The quick and the deadly: growth vs virulence in a seed bank pathogen.
*We studied the relationship between virulence (ability to kill nondormant Bromus tectorum seeds) and mycelial growth index in the necrotrophic seed pathogen Pyrenophora semeniperda. Seed pathosystems involving necrotrophs differ from those commonly treated in traditional evolution-of-virulence models in that host death increases pathogen fitness by preventing germination, thereby increasing available resources. Because fast-germinating, nondormant B. tectorum seeds commonly escape mortality, we expected virulence to be positively correlated with mycelial growth index. *We performed seed inoculations using conidia from 78 pathogen isolates and scored subsequent mortality. For a subset of 40 of these isolates, representing a range of virulence phenotypes, we measured mycelial growth index. *Virulence varied over a wide range (3-43% seed mortality) and was significantly negatively correlated with mycelial growth index (R(2) = 0.632). More virulent isolates grew more slowly than less virulent isolates. *We concluded that there is an apparent tradeoff between virulence and growth in this pathogen, probably because the production of toxins necessary for necrotrophic pathogenesis competes with metabolic processes associated with growth. Variation in both virulence and growth rate in this pathosystem may be maintained in part by seasonal variation in the relative abundance of rapidly germinating vs dormant host seeds available to the pathogen.
Meyer
Susan E
SE
US Forest Service, Rocky Mountain Research Station, Shrub Sciences Laboratory, 735 North 500 East, Provo, UT 84606, USA.
Stewart
Thomas E
TE
Department of Plant and Wildlife Science, Brigham Young University, Provo, UT 84601, USA.
Clement
Suzette
S
US Forest Service, Rocky Mountain Research Station, Shrub Sciences Laboratory, 735 North 500 East, Provo, UT 84606, USA.
D001203:Ascomycota / Q000254:growth & development* / Q000302:isolation & purification / Q000472:pathogenicity*; D018070:Biological Specimen Banks; D031724:Bromus / Q000382:microbiology*; D025282:Mycelium / Q000254:growth & development; D012639:Seeds / Q000382:microbiology*; D014774:Virulence
Alizón S, Hurford A, Midéo N, Van Ballen M. 2009. Virulence evolution and the trade-off hypothesis: history, current state of affairs, and the future. Journal of Evolutionary Biology 22: 245-259.
Anderson RM, May RM. 1982. Coevolution of hosts and parasites. Parasitology 85: 411-426.
Apoga D, Åkesson H, Jansson H, Odham G. 2002. Relationship between the production of the phytotoxin prehelminthosporol and virulence in isolates of Bipolaris sorokiniana. European Journal of Plant Pathology 108: 519-526.
Beckstead J, Meyer SE, Connolly BM, Huck MB, Street LE. 2010. Cheatgrass facilitates spillover of a seed bank pathogen onto native grass species. Journal of Ecology 98: 168-177.
Beckstead J, Meyer SE, Molder C, Smith C. 2007. A race for survival: can Bromus tectorum seeds escape Pyrenophora semeniperda-caused mortality by germinating quickly? Annals of Botany 99: 907-914.
Campbell MA, Medd RW. 2003. Leaf, floret and seed infection of wheat by Pyrenophora semeniperda. Plant Pathology 52: 437-447.
Campbell MA, Medd RW, Brown JF. 1996. Growth and sporulation of Pyrenophora semeniperda in vitro: effects of culture media, temperature and pH. Mycological Research 100: 311-317.
Campbell MA, Medd RW, Brown JF. 2003a. Phytotoxicity of metabolites produced by Pyrenophora semeniperda in liquid culture. Australian Journal of Experimental Agriculture 43: 1237-1244.
Campbell MA, Medd RW, Brown JF. 2003b. Optimizing conditions for growth and sporulation of Pyrenophora semeniperda. Plant Pathology 52: 448-454.
Capio ER, Tate ME, Wallwork H. 2004. Phytotoxic metabolites from Drechslera wirreganensis and D. campanulata. Australasian Plant Pathology 33: 23-28.
Combes C. 1997. Fitness and parasites: pathology and selection. International Journal for Parasitology 27: 1-10.
