Effectors — key proteins in the interaction potato — Phytophthora infestans
Marta Brylińska
m.brylinska@ihar.edu.plPracownia Badania Odporności na Grzyby i Bakterie, Instytut Hodowli i Aklimatyzacji Roślin — Państwowy Instytut Badawczy, Młochów (Poland)
Jadwiga Śliwka
Pracownia Badania Odporności na Grzyby i Bakterie, Instytut Hodowli i Aklimatyzacji Roślin — Państwowy Instytut Badawczy, Młochów (Poland)
Abstract
Potato is one of the most appreciated crops in the world, with total production near 340 million tons making it the fourth most important crop plant. Potato production is severely reduced by late blight caused by Phytophthora infestans. This pathogen is so successful thanks to proteins secreted during interaction with the host — effectors. The identification and knowledge of functions of a wide variety of effector proteins are very important for understanding the interactions of plants with pathogens and may find practical use in resistance breeding. The plant is defended by resistance (R) proteins. In this review the knowledge about interactions between effectors and R proteins was summarized with potato — P. infestans pathosystem as an example. Two different classes of effectors were presented. The plant immune system model was discussed as well as the host responses to infection. We presented examples of the most studied effectors which employ different mechanisms for evading recognition by the resistance proteins.
Supporting Agencies
Keywords:
late blight, resistance, Solnaum tuberosumReferences
Armstrong M. R., Whisson S. C., Pritchard L., Bos J. I. B., Venter E., Avrova A. O., Rehmany A. P., Böhme U., Brooks K., Cherevach I., Hamlin N., White B., Fraser A., Lord A., Quail M. A., Churcher A., Hall N., Berriman M., Huang S., Kamoun S., Beynon J. L., Birch P. R. J. 2005. An ancestral oomycete locus contains late blight avirulence gene Avr3a, encoding a protein that is recognized in the host cytoplasm. PNAS. 102: 7766 — 7771.
Google Scholar
Birch P. R. J., Rehmany A. P., Pritchard L., Kamoun S., Beynon J. L. 2006. Trafficking arms: oomycete effectors enter host plant cells. TRENDS in Microbiology. 14 (1): 8 — 11.
Google Scholar
Black W., Mastenbroek C., Mills W. R., Peterson L. C. 1953. A proposal for an international nomenclature of races of Phytophthora infestans and of genes controlling immunity in Solanum demissum derivatives. Euphytica 2 (3): 173 — 240.
Google Scholar
Bouwmeester K., van Poppel P. M. J. A., Govers F. 2009. Genome biology cracks enigmas of Oomycete plant pathogens. Annual Plant Reviews. 34: 102 — 133.
Google Scholar
Champouret N. 2010. Functional Genomics of Phytophthora infestans Effectors and Solanum Resistance Genes. Phd thesis. ISBN 978_90_8585_658_0.
Google Scholar
Chen Y., Liu Z., Halterman D. A. 2012. Molecular Determinants of Resistance Activation and Suppression by Phytophthora infestans Effector IPI – O. PLoS Pathogens. 8(3): e1002595. doi: 10.1371/journal. ppat.1002595.
Google Scholar
Dodds P. N., Rathjen J. P. 2010. Plant immunity: towards an integrated view of plant — pathogen interactions. Nature Reviews Genetics. 11: 539 — 548.
Google Scholar
Gilroy E. M., Breen S., Whisson S. C., Squires J., Hein I., Kaczmarek M., Turnbull D., Boevink P. C., Lokossou A., Cano L. M., Morales J., Avrova A. O., Pritchard L., Randall E., Lees A., Govers F., van West P., Kamoun S., Vleeshouwers V. G. A. A., Cooke D. E. L., Birch P. R. J. 2011. Presence/ absence, differential expression and sequence polymorphisms between PiAVR2 and PiAVR2-like in Phytophthora infestans determine virulence on R2 plants. New Phytologist. 191: 763 — 776.
Google Scholar
Gilroy E. M., Taylor R. M., Hein I., Boevink P., Sadanandom A., Birch P. R. J. 2011. CMPG1 — dependent cell death follows perception of diverse pathogen elicitors at the host plasma membrane and is suppressed by Phytophthora infestans RXLR effector AVR3a. New Phytologist. 190: 653 — 666.
