Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans

Brian J. Haas; Sophien Kamoun; Michael C. Zody; Rays H. Y. Jiang; Robert E. Handsaker; Liliana M. Cano; Manfred Grabherr; Chinnappa D. Kodira; Sylvain Raffaele; Trudy Torto-Alalibo; Tolga O. Bozkurt; Audrey M. V. Ah-Fong; Lucia Alvarado; Vicky L. Anderson; Miles R. Armstrong; Anna Avrova; Laura Baxter; Jim Beynon; Petra C. Boevink; Stephanie R. Bollmann; Jorunn I. B. Bos; Vincent Bulone; Guohong Cai; Cahid Cakir; James C. Carrington; Megan Chawner; Lucio Conti; Stefano Costanzo; Richard Ewan; Noah Fahlgren; Michael A. Fischbach; Johanna Fugelstad; Eleanor M. Gilroy; Sante Gnerre; Pamela J. Green; Laura J. Grenville-Briggs; John Griffith; Niklaus J. Grünwald; Karolyn Horn; Neil R. Horner; Chia-Hui Hu; Edgar Huitema; Dong-Hoon Jeong; Alexandra M. E. Jones; Jonathan D. G. Jones; Richard W. Jones; Elinor K. Karlsson; Sridhara G. Kunjeti; Kurt Lamour; Zhenyu Liu; LiJun Ma; Daniel MacLean; Marcus C. Chibucos; Hayes McDonald; Jessica McWalters; Harold J. G. Meijer; William Morgan; Paul F. Morris; Carol A. Munro; Keith O'Neill; Manuel Ospina-Giraldo; Andrés Pinzón; Leighton Pritchard; Bernard Ramsahoye; Qinghu Ren; Silvia Restrepo; Sourav Roy; Ari Sadanandom; Alon Savidor; Sebastian Schornack; David C. Schwartz; Ulrike D. Schumann; Ben Schwessinger; Lauren Seyer; Ted Sharpe; Cristina Silvar; Jing Song; David J. Studholme; Sean Sykes; Marco Thines; Peter J. I. van de Vondervoort; Vipaporn Phuntumart; Stephan Wawra; Rob Weide; Joe Win; Carolyn Young; Shiguo Zhou; William Fry; Blake C. Meyers; Pieter van West; Jean Ristaino; Francine Govers; Paul R. J. Birch; Stephen C. Whisson; Howard S. Judelson; Chad Nusbaum

doi:10.1038/nature08358

Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans

Brian J. Haas, Sophien Kamoun^*, Michael C. Zody, Rays H. Y. Jiang, Robert E. Handsaker, Liliana M. Cano, Manfred Grabherr, Chinnappa D. Kodira, Sylvain Raffaele, Trudy Torto-Alalibo, Tolga O. Bozkurt, Audrey M. V. Ah-Fong, Lucia Alvarado, Vicky L. Anderson, Miles R. Armstrong, Anna Avrova, Laura Baxter, Jim Beynon, Petra C. Boevink, Stephanie R. BollmannJorunn I. B. Bos, Vincent Bulone, Guohong Cai, Cahid Cakir, James C. Carrington, Megan Chawner, Lucio Conti, Stefano Costanzo, Richard Ewan, Noah Fahlgren, Michael A. Fischbach, Johanna Fugelstad, Eleanor M. Gilroy, Sante Gnerre, Pamela J. Green, Laura J. Grenville-Briggs, John Griffith, Niklaus J. Grünwald, Karolyn Horn, Neil R. Horner, Chia-Hui Hu, Edgar Huitema, Dong-Hoon Jeong, Alexandra M. E. Jones, Jonathan D. G. Jones, Richard W. Jones, Elinor K. Karlsson, Sridhara G. Kunjeti, Kurt Lamour, Zhenyu Liu, LiJun Ma, Daniel MacLean, Marcus C. Chibucos, Hayes McDonald, Jessica McWalters, Harold J. G. Meijer, William Morgan, Paul F. Morris, Carol A. Munro, Keith O'Neill, Manuel Ospina-Giraldo, Andrés Pinzón, Leighton Pritchard, Bernard Ramsahoye, Qinghu Ren, Silvia Restrepo, Sourav Roy, Ari Sadanandom, Alon Savidor, Sebastian Schornack, David C. Schwartz, Ulrike D. Schumann, Ben Schwessinger, Lauren Seyer, Ted Sharpe, Cristina Silvar, Jing Song, David J. Studholme, Sean Sykes, Marco Thines, Peter J. I. van de Vondervoort, Vipaporn Phuntumart, Stephan Wawra, Rob Weide, Joe Win, Carolyn Young, Shiguo Zhou, William Fry, Blake C. Meyers, Pieter van West, Jean Ristaino, Francine Govers, Paul R. J. Birch, Stephen C. Whisson, Howard S. Judelson, Chad Nusbaum

