Lifestyle transitions in plant pathogenic Colletotrichum fungi deciphered by genome and transcriptome analyses

Richard J. O'Connell; Michael R. Thon; Stéphane Hacquard; Stefan G. Amyotte; Jochen Kleemann; Maria F. Torres; Ulrike Damm; Ester A. Buiate; Lynn Epstein; Noam Alkan; Janine Altmüller; Lucia Alvarado-Balderrama; Christopher A. Bauser; Christian Becker; Bruce W. Birren; Zehua Chen; Jaeyoung Choi; Jo Anne Crouch; Jonathan P. Duvick; Mark A. Farman; Pamela Gan; David Heiman; Bernard Henrissat; Richard J. Howard; Mehdi Kabbage; Christian Koch; Barbara Kracher; Yasuyuki Kubo; Audrey D. Law; Marc Henri Lebrun; Yong Hwan Lee; Itay Miyara; Neil Moore; Ulla Neumann; Karl Nordström; Daniel G. Panaccione; Ralph Panstruga; Michael Place; Robert H. Proctor; Dov Prusky; Gabriel Rech; Richard Reinhardt; Jeffrey A. Rollins; Steve Rounsley; Christopher L. Schardl; David C. Schwartz; Narmada Shenoy; Ken Shirasu; Usha R. Sikhakolli; Kurt Stüber; Serenella A. Sukno; James A. Sweigard; Yoshitaka Takano; Hiroyuki Takahara; Frances Trail; H. Charlotte Van Der Does; Lars M. Voll; Isa Will; Sarah Young; Qiandong Zeng; Jingze Zhang; Shiguo Zhou; Martin B. Dickman; Paul Schulze-Lefert; Emiel Ver Loren Van Themaat; Li Jun Ma; Lisa J. Vaillancourt

doi:10.1038/ng.2372

Lifestyle transitions in plant pathogenic Colletotrichum fungi deciphered by genome and transcriptome analyses

Richard J. O'Connell, Michael R. Thon, Stéphane Hacquard, Stefan G. Amyotte, Jochen Kleemann, Maria F. Torres, Ulrike Damm, Ester A. Buiate, Lynn Epstein, Noam Alkan, Janine Altmüller, Lucia Alvarado-Balderrama, Christopher A. Bauser, Christian Becker, Bruce W. Birren, Zehua Chen, Jaeyoung Choi, Jo Anne Crouch, Jonathan P. Duvick, Mark A. FarmanPamela Gan, David Heiman, Bernard Henrissat, Richard J. Howard, Mehdi Kabbage, Christian Koch, Barbara Kracher, Yasuyuki Kubo, Audrey D. Law, Marc Henri Lebrun, Yong Hwan Lee, Itay Miyara, Neil Moore, Ulla Neumann, Karl Nordström, Daniel G. Panaccione, Ralph Panstruga, Michael Place, Robert H. Proctor, Dov Prusky, Gabriel Rech, Richard Reinhardt, Jeffrey A. Rollins, Steve Rounsley, Christopher L. Schardl, David C. Schwartz, Narmada Shenoy, Ken Shirasu, Usha R. Sikhakolli, Kurt Stüber, Serenella A. Sukno, James A. Sweigard, Yoshitaka Takano, Hiroyuki Takahara, Frances Trail, H. Charlotte Van Der Does, Lars M. Voll, Isa Will, Sarah Young, Qiandong Zeng, Jingze Zhang, Shiguo Zhou, Martin B. Dickman, Paul Schulze-Lefert, Emiel Ver Loren Van Themaat, Li Jun Ma, Lisa J. Vaillancourt

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Abstract

Colletotrichum species are fungal pathogens that devastate crop plants worldwide. Host infection involves the differentiation of specialized cell types that are associated with penetration, growth inside living host cells (biotrophy) and tissue destruction (necrotrophy). We report here genome and transcriptome analyses of Colletotrichum higginsianum infecting Arabidopsis thaliana and Colletotrichum graminicola infecting maize. Comparative genomics showed that both fungi have large sets of pathogenicity-related genes, but families of genes encoding secreted effectors, pectin-degrading enzymes, secondary metabolism enzymes, transporters and peptidases are expanded in C. higginsianum. Genome-wide expression profiling revealed that these genes are transcribed in successive waves that are linked to pathogenic transitions: effectors and secondary metabolism enzymes are induced before penetration and during biotrophy, whereas most hydrolases and transporters are upregulated later, at the switch to necrotrophy. Our findings show that preinvasion perception of plant-derived signals substantially reprograms fungal gene expression and indicate previously unknown functions for particular fungal cell types.

