Pathogen and host genotype differently affect pathogen fitness through their effects on different life-history stages

BMC Evolutionary Biology

Georgiana May³  Martin Carson¹  Emily Bruns² 

[1] United States Department of Agriculture – Agriculture Research Service, Cereal Disease Laboratory, University of Minnesota, Saint Paul, 55108, USA;Graduate Program in Ecology, Evolution and Behavior, University of Minnesota, Saint Paul, MN, 55108, USA;Department of Ecology Evolution and Behavior, University of Minnesota, Saint Paul, MN, 55108, USA

关键词: Avena sativa;    Puccinia coronata;    Pathogen reproductive rate;    Fitness;    Density-dependence;    Life history;    Host-pathogen interactions;   

Others  :  1140661
DOI  :  10.1186/1471-2148-12-135

 received in 2012-05-04, accepted in 2012-07-10,  发布年份 2012

【 摘 要 】

Background

Adaptation of pathogens to their hosts depends critically on factors affecting pathogen reproductive rate. While pathogen reproduction is the end result of an intricate interaction between host and pathogen, the relative contributions of host and pathogen genotype to variation in pathogen life history within the host are not well understood. Untangling these contributions allows us to identify traits with sufficient genetic variation for selection to act and to identify mechanisms of coevolution between pathogens and their hosts. We investigated the effects of pathogen and host genotype on three life-history components of pathogen fitness; infection efficiency, latent period, and sporulation capacity, in the oat crown rust fungus, Puccinia coronata f.sp. avenae, as it infects oats (Avena sativa).

Results

We show that both pathogen and host genotype significantly affect total spore production but do so through their effects on different life-history stages. Pathogen genotype has the strongest effect on the early stage of infection efficiency, while host genotype most strongly affects the later life-history stages of latent period and sporulation capacity. In addition, host genotype affected the relationship between pathogen density and the later life-history traits of latent period and sporulation capacity. We did not find evidence of pathogen-by-host genotypic (GxG) interactions.

Conclusion

Our results illustrate mechanisms by which variation in host populations will affect the evolution of pathogen life history. Results show that different pathogen life-history stages have the potential to respond differently to selection by host or pathogen genotype and suggest mechanisms of antagonistic coevolution. Pathogen populations may adapt to host genotypes through increased infection efficiency while their plant hosts may adapt by limiting the later stages of pathogen growth and spore production within the host.

