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

R.J. O'Connell; M.R. Thon; S. Hacquard; S.G. Amyotte; J. Kleemann; M.F. Torres; U. Damm; E.A. Buiate; L. Epstein; N. Alkan; J. Altmuller; L. Alvarado-Balderrama; C.A. Bauser; C. Becker; B.W. Birren; Z. Chen; J. Choi; J.A. Crouch; J.P. Duvick; M.A. Farman; P. Gan; D. Heiman; B. Henrissat; R.J. Howard; M. Kabbage; C. Koch; B. Kracher; Y. Kubo; A.D. Law; M.-H. Lebrun; Y.-H. Lee; I. Miyara; N. Moore; U. Neumann; K. Nordstrom; D.G. Panaccione; R. Panstruga; M. Place; R.H. Proctor; D. Prusky; G. Rech; R. Reinhardt; J.A. Rollins; S. Rounsley; C.L. Schardl; D.C. Schwartz; N. Shenoy; K. Shirasu; U.R. Sikhakolli; K. Stuber; S.A. Sukno; J.A. Sweigard; Y. Takano; H. Takahara; F. Trail; H.C. Does; L.M. Voll; I. Will; S. Young; Q. Zeng; Jingze Zhang; S. Zhou; M.B. Dickman; P. Schulze-Lefert; E. Verloren van Themaat; L.-J. Ma; L.J. Vaillancourt

doi:10.1038/ng.2372

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

R.J. O'Connell, M.R. Thon, S. Hacquard, S.G. Amyotte, J. Kleemann, M.F. Torres, U. Damm, E.A. Buiate, L. Epstein, N. Alkan, J. Altmuller, L. Alvarado-Balderrama, C.A. Bauser, C. Becker, B.W. Birren, Z. Chen, J. Choi, J.A. Crouch, J.P. Duvick, M.A. FarmanP. Gan, D. Heiman, B. Henrissat, R.J. Howard, M. Kabbage, C. Koch, B. Kracher, Y. Kubo, A.D. Law, M.-H. Lebrun, Y.-H. Lee, I. Miyara, N. Moore, U. Neumann, K. Nordstrom, D.G. Panaccione, R. Panstruga, M. Place, R.H. Proctor, D. Prusky, G. Rech, R. Reinhardt, J.A. Rollins, S. Rounsley, C.L. Schardl, D.C. Schwartz, N. Shenoy, K. Shirasu, U.R. Sikhakolli, K. Stuber, S.A. Sukno, J.A. Sweigard, Y. Takano, H. Takahara, F. Trail, H.C. Does, L.M. Voll, I. Will, S. Young, Q. Zeng, Jingze Zhang, S. Zhou, M.B. Dickman, P. Schulze-Lefert, E. Verloren van Themaat, L.-J. Ma, L.J. Vaillancourt

Research output: Contribution to journal/periodical › Article › Scientific › peer-review

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
Journal	Nature Genetics
Volume	44
Issue number	9
DOIs	https://doi.org/10.1038/ng.2372
Publication status	Published - 2012

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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., Altmuller, 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

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. ; Altmuller, J. ; Alvarado-Balderrama, L. ; Bauser, C.A. ; Becker, C. ; Birren, B.W. ; Chen, Z. ; Choi, J. ; Crouch, J.A. ; Duvick, J.P. ; Farman, M.A. ; Gan, P. ; Heiman, D. ; Henrissat, B. ; Howard, R.J. ; Kabbage, M. ; Koch, C. ; Kracher, B. ; Kubo, Y. ; Law, A.D. ; Lebrun, M.-H. ; Lee, Y.-H. ; Miyara, I. ; Moore, N. ; Neumann, U. ; Nordstrom, K. ; Panaccione, D.G. ; Panstruga, R. ; Place, M. ; Proctor, R.H. ; Prusky, D. ; Rech, G. ; Reinhardt, R. ; Rollins, J.A. ; Rounsley, S. ; Schardl, C.L. ; Schwartz, D.C. ; Shenoy, N. ; Shirasu, K. ; Sikhakolli, U.R. ; Stuber, K. ; Sukno, S.A. ; Sweigard, J.A. ; Takano, Y. ; Takahara, H. ; Trail, F. ; Does, H.C. ; Voll, L.M. ; Will, I. ; Young, S. ; Zeng, Q. ; Zhang, Jingze ; Zhou, S. ; Dickman, M.B. ; Schulze-Lefert, P. ; Verloren van Themaat, E. ; Ma, L.-J. ; Vaillancourt, L.J. / Lifestyle transitions in plant pathogenic Colletotrichum fungi deciphered by genome and transcriptome analyses. In: Nature Genetics. 2012 ; Vol. 44, No. 9. pp. 1060-1065.

@article{08fba88859d34d84bbdc184d16341383,

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 = "R.J. O'Connell and M.R. Thon and S. Hacquard and S.G. Amyotte and J. Kleemann and M.F. Torres and U. Damm and E.A. Buiate and L. Epstein and N. Alkan and J. Altmuller and L. Alvarado-Balderrama and C.A. Bauser and C. Becker and B.W. Birren and Z. Chen and J. Choi and J.A. Crouch and J.P. Duvick and M.A. Farman and P. Gan and D. Heiman and B. Henrissat and R.J. Howard and M. Kabbage and C. Koch and B. Kracher and Y. Kubo and A.D. Law and M.-H. Lebrun and Y.-H. Lee and I. Miyara and N. Moore and U. Neumann and K. Nordstrom and D.G. Panaccione and R. Panstruga and M. Place and R.H. Proctor and D. Prusky and G. Rech and R. Reinhardt and J.A. Rollins and S. Rounsley and C.L. Schardl and D.C. Schwartz and N. Shenoy and K. Shirasu and U.R. Sikhakolli and K. Stuber and S.A. Sukno and J.A. Sweigard and Y. Takano and H. Takahara and F. Trail and H.C. Does and L.M. Voll and I. Will and S. Young and Q. Zeng and Jingze Zhang and S. Zhou and M.B. Dickman and P. Schulze-Lefert and {Verloren van Themaat}, E. and L.-J. Ma and L.J. Vaillancourt",

