Abstract
Transcriptional changes during asexual sporangia formation by the late blight pathogen Phytophthora infestans were identified using microarrays representing 15,646 genes and RNA from sporulation time-courses, purified spores, and sporulation-defective strains. Results were confirmed by reverse transcription-polymerase chain reaction analyses of sporulation on artificial media and infected tomato. During sporulation, about 12% of genes were up-regulated compared to vegetative hyphae and 5% were down-regulated. The most prevalent induced genes had functions in signal transduction, flagella assembly, cellular organization, metabolism, and molecular or vesicular transport. Distinct patterns of expression were discerned based on the kinetics of mRNA induction and their persistence in sporangia. For example, most flagella-associated transcripts were induced very early in sporulation and maintained in sporangia, while many participants in metabolism or small molecule transport were also induced early but had low levels in sporangia. Data from this study are a resource for understanding sporogenesis, which is critical to the pathogenic success of P. infestans and other oomycetes.
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Adl SM, Simpson AG, Farmer MA, Andersen RA, Anderson OR, Barta JR, Bowser SS, Brugerolle G, Fensome RA, Fredericq S, James TY, Karpov S, Kugrens P, Krug J, Lane CE, Lewis LA, Lodge J, Lynn DH, Mann DG, McCourt RM, Mendoza L, Moestrup O, Mozley-Standridge SE, Nerad TA, Shearer CA, Smirnov AV, Spiegel FW, Taylor MF (2005) The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. J Eukaryot Microbiol 52:399–451
Ah Fong A, Judelson HS (2003) Cell cycle regulator Cdc14 is expressed during sporulation but not hyphal growth in the fungus-like oomycete Phytophthora infestans. Mol Microbiol 50:487–494
Axelrod DE, Gealt M, Pastushok M (1973) Gene control of developmental competence in Aspergillus nidulans. Dev Biol 34:9–15
Christen J, Hohl HR (1972) Growth and ultrastructural differentiation of sporangia in Phytophthora palmivora. Can J Microbiol 18:1959–1964
Clark MC, Melanson DL, Page OT (1978) Purine metabolism and differential inhibition of spore germination in Phytophthora infestans. Can J Microbiol 24:1032–1038
Cohen Y, Eyal H, Sadon T (1975) Light induced inhibition of sporangial formation of Phytophthora infestans on potato leaves. Can J Bot 53:2680–2686
Deacon JW, Donaldson SP (1993) Molecular recognition in the homing responses of zoosporic fungi, with special reference to Pythium and Phytophthora. Mycol Res 97:1153–1171
Fry WE (2008) Phytophthora infestans: the plant (and R gene) destroyer. Mol Plant Pathol 9:385–402
Grenville-Briggs LJ, Avrova AO, Bruce CR, Williams A, Whisson SC, Birch PR, van West P (2005) Elevated amino acid biosynthesis in Phytophthora infestans during appressorium formation and potato infection. Fungal Genet Biol 42:244–256
Hardham AR (2001) Cell biology of fungal infection of plants. In: Howard RJ, Gow NAR (eds) The Mycota. Springer, Heidelberg, pp 91–123
Hardham AR, Hyde GJ (1997) Asexual sporulation in the oomycetes. Adv Bot Res 24:353–398
Judelson HS, Ah-Fong AMV, Aux G, Avrova AO, Bruce C, Cakir C, da Cunha L, Grenville-Briggs L, Latijnhouwers M, Ligterink W, Meijer HJG, Roberts S, Thurber CS, Whisson SC, Birch PRJ, Govers F, Kamoun S, van West P, Windass J (2008) Gene expression profiling during asexual development of the late blight pathogen Phytophthora infestans reveals a highly dynamic transcriptome. Mol Plant Microbe Interact 21:433–447
Judelson HS, Blanco FA (2005) The spores of Phytophthora: weapons of the plant destroyer. Nat Microbiol Rev 3:47–58
Kim KS, Judelson HS (2003) Sporangia-specific gene expression in the oomyceteous phytopathogen Phytophthora infestans. Eukaryot Cell 2:1376–1385
Latijnhouwers M, Ligterink W, Vleeshouwers VGAA, Van West P, Govers F (2004) A G-alpha subunit controls zoospore motility and virulence in the potato late blight pathogen Phytophthora infestans. Mol Microbiol 51:925–936
Maltese CE, Conigliaro G, Shaw DS (1995) The development of sporangia of Phytophthora infestans. Mycol Res 99:1175–1181
Marks GE (1965) The cytology of Phytophthora infestans. Chromosoma 16:681–692
Penington CJ, Iser JR, Grant BR, Gayler KR (1989) Role of RNA and protein synthesis in stimulated germination of zoospores of the pathogenic fungus Phytophthora palmivora. Exp Mycol 13:158–168
Raffray JB, Sequeira L (1971) Dark induction of sporulation in Bremia lactucae. Can J Bot 49:237–239
Randall TA, Dwyer RA, Huitema E, Beyer K, Cvitanich C, Kelkar H, Ah Fong AMV, Gates K, Roberts S, Yatzkan E, Gaffney T, Law M, Testa A, Torto T, Zhang M, Zheng L, Mueller E, Windass J, Binder A, Birch PRJ, Gisi U, Govers F, Gow NAR, Mauch F, van West P, Waugh ME, Yu J, Boller T, Kamoun S, Lam ST, Judelson HS (2005) Large-scale gene discovery in the oomycete Phytophthora infestans reveals likely components of phytopathogenicity shared with true fungi. Mol Plant Microbe Interact 18:229–243
Ribeiro OK (1983) Physiology of asexual sporulation and spore germination in Phytophthora. In: Erwin DC, Bartnicki-Garcia S, Tsao PH (eds) Phytophthora, its biology, taxonomy, ecology, and pathology. APS Press, St Paul, pp 55–70
Robold AV, Hardham AR (2005) During attachment Phytophthora spores secrete proteins containing thrombospondin type 1 repeats. Curr Genet 47:307–315
Roncal T, Ugalde U (2003) Conidiation induction in Penicillium. Res Microbiol 154:539–546
Sato N (1994) Maturation of sporangia of Phytophthora infestans affecting the rapidity of indirect germination. Ann Phytopath Soc Jpn 60:53–59
Walker CA, Koppe M, Grenville-Briggs LJ, Avrova AO, Horner NR, McKinnon AD, Whisson SC, Birch PR, van West P (2008) A putative DEAD-box RNA-helicase is required for normal zoospore development in the late blight pathogen Phytophthora infestans. Fungal Genet Biol 45:954–962
Wallin JR (1953) The production and survival of sporangia of Phytophthora infestans on tomato and potato plants in the field. Phytopathology 43:505–508
Yu JH, Mah JH, Seo JA (2006) Growth and developmental control in the model and pathogenic Aspergilli. Eukaryot Cell 5:1577–1584
Acknowledgments
We are grateful to Syngenta Corporation for providing the Affymetrix GeneChips, and to T. Zhu and G. Aux for technical assistance in analysis of the arrays. This work was funded by the United States Department of Agriculture-National Research Initiative program of the Cooperative State Research, Education, and Extension Service.
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Communicated by J. Perez-Martin.
Microarray data reported in this paper are deposited at NCBI GEO as experiment series GSE13580.
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Judelson, H.S., Narayan, R.D., Ah-Fong, A.M.V. et al. Gene expression changes during asexual sporulation by the late blight agent Phytophthora infestans occur in discrete temporal stages. Mol Genet Genomics 281, 193–206 (2009). https://doi.org/10.1007/s00438-008-0407-5
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DOI: https://doi.org/10.1007/s00438-008-0407-5