【 授权许可】

   
2012 Bruns et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Roff D: Life History Evolution. Sinauer Associates, Sunderland, MA; 2002.
• [2]Agnew P, Koella JC, Michalakis Y: Host life history responses to parasitism. Microbes Infect 2000, 2:891-896.
• [3]Gandon S, Agnew P, Michalakis Y: Coevolution between parasite virulence and host life-history traits. Am Nat 2002, 160:374-388.
• [4]Bonds MH: Host life-history strategy explains pathogen-induced sterility. Am Nat 2006, 168:281-293.
• [5]Ohlberger J, Langangen Ø, Edeline E, Olsen EM, Winfield IJ, Fletcher JM, James JB, Stenseth NC, Vøllestad LA: Pathogen-induced rapid evolution in a vertebrate life-history trait. Proc R Soc Lond B 2011, 278:35-41.
• [6]Fredensborg BL, Poulin R: Parasitism shaping host life-history evolution: adaptive responses in a marine gastropod to infection by trematodes. J Anim Ecol 2006, 75:44-53.
• [7]Chadwick W, Little TJ: A parasite-mediated life-history shift in Daphnia magna. Proc R Soc Lond B 2005, 272:505-509.
• [8]Woodhams DC, Alford RA, Briggs CJ, Johnson M, Louise A, Woodhams C, Alford A, Briggs J: Life-history trade-offs influence disease in changing climates: strategies of an amphibian pathogen. Ecology 2008, 89:1627-1639.
• [9]Nidelet T, Koella JC, Kaltz O: Effects of shortened host life span on the evolution of parasite life history and virulence in a microbial host-parasite system. BMC Evol Biol 2009, 9:65. BioMed Central Full Text
• [10]Ben-Ami F, Mouton L, Ebert D: The effects of multiple infections on the expression and evolution of virulence in a Daphnia-endoparasite system. Evolution 2008, 62:1700-1711.
• [11]May RM, Anderson RM: Epidemiology and genetics in the coevolution of parasites and hosts. Proc R Soc Lond B 1983, 219:281-313.
• [12]Leonard KJ: Selection pressures and plant pathogens. Annal NY Acad Sci 1977, 287:207-222.
• [13]Frank S: Coevolutionary genetics of hosts and parasites with quantitative inheritance. Evol Ecol 1994, 8:74-94.
• [14]Tellier A, Brown J: Stability of genetic polymorphism in host-parasite interactions. Proc R Soc Lond B 2007, 274:809-817.
• [15]Thompson J, Burdon JJ: Gene-for-gene coevolution between plants and parasites. Nature 1992, 360:121-125.
• [16]Bergelson J, Kreitman M, Stahl EA, Tian D: Evolutionary dynamics of plant R-genes. Science 2001, 292:2281-2285.
• [17]Agrawal A, Lively CM: Infection genetics: gene-for-gene versus matching- alleles models and all points in between. Evol Ecol Res 2002, 4:79-90.
• [18]Thrall PH, Burdon JJ: Evolution of gene-for-gene systems in metapopulations: The effect of spatial scale of host and pathogen dispersal. Plant Pathol 2002, 51:169-184.
• [19]Jones JDG, Dangl JL: The plant immune system. Nature 2006, 444:323-329.
• [20]Gandon S, Capowiez Y, Dubois Y, Michalakis Y, Olivieri I: Local adaptation and gene-for-gene coevolution in a metapopulation model. Proc R Soc Lond B 1996, 263:1003-1009.
• [21]Laine-liisa A: Spatial scale of local adaptation in a plant-pathogen metapopulation. J Evol Biol 2005, 18:930-938.
• [22]Burdon JJ, Thrall PH: Co-evolution of plants and their pathogens in natural habitats. Science 2009, 324:755-756.
• [23]Thrall PH, Laine AL, Ravensdale M, Nemri A, Dodds PN, Barrett LG, Burdon JJ: Rapid genetic change underpins antagonistic coevolution in a natural host-pathogen metapopulation. Ecol Lett 2012, 15:425-435.
• [24]Young ND: QTL mapping and quantitative disease resistance in plants. Annu Rev Phytopathol 1996, 34:479-501.
• [25]Poland JA, Balint-Kurti PJ, Wisser RJ, Pratt RC, Nelson RJ: Shades of gray: the world of quantitative disease resistance. Trends Plant Sci 2009, 14:21-29.
• [26]Duneau D, Luijckx P, Ben-ami F, Laforsch C, Ebert D: Resolving the infection process reveals striking differences in the contribution of environment, genetics and phylogeny to host-parasite interactions. BMC Biol 2011, 9:11. BioMed Central Full Text
• [27]Grech K, Watt K, Read A: Host-parasite interactions for virulence and resistance in a malaria model system. J Evol Biol 2006, 19:1620-1630.
• [28]deRoode JC, Altizer S: Host-parasite genetic interactions and virulence-transmission relationships in natural populations of monarch butterflies. Evolution 2010, 64:502-514.
• [29]Salvaudon L, Héraudet V, Shykoff J: a: Genotype-specific interactions and the trade-off between host and parasite fitness. BMC EvolBiol 2007, 7:189. BioMed Central Full Text
• [30]Decaestecker E, Vergote A, Ebert D, Meester LD: Evidence for strong host clone-parasite species interactions in the Daphnia microparasite system. Evolution 2003, 57:784-792.
• [31]Kaltz O, Shykoff J: Local adaptation in host–parasite systems. Heredity 1998, 81:361-370.
• [32]Greischar MA, Koskella B: A synthesis of experimental work on parasite local adaptation. Ecol Lett 2007, 10:418-434.
• [33]Lambrechts L, Chevillon C, Albright RG, Thaisomboonsuk B, Richardson JH, Jarman RG, Scott TW: Genetic specificity and potential for local adaptation between dengue viruses and mosquito vectors. BMC Evol Biol 2009, 9:160. BioMed Central Full Text
• [34]Sicard D, Pennings P, Grandclement C, Acosta J, Kaltz O, Shykoff J: Specialization and local adaptation of a fungal parasite on two host plant species as revealed by two fitness traits. Evolution 2007, 61:27-41.
• [35]Restif O, Koella JC: Shared control of epidemiological traits in a coevolutionary model of host-parasite interactions. Am Nat 2003, 161:827-836.