Google Scholar
Haas B. J., Kamoun S., Zody M. C., Jiang R. H. Y., Handsaker R. E., Cano L. M., Grabherr M., Kodira C. D., Raffaele S., Torto-Alalibo T., Bozkurt T. O., Ah-Fong A. M. V., Alvarado L., Anderson V. L., Armstrong M. R., Avrova A., Baxter L., Beynon J., Boevink P. C., Bollmann S. R., Bos J. I. B., Bulone V., Cai G., Cakir C., Carrington J. C., Chawner M., Conti L., Costanzo S., Ewan R., Fahlgren N., Fischbach M. A., Fugelstad J., Gilroy E. M., Gnerre S., Green P. J., Grenville-Briggs L. J., Griffith J., Grünwald N. J., Horn K., Horner N. R., Hu C., Huitema E., Jeong D., Jones A. M. E., Jones J. D. G., Jones R. W., Karlsson E. K., Kunjeti S. G., Lamour K., Liu Z., Ma L. J., MacLean D., Chibucos M. C., McDonald H., McWalters J., Meijer H. J. G., Morgan W., Morris P. F., Munro C. A., O’Neill K., Ospina-Giraldo M., Pinzo´n A., Pritchard L., Ramsahoye B., Ren Q., Restrepo S., Roy S., Sadanandom A., Savidor A., Schornack S., Schwartz D. C., Schumann U. D., Schwessinger B., Seyer L., Sharpe T., Silvar C., Song J., Studholme D. J., Sykes S., Thines M., van de Vondervoort P. J. I., Phuntumart V., Wawra S., Weide R., Win J., Young C., Zhou S., Fry W., Meyers B. C., van West P., Ristaino J., Govers F., Birch P. R. J., Whisson S. C., Judelson & Chad Nusbaum H. S. 2009. Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature. 461: doi:10.1038/nature08358.
Google Scholar
Jones J. D. G., Dangl J. L. 2006. The plant immune system. Nature. 444: doi:10.1038/nature05286.
Google Scholar
Kale S. D., Gu B., Capelluto D. G. S., Dou D., Feldman E., Rumore A., Arredondo F. D., Hanlon R., Fudal I., Rouxel T., Lawrence C. B., Shan W., Tyler B. M. 2010. External lipid PI3P mediates entry of eukaryotic pathogen effectors into plant and animal host cells. Cell. 142: 284 — 295.
Google Scholar
Kale S. D. 2012. Oomycete and fungal effector entry, a microbial Trojan horse. New Phytologist. 193: 874 — 881.
Google Scholar
Kamoun S. 2003. Molecular Genetics of Pathogenic Oomycetes. Eukaryotic Cell. 2: 191 — 199.
Google Scholar
Kamoun S. 2006. A Catalogue of the effector secretome of plant pathogenic oomycetes. Annu. Rev. Phytopathol. 44: 41 — 60.
Google Scholar
Morgan W., Kamoun S. 2007. RXLR effectors of plant pathogenic oomycetes. Current Opinion in Microbiology. 10: 332 — 338.
Google Scholar
Przyborski J., Lanzer M. 2004. The Malarial Secretome. SCIENCE. Doi: 10.1126/science.1107072.
Google Scholar
Rodewald J., Trognitz B. 2013. Solanum resistance genes against Phytophthora infestans and their corresponding avirulence genes. Molecular Plant Pathology. 14 (7): 740 — 757.
Google Scholar
Saunders D. G. O., Breen S., Win J., Schornack S., Hein I., Bozkurt T. O., Champouret N., Vleeshouwers V. G. A. A., Birch P. R. J., Gilroy E. M., Kamoun S. 2012. Host protein BSL1 associates with Phytophthora infestans RXLR effector AVR2 and the Solanum demissum immune receptor R2 to mediate disease resistance. The Plant Cell. 24 (8): 3420 — 3434.
