How does host genotype diversity affect the pathogen population?

1. How does host genotype diversity affect the pathogen population? • Mixtures (blends) and multilines (mixtures of NILs) • Mechanisms • Dilution of inoculum • Barrier effect • Induced resistance

2. Technically… • Mixture: different species • fescue + bluegrass • Blend: different varieties, same species • E.g., wheat varieties NC Neuse + USG 3592

3. “Mid-component”: the mean of the mixture’s component cultivars when they are grown as pure stands • Mixture performance is typically evaluated by comparison to the mid-component • Disease severity • Yield • Quality

4. More on disease reduction mechanisms in small-grain blends • Induced resistance accounted for about 30% of total stripe rust reduction in wheat cultivar mixtures (Calonnec et al, 1996, Eur. J. Plant Pathol. 5:733-741) • Differences in genetic background among cultivars (partial resistance) led to additional 33% reduction of powdery mildew beyond that accounted for by R-gene differences (Wolfe et al., 1981, in Jenkyn and Plumb, eds, Strategies for the Control of Cereal Disease, Oxford: Blackwell) • Compensation of resistant cultivars through increased tillering accounted for 6% of total disease reduction by club wheat mixtures inoculated with stripe rust (Finckh & Mundt, 1992, Phytopathology 82:905-913) • Disease reductions below mid-component were statistically significant in 20 of 58 two-, three-, and four-component mixtures

5. From data in Finckh & Mundt, 1992, Stripe rust, yield, and plant competition in wheat cultivar mixtures, Phytopathology 82:905-913

6. Club wheat mixture: components can be distinguished by head color

7. Good reviews of host genotype diversity literature • Smithson & Lenné, 1996, “Varietal mixtures: a viable strategy for sustainable productivity in subsistence agriculture,” Ann. Appl. Biol, 128:127-158. • Garrett & Mundt, 1999, “Epidemiology in mixed host populations,” Phytopathology 89:984-990. • Mundt, 2002, “Use of multiline cultivars and cultivar mixtures for disease management,” Annu. Rev. Phytopathol. 40:381-410.

8. Characteristics that predict whether blends will reduce disease (Garrett & Mundt, 1999) • Things that maximize allo- vs. autodeposition • Genotype unit area • Shallow dispersal gradient of pathogen spores • Small lesion size • Short pathogen generation time • Strong host specialization Small GUA Large GUA

9. “Wheat blends stabilize yields,” The Furrow, John Deere, January 1997. • Reduce year-to-year yield fluctuation • Insure against future stresses: “Planting blends is one way to reduce the chances of picking the wrong variety for the conditions that develop.”– Jim Shroyer, Kansas State University agronomist “Ted Wolf grows equal amounts of three different varieties, then plants them as a blend the following year.”

10. Wheat blends in the U.S.(NASS, planted acres) J

11. Cereal blends internationally • German Democratic Republic (DDR = former East Germany): largest-ever blend “experiment” • From 1984 to 1990, cultivar mixtures comprised up to 92% of the barley acreage.

12. Barley mixtures planted until political re-unification of East and West Germany when government support for the project stopped. • Barley monoculture has been re-established in Germany and fungicide use has increased. • Wolfe M.S., 1997. Variety mixtures: concept and value. In: Variety Mixtures in theory and practice, Wolfe, M. S. (ed.). European Union Variety and Species Mixtures working group of COST Action 817. Online at: http://www.scri.sari.ac.uk/TiPP/Mix/Booklet/default.htm

13. Other blend experiences with disease reduction • Small grains • 10% of bread wheat acreage is currently in blends in Switzerland, Poland • Rice mixtures (planted by rows) in 10 Chinese townships (6,000-acre experiment!) reduced rice blast on S varieties by 94% (Zhu et al, 2000, Nature 406:718-722)

14. Potato late blight – mixed results: • blends reduced late blight severity for focal and general patterns of primary inoculum in Oregon, but had little effect in Ecuador (Garrett & Mundt,1999, Phytopathology, 89:984-990; 2000, Phytopathology, 90:1307-1312) • alternating S-R rows reduced late blight severity on S cultivar (Andrivon et al., 2003, Plant Pathol., 52:586-596) • no late-blight reduction by mixtures in UK (Phillips et al. 2005, Ann. Appl. Bio., 147:245-252)

15. Hemileia vastatrix – coffee rust • Coffee rust is the most economically important coffee disease in the world, and in monetary value, coffee is the most important agricultural product in international trade. (http://www.apsnet.org/Education/LessonsPlantPath/Coffeerust/default.htm)

16. So far, nine rust R-genes identified, mostly from C. canephora and C. liberica • The challenge is to deploy R genes in such a way they are not immediately overcome by new races of H. vastatrix. Figure 12. Susceptible Coffea arabica on the left; a resistant hybrid with C. canephora on the right. • So far, > 40 races of H. vastatrix identified. New ones continue to appear; some are able to attack previously resistant hybrids. • To reduce the rate of selection of virulent races, Cenicafé, a national coffee research center in Colombia, created a composite cultivar with uniform agronomic characteristics and coffee quality, but a mixture of genes for rust resistance.

17. Willows (and poplars) grown as “short-rotation coppice” – major energy crop in N. Ireland, UK, Sweden • A plantation yields 8 -18 tonnes of dry woodchip per hectare per year, and can be harvested on a 2-5 yr cycle up to 30 years before replanting. • Melampsora epitea causes rust on Salix (willow) • M. larici-populina causes rust on Populus (poplar) • Cultivars range from MS to immune; resistance can break down after 8-12 yr of heavy epidemics (e.g., N. Ireland) • Concerns that large-scale willow monocultures place strong selection pressure on Melampsora population • For pests such as brassy and blue willow beetles, as well as rust, planting a carefully selected mix of varieties is recommended. Fungicides not economically practical. • Will “super-races” evolve in mixtures?