Desjardins AE, Plattner RD, Nelsen TC, Leslie JF. 1995. Genetic analysis of fumonosin production and virulence of Gibberella fujikuroi mating population A (Fusarium moniliforme) on maize (Zea mays). Applied Environmental Microbiology 61: 79-86.
Evidente A, Andolfi A, Vurro M, Zono MC, Motta A. 2002. Cytochalasins Z1, Z2 and Z3, three 24-oxa[14]cytochalasins produced by Pyrenophora semeniperda. Phytochemistry 60: 45-53.
Frank SA, Schmid-Hempel P. 2008. Mechanisms of pathogenesis and the evolution of parasite virulence. Journal of Evolutionary Biology 21: 396-404.
Gilbert GS. 2002. Evolutionary ecology of plant diseases in natural ecosystems. Annual Review of Phytopathology 40: 13-43.
van Kan JAL. 2006. Licensed to kill: the lifestyle of a necrotrophic plant pathogen. Trends in Plant Science 11: 247-253.
Kreitlow KW, Bleak AT. 1964. Podosporiella verticillata, a soil-borne pathogen of some western Gramineae. Phytopathology 54: 353-357.
Lipsitch M, Herre EA, Nowak MA. 1995. Host population structure and the evolution of virulence: a ‘law of diminishing returns’. Evolution 49: 743-748.
Lipsitch M, Siller S, Nowak MA. 1996. The evolution of virulence in pathogens with vertical and horizontal transmission. Evolution 50: 1729-1741.
May RM, Nowak MA. 1995. Coinfection and the evolution of parasite virulence. Proceedings of the Royal Society of London. Series B, Biological Sciences 261: 209-215.
Medd RW, Campbell MA. 2005. Grass seed infection following inundation with Pyrenophora semeniperda. Biocontrol Science and Technology 15: 21-36.
Medd RW, Murray GM, Pickering DI. 2003. Review of the epidemiology and economic importance of Pyrenophora semeniperda. Australasian Plant Pathology 32: 539-550.
Meyer SE, Quinney D, Nelson DL, Weaver J. 2007. Impact of the pathogen Pyrenophora semeniperda on Bromus tectorum seedbank dynamics in North American cold deserts. Weed Research 47: 54-62.
de Nooij MP, van Damme JMM. 1988. Variation in host susceptibility among and within populations of Plantago lanceolata L. infected by the fungus Phomopsis subordinaria (Desm.) Trav. Oecologia 75: 535-538.
Nowak MA, May RM. 1994. Superinfection and the evolution of parasite virulence. Proceedings of the Royal Society of London. Series B, Biological Sciences 255: 81-89.
O’Keefe JK, Antonovics J. 2002. Playing by different rules: the evolution of virulence in sterilizing pathogens. American Naturalist 159: 597-605.
Oöi M, Aulk T, Whelan R. 2004. Comparison of the cut and tetrazolium tests for assessing seed viability: a study using Australian native Leucopogon species. Ecological Management & Restoration 5: 141-143.
Panaccione DG. 1993. The fungal genus Cochliobolus and toxin-mediated plant disease. Trends in Microbiology 14: 14-20.
Pfennig KS. 2001. Evolution of pathogen virulence: the role of variation in host phenotype. Proceedings of the Royal Society of London. Series B, Biological Sciences 268: 755-760.
Poulin R, Combes C. 1999. The concept of virulence: interpretations and implications. Parasitology Today 15: 474-475.
Reino JL, Hernández-Galán R, Durán-Patrón R, Collado IG. 2004. Virulence-toxin production relationship of the plant pathogenic fungus Botrytis cinerea. Journal of Phytopathology 152: 563-566.
Sacristán S, García-Arenál F. 2008. The evolution of virulence and pathogenicity in plant pathogen populations. Molecular Plant Biology 9: 369-384.
Stewart TE, Allen PS, Meyer SE. 2009. First report of Pyrenophora seminiperda in Turkey and Greece. Plant Disease 93: 1351.
Thrall PH, Barrett LG, Burdon JJ, Alexander HM. 2005. Variation in pathogen aggressiveness within a metapopulation of the Cakile maritima-Alternaria brassicicola host-pathogen association. Plant Pathology 54: 265-274.