^*Corresponding author for this work

Strathclyde Institute Of Pharmacy And Biomedical Sciences

Research output: Contribution to journal › Article › peer-review

1199 Citations (Scopus)

Abstract

Phytophthora infestans is the most destructive pathogen of potato and a model organism for the oomycetes, a distinct lineage of fungus-like eukaryotes that are related to organisms such as brown algae and diatoms. As the agent of the Irish potato famine in the mid-nineteenth century, P. infestans has had a tremendous effect on human history, resulting in famine and population displacement. To this day, it affects world agriculture by causing the most destructive disease of potato, the fourth largest food crop and a critical alternative to the major cereal crops for feeding the worldĝ€™s population. Current annual worldwide potato crop losses due to late blight are conservatively estimated at $6.7 billion. Management of this devastating pathogen is challenged by its remarkable speed of adaptation to control strategies such as genetically resistant cultivars. Here we report the sequence of the P. infestans genome, which at 240 megabases (Mb) is by far the largest and most complex genome sequenced so far in the chromalveolates. Its expansion results from a proliferation of repetitive DNA accounting for 74% of the genome. Comparison with two other Phytophthora genomes showed rapid turnover and extensive expansion of specific families of secreted disease effector proteins, including many genes that are induced during infection or are predicted to have activities that alter host physiology. These fast-evolving effector genes are localized to highly dynamic and expanded regions of the P. infestans genome. This probably plays a crucial part in the rapid adaptability of the pathogen to host plants and underpins its evolutionary potential.

Original language	English
Pages (from-to)	393-398
Number of pages	6
Journal	Nature
Volume	461
Issue number	7262
DOIs	https://doi.org/10.1038/nature08358
Publication status	Published - 9 Sept 2009

Funding

Acknowledgements We thank L. Gaffney for help with figures and tables, E. Blanco and R. Guigo for training the GeneID gene prediction software, J. Crabtree for providing a Sybil (http://sybil.sf.net) software component used to render genome comparison illustrations, the Broad Institute Genome Sequencing Platform for sequence data generation, and C. Cuomo and D. Neafsey for comments on the manuscript. The project was supported by the National Research Initiative of the USDA Cooperative State Research, Education and Extension Service, grant numbers 2004-35600-15024 and 2006-35600-16623, and the National Science Foundation grants EF-0333274 and EF-0523670, and the Gatsby Charitable Foundation.

Keywords

phytophthora infestans
Irish potato famine
plant pathogen

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10.1038/nature08358

Cite this

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., ... Nusbaum, C. (2009). Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature, 461(7262), 393-398. https://doi.org/10.1038/nature08358

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title = "Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans",

abstract = "Phytophthora infestans is the most destructive pathogen of potato and a model organism for the oomycetes, a distinct lineage of fungus-like eukaryotes that are related to organisms such as brown algae and diatoms. As the agent of the Irish potato famine in the mid-nineteenth century, P. infestans has had a tremendous effect on human history, resulting in famine and population displacement. To this day, it affects world agriculture by causing the most destructive disease of potato, the fourth largest food crop and a critical alternative to the major cereal crops for feeding the worldĝ€{\texttrademark}s population. Current annual worldwide potato crop losses due to late blight are conservatively estimated at $6.7 billion. Management of this devastating pathogen is challenged by its remarkable speed of adaptation to control strategies such as genetically resistant cultivars. Here we report the sequence of the P. infestans genome, which at 240 megabases (Mb) is by far the largest and most complex genome sequenced so far in the chromalveolates. Its expansion results from a proliferation of repetitive DNA accounting for 74% of the genome. Comparison with two other Phytophthora genomes showed rapid turnover and extensive expansion of specific families of secreted disease effector proteins, including many genes that are induced during infection or are predicted to have activities that alter host physiology. These fast-evolving effector genes are localized to highly dynamic and expanded regions of the P. infestans genome. This probably plays a crucial part in the rapid adaptability of the pathogen to host plants and underpins its evolutionary potential.",