Original language	English
Pages (from-to)	1060-1065
Number of pages	6
Journal	Nature Genetics
Volume	44
Issue number	9
DOIs	https://doi.org/10.1038/ng.2372
State	Published - Sep 2012

Bibliographical note

Funding Information:
This manuscript is dedicated to the memory of Robert Hanau. This work was primarily supported by US Department of Agriculture (USDA)–Cooperative State Research, Education and Extension Service (CSREES) grant 2007-35600-17829 (L.J.V., M.B.D., S.R. and M.R.T.), the Max Planck Society (R.J.O.) and Deutsche Forschungsgemeinschaft (SPP1212) grant OC 104/1-3 (R.J.O.). Other funding sources included USDA-CSREES grant 2009-34457-20125 (L.J.V.), the University of Kentucky College of Agriculture Research Office (L.J.V.), Ministerio de Ciencia e Innovación (MICINN) of Spain grants AGL2008-03177/AGR and AGL2011-29446/AGR (M.R.T.) and the Programme for Promotion of Basic and Applied Research for Innovations in Bio-oriented Industry (P.G. and K. Shirasu). This is manuscript number 12-12-011, published with the approval of the Director of the University of Kentucky Agricultural Experiment Station. See the Supplementary Note for a full list of acknowledgments.

ASJC Scopus subject areas

Genetics

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10.1038/ng.2372

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O'Connell, R. J., Thon, M. R., Hacquard, S., Amyotte, S. G., Kleemann, J., Torres, M. F., Damm, U., Buiate, E. A., Epstein, L., Alkan, N., Altmüller, J., Alvarado-Balderrama, L., Bauser, C. A., Becker, C., Birren, B. W., Chen, Z., Choi, J., Crouch, J. A., Duvick, J. P., ... Vaillancourt, L. J. (2012). Lifestyle transitions in plant pathogenic Colletotrichum fungi deciphered by genome and transcriptome analyses. Nature Genetics, 44(9), 1060-1065. https://doi.org/10.1038/ng.2372

@article{df505a24f0374d8dae0e1f5f5da1fb42,

title = "Lifestyle transitions in plant pathogenic Colletotrichum fungi deciphered by genome and transcriptome analyses",

abstract = "Colletotrichum species are fungal pathogens that devastate crop plants worldwide. Host infection involves the differentiation of specialized cell types that are associated with penetration, growth inside living host cells (biotrophy) and tissue destruction (necrotrophy). We report here genome and transcriptome analyses of Colletotrichum higginsianum infecting Arabidopsis thaliana and Colletotrichum graminicola infecting maize. Comparative genomics showed that both fungi have large sets of pathogenicity-related genes, but families of genes encoding secreted effectors, pectin-degrading enzymes, secondary metabolism enzymes, transporters and peptidases are expanded in C. higginsianum. Genome-wide expression profiling revealed that these genes are transcribed in successive waves that are linked to pathogenic transitions: effectors and secondary metabolism enzymes are induced before penetration and during biotrophy, whereas most hydrolases and transporters are upregulated later, at the switch to necrotrophy. Our findings show that preinvasion perception of plant-derived signals substantially reprograms fungal gene expression and indicate previously unknown functions for particular fungal cell types.",

author = "O'Connell, {Richard J.} and Thon, {Michael R.} and St{\'e}phane Hacquard and Amyotte, {Stefan G.} and Jochen Kleemann and Torres, {Maria F.} and Ulrike Damm and Buiate, {Ester A.} and Lynn Epstein and Noam Alkan and Janine Altm{\"u}ller and Lucia Alvarado-Balderrama and Bauser, {Christopher A.} and Christian Becker and Birren, {Bruce W.} and Zehua Chen and Jaeyoung Choi and Crouch, {Jo Anne} and Duvick, {Jonathan P.} and Farman, {Mark A.} and Pamela Gan and David Heiman and Bernard Henrissat and Howard, {Richard J.} and Mehdi Kabbage and Christian Koch and Barbara Kracher and Yasuyuki Kubo and Law, {Audrey D.} and Lebrun, {Marc Henri} and Lee, {Yong Hwan} and Itay Miyara and Neil Moore and Ulla Neumann and Karl Nordstr{\"o}m and Panaccione, {Daniel G.} and Ralph Panstruga and Michael Place and Proctor, {Robert H.} and Dov Prusky and Gabriel Rech and Richard Reinhardt and Rollins, {Jeffrey A.} and Steve Rounsley and Schardl, {Christopher L.} and Schwartz, {David C.} and Narmada Shenoy and Ken Shirasu and Sikhakolli, {Usha R.} and Kurt St{\"u}ber and Sukno, {Serenella A.} and Sweigard, {James A.} and Yoshitaka Takano and Hiroyuki Takahara and Frances Trail and {Van Der Does}, {H. Charlotte} and Voll, {Lars M.} and Isa Will and Sarah Young and Qiandong Zeng and Jingze Zhang and Shiguo Zhou and Dickman, {Martin B.} and Paul Schulze-Lefert and {Ver Loren Van Themaat}, Emiel and Ma, {Li Jun} and Vaillancourt, {Lisa J.}",

