Biotic pests in cereal crop production: plant pathogens Wheat streak mosaic virus and Stem Rust Ug99 Mary Burrows, Dai Ito, Matt Moffet, Zach Miller, Fabian Menalled, Mareike Johnston, Luther Talbert, Tom Blake, and Phil Bruckner

Initiated in 2002 by USDA-CSREES with homeland security funding Goal: to provide diagnostic capability to the nation’s agricultural system Five regional hubs with responsibility for diagnostics, funding, public relations, epidemiology, and training

Regional Networks of NPDN Western Plant Diagnostic Network University of California, Davis Great Plains Diagnostic Network Kansas State University South Eastern Plant Diagnostic Network University of Florida North Central Plant Diagnostic Network Michigan State University North Eastern Plant Diagnostic Network Cornell University National Agricultural Pest Information System Purdue University

Network Responsibilities Data collection (detectors/diagnosticians) Communications system Information storage and management Data analysis New events and analysis of new appearance Pattern recognition Unusual patterns of endemic problems GIS Event propagation Tracking Reporting and alerts Link to State Departments of Ag and US regulatory agencies

WSMV: The Pathogen Family Potyviridae, genus Tritimovirus Mite-transmitted virus

Wheat streak mosaic virus Infects both winter and spring wheat –Symptoms in spring Earlier infection = greater yield loss Grassy weeds, volunteer wheat, corn, etc. can harbor both WSMV and the mite vector 5-10% yield loss/yr across Great Plains 100% yield loss in individual fields SDSU Extension

Disease cycle of WSMV

Weed Host: Volunteer Wheat

WSMV in Montana weeds, 2008 Volunteer wheat is the best non-crop host, but weed species are also are infected with virus and may serve as a source

Which weeds are susceptible? Common nameLiterature 1 ELISA 2 Jointed goatgrassYesLocal Wild oatYes+ Downy BromeYesLocal Crested WheatgrassNo- Thickspike Wheatgrass No- QuackgrassNo+ Slender WheatgrassNo- Smooth BromeNo- BarnyardgrassYes+ Green FoxtailYes- 1 WSMV host data taken from Somsen 1970, Townsend 1996, and Brey, Data from MSU: 'Local' = Virus restricted to inoculated leaves in preliminary assay

Regional variation in the susceptibility of weeds to WSMV Wheat = 1

Increase in regional virus incidence? Host PathogenEnvironment （ New York Times) SDSU Extension Vector

Determine prevalence of wheat viruses in the Great Plains (WSMV, HPV, TriMV, BYDV-PAV and CYDV-RPV)Determine prevalence of wheat viruses in the Great Plains (WSMV, HPV, TriMV, BYDV-PAV and CYDV-RPV) Nine states:Nine states: WY, MT, CO, KS, OK, TX, SD, ND, NE Determine geographic distribution for TriMV & HPVDetermine geographic distribution for TriMV & HPV Determine if host symptoms are diagnostic among virus species for single and multiple infectionsDetermine if host symptoms are diagnostic among virus species for single and multiple infections Collect and provide virus infected plant tissues to support research effortsCollect and provide virus infected plant tissues to support research efforts Increase communication about wheat viruses in the Great Plains RegionIncrease communication about wheat viruses in the Great Plains Region Wheat virus survey, 2008: Objectives

Objective: Objective: Determine prevalence of wheat viruses WSMV detected in all GPDN states at high percentage infection (10 – 83 %)WSMV detected in all GPDN states at high percentage infection (10 – 83 %) HPV detected in all GPDN statesHPV detected in all GPDN states HPV identified in MT and WY for the first timeHPV identified in MT and WY for the first time TriMV identified in all states, all but KS new reportsTriMV identified in all states, all but KS new reports

2008nWSMVWMoVTriMV Colorado Kansas Montana Nebraska North Dakota Oklahoma South Dakota Texas Wyoming Total Colorado Kansas Montana Nebraska North Dakota Oklahoma South Dakota Texas Wyoming Total

2008nWSMV + WMoVWSMV + TriMVWMoV + TriMVAll mite Colorado Kansas Montana Nebraska North Dakota Oklahoma South Dakota Texas Wyoming Total Colorado Kansas Montana Nebraska North Dakota Oklahoma South Dakota Texas Wyoming Total

Winter wheat: inoculated trials

Yield reductions due to spring inoculation with WSMV, 2008 & Variety Yield of control (bu/a) % yield reduction Yield of control (bu/a) % yield reduction Genou CDC Falcon Rampart Neeley Ledgar Jagalene Tiber Yellowstone Rocky Pryor Morgan MTV Average

Spring wheat: inoculated trials

Yield reductions due to inoculation with WSMV, 2008 & Variety Yield of control (bu/A) % yield reduction Yield of control (bu/A) % yield reduction Reeder Choteau McNeal Conan Fortuna Ernest Corbin Hank Amidon Scholar Metcalfe N/A Haxby N/A Mean

Race Evolution in TTKS (Ug99) Lineage & Implications to Resistance Breeding Yue Jin, USDA-ARS

Ug99 First reported in Uganda in Pretorius et al Plant Dis 84:203 Virulent on Sr31 Sr31 is located on 1BL.1RS translocation Also carries Lr26, Yr9 Increased adaptation and higher yield. As a result, widely spread in wheat worldwide Helped to reduce stem rust population worldwide Virulence to Yr9, originated in the eastern Africa in mid 80s, caused worldwide epidemics