Google Scholar
Schornack S., Huitema E., Cano L. M., Bozkurt T. O., Oliva R., van Damme M., Schwizer S., Raffaele S., Chaparro-Garcia A., Farrer R., Segretin M. E., Bos J., Haas B. J., Zody M. C., Nusbaum C., Win J., Thines M., Kamoun S. 2009. Ten things to know about oomycete effectors. Molecular Plant Pathology. 10 (6): 795 — 803.
Google Scholar
Stassen J. H. M., Van den Ackerveken G. 2011. How do oomycete effectors interfere with plant life? Current Opinion in Plant Biology. 14: 407 — 414.
Google Scholar
van Damme M., Schornack S., Cano L. M., Huitema E., Kamoun S. 2009. Interactions between Phytophthora infestans and Solanum. In: K. Lamour and S. Kamoun (ed.), Oomycete Genetics and Genomics. Diversity, Interactions, and Research Tools. Hoboken, New Jersey: Wiley — Blackwell.: 287 — 302.
Google Scholar
van Damme M., Cano L. M., Oliva R., Schornack S., Segretin M. E., Kamoun S., Raffaele S. 2011. Evolutionary and functional dynamics of oomycete effector genes. In: F. Martin i S. Kamoun (ed.), Effectors in plant — microbe interactions. Wiley — Blackwell.
Google Scholar
van Poppel P. M. J. A. 2009. The Phytophthora infestans avirulence gene PiAvr4 and its potato counterpart R4. Phd thesis. ISBN 978-90-85858-306-0.
Google Scholar
van Poppel P. M. J. A., Jiang R. H. Y., Śliwka J., Govers F. 2009. Recognition of Phytophthora infestans Avr4 by potato R4 is triggered by C-terminal domains comprising W motifs. Molecular Plant Pathology. 10 (5): 611 — 620.
Google Scholar
Vleeshouwers V. G. A. A., Raffaele S., Vossen J., Champouret N., Oliva R., Segretin M. E., Rietman H., Cano L. M., Lokossou A., Kessel G., Pel M. A., Kamoun S. 2011. Understanding and exploiting late blight resistance in the age of effectors. Annu. Rev. Phytopathol. 49: 507 — 531
Google Scholar
Vleeshouwers V. G. A. A., Oliver R. P. 2014. Effectors as tools in disease resistance breeding against biotrophic, hemibiotrophic, and necrotrophic plant pathogens. Molecular Plant-Microbe Interactions. 27(3): 196 — 206.
Google Scholar
Wawra S., Belmonte R., Löbach L., Saraiva M., Willems A., van West P. 2012. Secretion, delivery and function of oomycete effector proteins. Current Opinion in Microbiology. 15: 685 — 691.
Google Scholar
Whisson S. C., Avrova A. O., Boevink P. C., Armstrong M. R., Seman Z. A., Hein I., Birch P. R. J. 2011. Exploiting knowledge of pathogen effectors to enhance late blight resistance Potato. Potato Research. 54: 325 — 340.
Google Scholar
Win J., Chaparro-Garcia A., Belhaj K., Saunders D. G. O., Yoshida K., Dong S., Schornack S., Zipfel C., Robatzek S., Hogenhout S. A., Kamoun S. 2013. Effector biology of plant — associated organisms: concepts and perspectives. Cold Spring Harbor Laboratory Press. Doi: 10.1101/sqb.2012.77.015933.
Google Scholar
Yaeno T., Li H., Chaparro-Garcia A., Schornack S., Koshiba S., Watanabe S., Kigawa T., Kamoun S., Shirasu K. 2011. Phosphatidylinositol monophosphate – binding interface in the oomycete RXLR effector AVR3a is required for its stability in host cells to modulate plant immunity. PNAS. Doi: 10.1073/pnas.1106002108
Google Scholar
Authors
Marta Brylińskam.brylinska@ihar.edu.pl
Pracownia Badania Odporności na Grzyby i Bakterie, Instytut Hodowli i Aklimatyzacji Roślin — Państwowy Instytut Badawczy, Młochów Poland
Authors
Jadwiga ŚliwkaPracownia Badania Odporności na Grzyby i Bakterie, Instytut Hodowli i Aklimatyzacji Roślin — Państwowy Instytut Badawczy, Młochów Poland
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Copyright (c) 2014 Marta Brylińska, Jadwiga Śliwka
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