note = "Funding Information: This manuscript is dedicated to the memory of Robert Hanau. This work was primarily supported by US Department of Agriculture (USDA)–Cooperative State Research, Education and Extension Service (CSREES) grant 2007-35600-17829 (L.J.V., M.B.D., S.R. and M.R.T.), the Max Planck Society (R.J.O.) and Deutsche Forschungsgemeinschaft (SPP1212) grant OC 104/1-3 (R.J.O.). Other funding sources included USDA-CSREES grant 2009-34457-20125 (L.J.V.), the University of Kentucky College of Agriculture Research Office (L.J.V.), Ministerio de Ciencia e Innovaci{\'o}n (MICINN) of Spain grants AGL2008-03177/AGR and AGL2011-29446/AGR (M.R.T.) and the Programme for Promotion of Basic and Applied Research for Innovations in Bio-oriented Industry (P.G. and K. Shirasu). This is manuscript number 12-12-011, published with the approval of the Director of the University of Kentucky Agricultural Experiment Station. See the Supplementary Note for a full list of acknowledgments.",

year = "2012",

month = sep,

doi = "10.1038/ng.2372",

language = "English",

volume = "44",

pages = "1060--1065",

number = "9",

}

O'Connell, RJ, Thon, MR, Hacquard, S, Amyotte, SG, Kleemann, J, Torres, MF, Damm, U, Buiate, EA, Epstein, L, Alkan, N, Altmüller, J, Alvarado-Balderrama, L, Bauser, CA, Becker, C, Birren, BW, Chen, Z, Choi, J, Crouch, JA, Duvick, JP, Farman, MA, Gan, P, Heiman, D, Henrissat, B, Howard, RJ, Kabbage, M, Koch, C, Kracher, B, Kubo, Y, Law, AD, Lebrun, MH, Lee, YH, Miyara, I, Moore, N, Neumann, U, Nordström, K, Panaccione, DG, Panstruga, R, Place, M, Proctor, RH, Prusky, D, Rech, G, Reinhardt, R, Rollins, JA, Rounsley, S, Schardl, CL, Schwartz, DC, Shenoy, N, Shirasu, K, Sikhakolli, UR, Stüber, K, Sukno, SA, Sweigard, JA, Takano, Y, Takahara, H, Trail, F, Van Der Does, HC, Voll, LM, Will, I, Young, S, Zeng, Q, Zhang, J, Zhou, S, Dickman, MB, Schulze-Lefert, P, Ver Loren Van Themaat, E, Ma, LJ & Vaillancourt, LJ 2012, 'Lifestyle transitions in plant pathogenic Colletotrichum fungi deciphered by genome and transcriptome analyses', Nature Genetics, vol. 44, no. 9, pp. 1060-1065. https://doi.org/10.1038/ng.2372

TY - JOUR

T1 - Lifestyle transitions in plant pathogenic Colletotrichum fungi deciphered by genome and transcriptome analyses

AU - O'Connell, Richard J.

AU - Thon, Michael R.

AU - Hacquard, Stéphane

AU - Amyotte, Stefan G.

AU - Kleemann, Jochen

AU - Torres, Maria F.

AU - Damm, Ulrike

AU - Buiate, Ester A.

AU - Epstein, Lynn

AU - Alkan, Noam

AU - Altmüller, Janine

AU - Alvarado-Balderrama, Lucia

AU - Bauser, Christopher A.

AU - Becker, Christian

AU - Birren, Bruce W.

AU - Chen, Zehua

AU - Choi, Jaeyoung

AU - Crouch, Jo Anne

AU - Duvick, Jonathan P.

AU - Farman, Mark A.

AU - Gan, Pamela

AU - Heiman, David

AU - Henrissat, Bernard

AU - Howard, Richard J.

AU - Kabbage, Mehdi

AU - Koch, Christian

AU - Kracher, Barbara

AU - Kubo, Yasuyuki

AU - Law, Audrey D.

AU - Lebrun, Marc Henri

AU - Lee, Yong Hwan

AU - Miyara, Itay

AU - Moore, Neil

AU - Neumann, Ulla

AU - Nordström, Karl

AU - Panaccione, Daniel G.