• [36]Lambrechts L, Fellous S, Koella JC: Coevolutionary interactions between host and parasite genotypes. Trends Parasitol 2006, 22:12-16.
• [37]Alizon S, Hurford A, Mideo N, Van Baalen M: Virulence evolution and the trade-off hypothesis: history, current state of affairs and the future. J Evol Biol 2009, 22:245-259.
• [38]Asplen MK, Bruns E, David AS, Denison RF, Epstein B, Kaiser MC, Kaser JM, Lacroix C, Mohl EK, Quiram G, Prescott K, Stanton-Geddes J, Vincent JB, Wragg PD, May G: Do trade-offs have explanatory power for the evolution of organismal interactions? Evolution 2012, 66:1297-1307.
• [39]Jarosz A, Davelos A: Effect of disease in wild plant populations and the evolution of pathogen aggressiveness. New Phytol 1995, 129:371-387.
• [40]Alexander H, Thrall P, Antonovics J, Jarosz A, Oudemans P: Population dynamics and genetics of plant disease: a case study of anther-smut disease. Ecology 1996, 77:990-996.
• [41]Pariaud B, Ravigne V, Halkett F, Goyeau H, Carlier J, Lannou C: Aggressiveness and its role in the adaptation of plant pathogens. Plant Pathol 2009, 58:409-424.
• [42]Gilligan CA: Sustainable agriculture and plant diseases: an epidemiological perspective. Phil Trans R Soc B 2008, 363:741-759.
• [43]Pariaud B, Robert C, Goyeau H, Lannou C: Aggressiveness components and adaptation to a host cultivar in wheat leaf rust. Phytopathology 2009, 99:869-878.
• [44]Rigaud T, Perrot-Minnot M-J, Brown MJF: Parasite and host assemblages: embracing the reality will improve our knowledge of parasite transmission and virulence. Proc R Soc Lond B 2010, 277:3693-3702.
• [45]Barrett L, Thrall P, Burdon J, Linde C: Life history determines genetic structure and evolutionary potential of host-parasite interactions. Trends Ecol Evol 2008, 23:678-685.
• [46]Chong J, Leonard K, Salmeron J: A North American system of nomenclature for Puccinia coronata f.sp. avenae. Plant Dis 2000, 84:580-585.
• [47]Fleischmann G, Baker R: Oat crown rust race differentiation: Replacement of the standard differential varieties with a new set of single resistance gene lines derived fromAvena sterilis. Can J Botany 1971, 49:1433-1437.
• [48]Leonard KJ, Anikster Y, Manisterski J: Patterns of virulence in natural populations ofPuccinia coronataon wild oat in Israel and in agricultural populations on cultivated oat in the United States. Phytopathology 2004, 94:505-514.
• [49]Carson ML: Virulence frequencies in oat crown rust in the United States from 2001 through 2005. Plant Dis 2008, 92:379-384.
• [50]Fleischmann G, Mckenzie RIH: Inheritance of crown rust resistance inAvena sterilis. Crop Sci 1968, 8:710-713.
• [51]Abramoff MD, Magelhaes PJ, Ram SJ: Image processing with Image. J. BiophotonicsInt 2004, 11:36-42.
• [52]Carius H, Little T, Ebert D: Genetic variation in a host-parasite association: potential for coevolution and frequency-dependent selection. Evolution 2001, 55:1136-1145.
• [53]Niks RE, Rubiales D: Potentially durable resistance mechanisms in plants to specialised fungal pathogens. Euphytica 2002, 124:201-216.
• [54]Staples RC: Nutrients for a rust fungus: the role of haustoria. Trends Plant Sci 2001, 6:496-498.
• [55]Robert C, Bancal M-O, Lannou C: Wheat leaf rust uredospore production on adult plants: influence of leaf nitrogen content andSeptoriatriticiblotch. Phytopathology 2004, 94:712-721.
• [56]Newton MR, Kinkel LL, Leonard KJ: Competition and density-dependent fitness in a plant parasitic fungus. Ecology 1997, 78:1774-1784.
• [57]Bell AS, de Roode JC, Sim D, Read AF: Within-host competition in genetically diverse malaria infections: parasite virulence and competitive success. Evolution 2006, 60:1358-1371.
• [58]May R, Nowak M: Coinfection and the evolution of parasite virulence. Proc R SocLond B 1995, 261:209-215.
• [59]Leach JE, Vera Cruz CM, Bai J, Leung H: Pathogen fitness penalty as a predictor of durability of disease resistance genes. Annu Rev Phytopathol 2001, 39:187-224.
• [60]Sacristan S, Garcia-Arenal F: The evolution of virulence and pathogenicity in plant pathogen populations. Mol Plant Pathol 2008, 9:369-384.
• [61]Van Ginkel M, Scharen AL: Host-pathogen relationships of wheat andSeptoriatritici. Phytopathology 1988, 78:762-766.
• [62]Villaréal LM, Lannou C: Selection for increased spore efficacy by host genetic background in a wheat powdery mildew population. Phytopathology 2000, 90:1300-1306.
• [63]Legros M, Koella JC: Experimental evolution of specialization by a microsporidian parasite. BMC Evol Biol 2010, 10:159. BioMed Central Full Text
• [64]Groth J, Roelfs A: Effect of sexual and asexual reproduction on race abundance in cereal rust fungus populations. Phytopathology 1982, 72:1503-1507.
• [65]Wolinska J, King KC: Environment can alter selection in host-parasite interactions. Trends Parasitol 2009, 25:236-244.
• [66]Gilbert GS: Evolutionary ecology of plant diseases in natural ecosystems. Annu Rev Phytopathol 2002, 40:13-43.
• [67]Casadevall A, Pirofski L: The damage-response framework of microbial pathogenesis. Nat Rev Microbiol 2003, 1:17-24.
• [68]Bushnell WR: Structural and physiological alterations in susceptible host tissue. In The Cereal Rusts: Volume 1 Origins, Specificity, Structure, and Physiology. Edited by Bushnell WR, Roelfs . Academic Press Inc, Orlando; 1984:477-507.
• [69]Staves PA, Knell RJ: Virulence and competitiveness: testing the relationship during inter- and intraspecific mixed infections. Evolution 2010, 64:2643-2652.