note = "Reporting year: 2012",

year = "2012",

doi = "10.1038/ng.2372",

language = "English",

volume = "44",

pages = "1060--1065",

journal = "Nature Genetics",

issn = "1061-4036",

publisher = "Nature Publishing Group",

number = "9",

}

O'Connell, RJ, Thon, MR, Hacquard, S, Amyotte, SG, Kleemann, J, Torres, MF, Damm, U, Buiate, EA, Epstein, L, Alkan, N, Altmuller, 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, M-H, Lee, Y-H, Miyara, I, Moore, N, Neumann, U, Nordstrom, 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, Stuber, K, Sukno, SA, Sweigard, JA, Takano, Y, Takahara, H, Trail, F, Does, HC, Voll, LM, Will, I, Young, S, Zeng, Q, Zhang, J, Zhou, S, Dickman, MB, Schulze-Lefert, P, Verloren van Themaat, E, Ma, L-J & 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

Lifestyle transitions in plant pathogenic Colletotrichum fungi deciphered by genome and transcriptome analyses. / 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.; Altmuller, J.; Alvarado-Balderrama, L.; Bauser, C.A.; Becker, C.; Birren, B.W.; Chen, Z.; Choi, J.; Crouch, J.A.; Duvick, J.P.; Farman, M.A.; Gan, P.; Heiman, D.; Henrissat, B.; Howard, R.J.; Kabbage, M.; Koch, C.; Kracher, B.; Kubo, Y.; Law, A.D.; Lebrun, M.-H.; Lee, Y.-H.; Miyara, I.; Moore, N.; Neumann, U.; Nordstrom, K.; Panaccione, D.G.; Panstruga, R.; Place, M.; Proctor, R.H.; Prusky, D.; Rech, G.; Reinhardt, R.; Rollins, J.A.; Rounsley, S.; Schardl, C.L.; Schwartz, D.C.; Shenoy, N.; Shirasu, K.; Sikhakolli, U.R.; Stuber, K.; Sukno, S.A.; Sweigard, J.A.; Takano, Y.; Takahara, H.; Trail, F.; Does, H.C.; Voll, L.M.; Will, I.; Young, S.; Zeng, Q.; Zhang, Jingze; Zhou, S.; Dickman, M.B.; Schulze-Lefert, P.; Verloren van Themaat, E.; Ma, L.-J.; Vaillancourt, L.J.

In: Nature Genetics, Vol. 44, No. 9, 2012, p. 1060-1065.

Research output: Contribution to journal/periodical › Article › Scientific › peer-review

TY - JOUR

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

AU - O'Connell, R.J.

AU - Thon, M.R.

AU - Hacquard, S.

AU - Amyotte, S.G.

AU - Kleemann, J.

AU - Torres, M.F.

AU - Damm, U.

AU - Buiate, E.A.

AU - Epstein, L.

AU - Alkan, N.

AU - Altmuller, J.

AU - Alvarado-Balderrama, L.

AU - Bauser, C.A.

AU - Becker, C.

AU - Birren, B.W.

AU - Chen, Z.

AU - Choi, J.

AU - Crouch, J.A.

AU - Duvick, J.P.

AU - Farman, M.A.

AU - Gan, P.

AU - Heiman, D.

AU - Henrissat, B.

AU - Howard, R.J.

AU - Kabbage, M.

AU - Koch, C.

AU - Kracher, B.

AU - Kubo, Y.

AU - Law, A.D.

AU - Lebrun, M.-H.

AU - Lee, Y.-H.

AU - Miyara, I.

AU - Moore, N.

AU - Neumann, U.

AU - Nordstrom, K.

AU - Panaccione, D.G.

AU - Panstruga, R.

AU - Place, M.

AU - Proctor, R.H.

AU - Prusky, D.

AU - Rech, G.

AU - Reinhardt, R.

AU - Rollins, J.A.

AU - Rounsley, S.

AU - Schardl, C.L.

AU - Schwartz, D.C.

AU - Shenoy, N.

AU - Shirasu, K.

AU - Sikhakolli, U.R.

AU - Stuber, K.

AU - Sukno, S.A.

AU - Sweigard, J.A.

AU - Takano, Y.

AU - Takahara, H.

AU - Trail, F.

AU - Does, H.C.

AU - Voll, L.M.

AU - Will, I.

AU - Young, S.

AU - Zeng, Q.

AU - Zhang, Jingze

AU - Zhou, S.

AU - Dickman, M.B.

AU - Schulze-Lefert, P.

AU - Verloren van Themaat, E.

AU - Ma, L.-J.

AU - Vaillancourt, L.J.

N1 - Reporting year: 2012

PY - 2012

Y1 - 2012

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.

U2 - 10.1038/ng.2372

DO - 10.1038/ng.2372

M3 - Article

VL - 44

SP - 1060

EP - 1065

JO - Nature Genetics

JF - Nature Genetics

SN - 1061-4036

IS - 9

ER -

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

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