AU - Panstruga, Ralph

AU - Place, Michael

AU - Proctor, Robert H.

AU - Prusky, Dov

AU - Rech, Gabriel

AU - Reinhardt, Richard

AU - Rollins, Jeffrey A.

AU - Rounsley, Steve

AU - Schardl, Christopher L.

AU - Schwartz, David C.

AU - Shenoy, Narmada

AU - Shirasu, Ken

AU - Sikhakolli, Usha R.

AU - Stüber, Kurt

AU - Sukno, Serenella A.

AU - Sweigard, James A.

AU - Takano, Yoshitaka

AU - Takahara, Hiroyuki

AU - Trail, Frances

AU - Van Der Does, H. Charlotte

AU - Voll, Lars M.

AU - Will, Isa

AU - Young, Sarah

AU - Zeng, Qiandong

AU - Zhang, Jingze

AU - Zhou, Shiguo

AU - Dickman, Martin B.

AU - Schulze-Lefert, Paul

AU - Ver Loren Van Themaat, Emiel

AU - Ma, Li Jun

AU - Vaillancourt, Lisa J.

N1 - Funding Information: This manuscript is dedicated to the memory of Robert Hanau. This work was primarily supported by US Department of Agriculture (USDA)–Cooperative State Research, Education and Extension Service (CSREES) grant 2007-35600-17829 (L.J.V., M.B.D., S.R. and M.R.T.), the Max Planck Society (R.J.O.) and Deutsche Forschungsgemeinschaft (SPP1212) grant OC 104/1-3 (R.J.O.). Other funding sources included USDA-CSREES grant 2009-34457-20125 (L.J.V.), the University of Kentucky College of Agriculture Research Office (L.J.V.), Ministerio de Ciencia e Innovación (MICINN) of Spain grants AGL2008-03177/AGR and AGL2011-29446/AGR (M.R.T.) and the Programme for Promotion of Basic and Applied Research for Innovations in Bio-oriented Industry (P.G. and K. Shirasu). This is manuscript number 12-12-011, published with the approval of the Director of the University of Kentucky Agricultural Experiment Station. See the Supplementary Note for a full list of acknowledgments.

PY - 2012/9

Y1 - 2012/9

N2 - Colletotrichum species are fungal pathogens that devastate crop plants worldwide. Host infection involves the differentiation of specialized cell types that are associated with penetration, growth inside living host cells (biotrophy) and tissue destruction (necrotrophy). We report here genome and transcriptome analyses of Colletotrichum higginsianum infecting Arabidopsis thaliana and Colletotrichum graminicola infecting maize. Comparative genomics showed that both fungi have large sets of pathogenicity-related genes, but families of genes encoding secreted effectors, pectin-degrading enzymes, secondary metabolism enzymes, transporters and peptidases are expanded in C. higginsianum. Genome-wide expression profiling revealed that these genes are transcribed in successive waves that are linked to pathogenic transitions: effectors and secondary metabolism enzymes are induced before penetration and during biotrophy, whereas most hydrolases and transporters are upregulated later, at the switch to necrotrophy. Our findings show that preinvasion perception of plant-derived signals substantially reprograms fungal gene expression and indicate previously unknown functions for particular fungal cell types.

AB - Colletotrichum species are fungal pathogens that devastate crop plants worldwide. Host infection involves the differentiation of specialized cell types that are associated with penetration, growth inside living host cells (biotrophy) and tissue destruction (necrotrophy). We report here genome and transcriptome analyses of Colletotrichum higginsianum infecting Arabidopsis thaliana and Colletotrichum graminicola infecting maize. Comparative genomics showed that both fungi have large sets of pathogenicity-related genes, but families of genes encoding secreted effectors, pectin-degrading enzymes, secondary metabolism enzymes, transporters and peptidases are expanded in C. higginsianum. Genome-wide expression profiling revealed that these genes are transcribed in successive waves that are linked to pathogenic transitions: effectors and secondary metabolism enzymes are induced before penetration and during biotrophy, whereas most hydrolases and transporters are upregulated later, at the switch to necrotrophy. Our findings show that preinvasion perception of plant-derived signals substantially reprograms fungal gene expression and indicate previously unknown functions for particular fungal cell types.

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U2 - 10.1038/ng.2372

DO - 10.1038/ng.2372

M3 - Article

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AN - SCOPUS:84865693932

SN - 1061-4036

VL - 44

SP - 1060

EP - 1065

JO - Nature Genetics

JF - Nature Genetics

IS - 9

ER -

Lifestyle transitions in plant pathogenic Colletotrichum fungi deciphered by genome and transcriptome analyses

Abstract

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