18. Rust caused by the fungus Melampsora is the most serious disease in short rotation coppice (SRC) willow plantations for renewable energy. Willows (Salix) are grown as a major SRC crop  for energy because of their yield potential and coppicing ability. In most willows, rust only infects expanded leaves (left picture). However, in some willows, such as Salix viminalis and S. caprea, rust also attacks stems and young leaves. When severe, rust defoliates susceptible plantings prematurely (right picture) and reduces yields by as much as 40%. Severe rust also predisposes plants to infections by secondary pathogens which may lead to death of the plants.

19. Huge willow mixture experiments in Northern Ireland(McCracken & Dawson, Eur. J. For. Path., 1998, 28:241-250). • 20 Salix genotypes, 96x14 m. plots; 5-, 10-, 15-, and 20-way mixtures • Melampsora rust reduced by 50% or more on S genotypes in mixtures, but impact still so great they contributed little to yield • However, yield from 10-, 15- and 20-way mixtures not adversely affected despite loss of S trees • Epidemic initiation slowed by up to 3 wks in mixtures vs. pure stands • Pathotype diversity greater in mixtures than in pure stands; possible dilution of aggressive pathotypes

20. (McCracken & Dawson, Eur. J. For. Path., 1998, 28:241-250).

21. Didelot et al, 2007, Effects of cultivar mixtures on scab control in apple orchards, Plant Pathol. 56:1014-1022 * Venturia inequalis causes apple scab * Within-row mixtures: 7-21% reduction in incidence over 2 yrs, 35% reduction in severity in second yr, compared to monoculture of S cultivar

22. Will host diversity select for super-races? • “super-races” = pathogens with complex virulence (i.e., virulence to multiple R genes) and high fitness • Experimental data are scarce: • A multiline favored wheat rust strains with intermediate numbers of virulences (Kolmer, 1995, Can. J. Bot. 73:1081–1088)

23. Chin and Wolfe (1984, Plant Pathol. 33:535-546) : planted pure stands and mixtures of 2 or 3 barley cultivars (H, W, M), each with a different gene for mildew resistance • In pure stands, pathogen genotypes with simple virulences were more fit than those with more complex virulence. • In mixtures, the mean fitnesses of simple genotypes over both cultivars were reduced relative to the complex genotype.

24. Pure Mixture • Chin and Wolfe, Fig. 1. , 1978 trial, isolates collected from H, W, or M 31 and 53 d from sowing. • Changes in the frequencies of different virulence combinations on Hassan, Wing, and Midas in pure stands (H:H, W:W, M:M) and in mixed stands (H:W:M • On H: selection for simple races, even in mixtures • On W: complex races increased in frequency, though simple race predominated • On M: mixed results, but complex races dominated H W M

26. Summary: Chin and Wolfe • Contrary to Vanderplank: Rate of decline of an unnecessary virulence gene depends on host (e.g., W virulence on H and M) • Simple races usually fitter in pure stands, but relative fitness of complex races increased in mixtures because of their greater flexibility • Although mixtures encouraged gradual selection for complex virulence, absolute numbers of complex genotypes were reduced due to reduction in population size. • However, if same host mixture is grown continuously several seasons, there may be selection for modifiers that improve performance of complex pathogen types. • Evolution of super-races?

27. Pathogen evolution in mixtures • Other mechanisms besides a cost of virulence may counter “super race” emergence in mixtures (Mundt, 2002; Lannou and Mundt, 1997, TAG 94:991-999) • Quantitative adaptation to host genetic background – disruptive selection • Effects on relative fitness of • Pathogen genotype frequencies • Pathogen density • Immigration

28. Mixtures of cultivars with different levels of partial resistance • Models predict these mixtures can increase, decrease, or have no effect on disease severity relative to component pure stands (Jeger et al, 1981, Ann. Appl. Biol. 98:187-198) • Benefit if cultivars differ in infection frequency (IF) or sporulation rate (SR) • If differ in both IF and SR, and are ranked same by both, benefit is greater • If differ in both IF and SR, and are ranked differently, disadvantage can occur

29. Most empirical studies of mixtures of susceptible and partially resistant cultivars are of splash-dispersed necrotrophs on cereals • Rynchosporium secalis on barley • Stagonospora nodorum on wheat • Bipolaris sorokiniana on wheat • Mycosphaerella graminicola on wheat • Results: on average, relatively low levels of disease control. A few larger reductions similar to those expected for race-specific, obligate pathogens.

30. Effects of wheat cultivar mixtures on epidemic progression of Septoria tritici blotch and pathogenicity of Mycosphaerella graminicola, 2002, Cowger and Mundt, Phytopathology 92:617-623. Percent disease 1998 1999 Inconsistent performance of a mixture confronted with a splash-dispersed epidemic depending on environment 2000 Percent disease

31. Pathogen evolution in mixtures: the bottom line • A given R gene should be more durable deployed in a mixture than a monoculture • Complex pathotypes may be favored in mixtures (especially wind-dispersed biotrophs with major-gene resistance?) • This selection of complex types can be slowed by rotation of components in space and/or time • Evolution to complexity should be more than offset by reduction in inoculum loads