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Haas, BJ, Kamoun, S, Zody, MC, Jiang, RHY, Handsaker, RE, Cano, LM, Grabherr, M, Kodira, CD, Raffaele, S, Torto-Alalibo, T, Bozkurt, TO, Ah-Fong, AMV, Alvarado, L, Anderson, VL, Armstrong, MR, Avrova, A, Baxter, L, Beynon, J, Boevink, PC, Bollmann, SR, Bos, JIB, Bulone, V, Cai, G, Cakir, C, Carrington, JC, Chawner, M, Conti, L, Costanzo, S, Ewan, R, Fahlgren, N, Fischbach, MA, Fugelstad, J, Gilroy, EM, Gnerre, S, Green, PJ, Grenville-Briggs, LJ, Griffith, J, Grünwald, NJ, Horn, K, Horner, NR, Hu, C-H, Huitema, E, Jeong, D-H, Jones, AME, Jones, JDG, Jones, RW, Karlsson, EK, Kunjeti, SG, Lamour, K, Liu, Z, Ma, L, MacLean, D, Chibucos, MC, McDonald, H, McWalters, J, Meijer, HJG, Morgan, W, Morris, PF, Munro, CA, O'Neill, K, Ospina-Giraldo, M, Pinzón, A, Pritchard, L, Ramsahoye, B, Ren, Q, Restrepo, S, Roy, S, Sadanandom, A, Savidor, A, Schornack, S, Schwartz, DC, Schumann, UD, Schwessinger, B, Seyer, L, Sharpe, T, Silvar, C, Song, J, Studholme, DJ, Sykes, S, Thines, M, van de Vondervoort, PJI, Phuntumart, V, Wawra, S, Weide, R, Win, J, Young, C, Zhou, S, Fry, W, Meyers, BC, van West, P, Ristaino, J, Govers, F, Birch, PRJ, Whisson, SC, Judelson, HS & Nusbaum, C 2009, 'Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans', Nature, vol. 461, no. 7262, pp. 393-398. https://doi.org/10.1038/nature08358

TY - JOUR

T1 - Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans

AU - Haas, Brian J.

AU - Kamoun, Sophien

AU - Zody, Michael C.

AU - Jiang, Rays H. Y.

AU - Handsaker, Robert E.

AU - Cano, Liliana M.

AU - Grabherr, Manfred

AU - Kodira, Chinnappa D.

AU - Raffaele, Sylvain

AU - Torto-Alalibo, Trudy

AU - Bozkurt, Tolga O.

AU - Ah-Fong, Audrey M. V.

AU - Alvarado, Lucia

AU - Anderson, Vicky L.

AU - Armstrong, Miles R.

AU - Avrova, Anna

AU - Baxter, Laura

AU - Beynon, Jim

AU - Boevink, Petra C.

AU - Bollmann, Stephanie R.

AU - Bos, Jorunn I. B.

AU - Bulone, Vincent

AU - Cai, Guohong

AU - Cakir, Cahid

AU - Carrington, James C.

AU - Chawner, Megan

AU - Conti, Lucio

AU - Costanzo, Stefano

AU - Ewan, Richard

AU - Fahlgren, Noah

AU - Fischbach, Michael A.

AU - Fugelstad, Johanna

AU - Gilroy, Eleanor M.

AU - Gnerre, Sante

AU - Green, Pamela J.

AU - Grenville-Briggs, Laura J.

AU - Griffith, John

AU - Grünwald, Niklaus J.

AU - Horn, Karolyn

AU - Horner, Neil R.

AU - Hu, Chia-Hui

AU - Huitema, Edgar

AU - Jeong, Dong-Hoon

AU - Jones, Alexandra M. E.

AU - Jones, Jonathan D. G.

AU - Jones, Richard W.

AU - Karlsson, Elinor K.

AU - Kunjeti, Sridhara G.

AU - Lamour, Kurt

AU - Liu, Zhenyu

AU - Ma, LiJun

AU - MacLean, Daniel

AU - Chibucos, Marcus C.

AU - McDonald, Hayes

AU - McWalters, Jessica

AU - Meijer, Harold J. G.

AU - Morgan, William

AU - Morris, Paul F.

AU - Munro, Carol A.