TTKS In 2002 and 2004, CIMMYT nursery planted in Njoro, Kenya were severely infected by stem rust. In 2005, we identified Kenyan isolates from 2004 were race TTKS. --Wanyera, Kinyua, Jin, Singh 2006 Plant Dis 90:113

Broad virulence of TTKS to North American spring wheat  US spring wheat CVs of the Northern Great Plains, known to have broad-based resistance to stem rust, were mostly susceptible (84%).  500 CIMMYT CVs released since 1950’s, 84% were susceptible. Conclusion: Ug99 possesses a unique virulence combination that renders many resistance genes ineffective. Jin & Singh, 2006, Plant Dis:90:

Evolution of the TTKS lineage TTKSK TTTSKTTKST Sr24- Sr31+ Sr36- Sr24+ Sr31+ Sr36- Sr24- Sr31+ Sr36+ Our data point to: Jin et al Plant Dis. 92: Jin et al Plant Dis. (in Press)

% of resistance to TypeEntryTTKSKTTKSTTTTSK (Ug99)Sr24vSr36v Hard red spring8921%12%21% Hard red winter41629%15%28% Soft red winter37727%25%11% Western wheat603%3%3% Total94226%18%19% Ramification of Sr24/Sr36 virulence to US Wheat based on testing of 2007 elite breeding germplasm

Current status of Ug99 New races constantly evolving Ug99 stalled in Iran due to long drought If moves to Pakistan/India will affect 15% of world’s wheat crop that feeds 1 billion of the world’s poorest people Strain of stem rust in India that overcomes Sr25 ‘Likely’ Ug99 has already spread beyond Iran - Rick Ward, co-coordinator of the Durable Rust Resistance in Wheat project, based at Cornell university; Rust Resistance in Wheat project

Projected potential pathways for Ug99 based on the migration of Yr9 virulence Singh et al CAB Review 1, 54

Ug99 migration Singh et al Advances in Agronomy v ? ?

The good news Phil and Luther are both working on it already! Li Huang, PSPP, has identified spring wheat mutants from a population derived by Mike Giroux with resistance to leaf, stem, and stripe rust – including all Ug99 derivatives Fungicide trials with great results Communication and education ramping up!

Wheat stem rust fungicide trial results (2008) Stein and Gupta, SDSU Stem rust (% leaf area)

Triazoles Triazole + Strobilurin

Fungicide modes of action: Triazoles FRAC group 3 DMI (demethylation) inhibitors; biosynthesis of sterols in fungal cell membrane; spore penetration and mycelial growth Provides days of protection Medium risk of resistance development Greater mobility in plant than strobilurin fungicides Most widely used class of fungicide in the world Control a wide array of fungal diseases Protective and curative effects (if applied early in disease development)

Fungicide movement in the plant From: Tenuta, A., D. Hershman, M. Draper and A. Dorrence Using foliar fungicides to manage soybean rust.. Land-Grant Universities Cooperating NCERA-208 and OMAF. Available online at state.edu/SoyRust/

Fungicide modes of action: Strobilurins FRAC group 11 QoI (quinone outside) inhibitors (respiration); spore germination, penetration, and mycelial growth Provides days of protection High risk of resistance development because it has a very specific mode of action (they block electron transfer at the site of quinol oxidation (the Qo site) in the cytochrome bc 1 complex, thus preventing ATP formation) Originally isolated from wood-rotting fungi Strobilurus tenacellus ‘Reduced-risk’ pesticide (pose less risk to human health than other chemical options at the time of registration by EPA) Control a wide array of fungal diseases Excellent preventative fungicides, but limited curative effects “Plant health benefit” independent of disease control?

Figure 1. Mobility of trifloxystrobin, an example of a QoI fungicide. /Strobilurin/top.htm

Preventing fungicide resistance Limit the number of applications of a single FRAC group per season Limit the number of consecutive applications of a single FRAC group Mix fungicides with different modes of action (FRAC groups) Use early in disease development

Stem rust fungicide trial RateActive IngredientCompany 1.Control 2.Proline 480 SC5.3 ozProthioconazoleBayer 3. Prosaro 421 SC7.5 ozTebuconazole + ProthioconazoleBayer 4. Quilt14 ozAzoxystrobin + PropiconazoleSyngenta 5. A15590C14 ozAzoxystrobin + PropiconazoleSyngenta 6. Alto 100SL4 ozCyproconazoleSyngenta 7. Caramba13.5 oz MetconazoleBASF 8. Twinline9 oz Pyraclostrobin +Metconazole BASF 9. Headline 2.09EC7.5 ozPyraclostrobinBASF 10. Gem 500 SC2.4 ozTrifloxystrobinBayer

Control (no fungicide), 14 daa

Strobilurin fungicides, 14 daa Headline Gem 500 SC

Strobiliurin + Trizole, 14 daa Quilt Quilt Xcel

Strobiliurin + Trizole, 14 daa Prosaro Twinline

Trizole fungicides, 14 daa Alto Proline Caramba

Compare sprayed and unsprayed plots

Yield, stem rust fungicide trial 2009, Bozeman a bcd cd bc a cd d bc b