commercial basis today. Included are the flat fan nozzle that would be used for Round up application, as well as air induction and twin jet nozzles. Preliminary data from both aerial and ground application show the need for high volume (10 gal. aerial and 20 gal. ground applied) to penetrate the canopy into the middle third. There is need for additional experimentation before a fungicide application method can be developed to economically protect the soybean crop. M. MILES, 2003

FUNGICIDES ARE USED IN SOYBEAN PRODUCTION IN THE MID AND DEEP SOUTH RESULTS ARE MIXED. QUADRIS QUADRIS + WARRIOR NOT ALWAYS ASSOCIATED WITH PEST CONTROL. D. HERSHMAN, U OF KY.

WHAT WILL WE HAVE FOR THE FUTURE? FUNGICIDES YIELD STABILITY PARTIAL RESISTANCE COMBINED SINGLE GENES GENES FROM RELATED SPECIES THE MOST SUCCESFULL APPROCH WILL HAVE ALL IN COMBINATION M MILES, 2003

RESEARCH SUPPORTED BY: USDA-ARS USDA CSREES UNITED SOYBEAN BOARD REPRESENTATIVES FROM THE CHEMICAL INDUSTRY