AU - O'Neill, Keith

AU - Ospina-Giraldo, Manuel

AU - Pinzón, Andrés

AU - Pritchard, Leighton

AU - Ramsahoye, Bernard

AU - Ren, Qinghu

AU - Restrepo, Silvia

AU - Roy, Sourav

AU - Sadanandom, Ari

AU - Savidor, Alon

AU - Schornack, Sebastian

AU - Schwartz, David C.

AU - Schumann, Ulrike D.

AU - Schwessinger, Ben

AU - Seyer, Lauren

AU - Sharpe, Ted

AU - Silvar, Cristina

AU - Song, Jing

AU - Studholme, David J.

AU - Sykes, Sean

AU - Thines, Marco

AU - van de Vondervoort, Peter J. I.

AU - Phuntumart, Vipaporn

AU - Wawra, Stephan

AU - Weide, Rob

AU - Win, Joe

AU - Young, Carolyn

AU - Zhou, Shiguo

AU - Fry, William

AU - Meyers, Blake C.

AU - van West, Pieter

AU - Ristaino, Jean

AU - Govers, Francine

AU - Birch, Paul R. J.

AU - Whisson, Stephen C.

AU - Judelson, Howard S.

AU - Nusbaum, Chad

PY - 2009/9/9

Y1 - 2009/9/9

N2 - Phytophthora infestans is the most destructive pathogen of potato and a model organism for the oomycetes, a distinct lineage of fungus-like eukaryotes that are related to organisms such as brown algae and diatoms. As the agent of the Irish potato famine in the mid-nineteenth century, P. infestans has had a tremendous effect on human history, resulting in famine and population displacement. To this day, it affects world agriculture by causing the most destructive disease of potato, the fourth largest food crop and a critical alternative to the major cereal crops for feeding the worldĝ€™s population. Current annual worldwide potato crop losses due to late blight are conservatively estimated at $6.7 billion. Management of this devastating pathogen is challenged by its remarkable speed of adaptation to control strategies such as genetically resistant cultivars. Here we report the sequence of the P. infestans genome, which at 240 megabases (Mb) is by far the largest and most complex genome sequenced so far in the chromalveolates. Its expansion results from a proliferation of repetitive DNA accounting for 74% of the genome. Comparison with two other Phytophthora genomes showed rapid turnover and extensive expansion of specific families of secreted disease effector proteins, including many genes that are induced during infection or are predicted to have activities that alter host physiology. These fast-evolving effector genes are localized to highly dynamic and expanded regions of the P. infestans genome. This probably plays a crucial part in the rapid adaptability of the pathogen to host plants and underpins its evolutionary potential.

AB - Phytophthora infestans is the most destructive pathogen of potato and a model organism for the oomycetes, a distinct lineage of fungus-like eukaryotes that are related to organisms such as brown algae and diatoms. As the agent of the Irish potato famine in the mid-nineteenth century, P. infestans has had a tremendous effect on human history, resulting in famine and population displacement. To this day, it affects world agriculture by causing the most destructive disease of potato, the fourth largest food crop and a critical alternative to the major cereal crops for feeding the worldĝ€™s population. Current annual worldwide potato crop losses due to late blight are conservatively estimated at $6.7 billion. Management of this devastating pathogen is challenged by its remarkable speed of adaptation to control strategies such as genetically resistant cultivars. Here we report the sequence of the P. infestans genome, which at 240 megabases (Mb) is by far the largest and most complex genome sequenced so far in the chromalveolates. Its expansion results from a proliferation of repetitive DNA accounting for 74% of the genome. Comparison with two other Phytophthora genomes showed rapid turnover and extensive expansion of specific families of secreted disease effector proteins, including many genes that are induced during infection or are predicted to have activities that alter host physiology. These fast-evolving effector genes are localized to highly dynamic and expanded regions of the P. infestans genome. This probably plays a crucial part in the rapid adaptability of the pathogen to host plants and underpins its evolutionary potential.

KW - phytophthora infestans

KW - Irish potato famine

KW - plant pathogen

UR - http://www.scopus.com/inward/record.url?scp=70349281388&partnerID=8YFLogxK

U2 - 10.1038/nature08358

DO - 10.1038/nature08358

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AN - SCOPUS:70349281388

SN - 0028-0836

VL - 461

SP - 393

EP - 398

JO - Nature

JF - Nature

IS - 7262

ER -

Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans

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