Finished Genome of the Fungal Wheat Pathogen Mycosphaerella graminicola Reveals Dispensome Structure, Chromosome Plasticity, and Stealth Pathogenesis

S.B. Goodwin; S. Ben M'Barek; B. Dhillon; A.H.J. Wittenberg; C.F. Crane; J.K. Hane; A.J. Foster; T.A.J. van der Lee; J. Grimwood; A. Aerts; J. Antoniw; A. Bailey; B. Bluhm; J.M. Bowler; J. Bristow; A. van der Burgt; B. Canto-Canché; A.C.L. Churchill; L. Conde-Ferràez; H.J. Cools; P.M. Coutinho; M. Csukai; P. Dehal; P. de Wit; B. Donzelli; H.G. Geest; R.C.H. van Ham; K.E. Hammond-Kosack; B. Henrissat; A. Kilian; A.K. Kobayashi; E. Koopmann; Y. Kourmpetis; A. Kuzniar; E. Lindquist; V. Lombard; C. Maliepaard; N. Martins; R. Mehrabi; J.P.H. Nap; A. Ponomarenko; J.J. Rudd; A. Salamov; J. Schmutz; H.J. Schouten; H. Shapiro; I. Stergiopoulos; S.F.F. Torriani; H. Tu; R.P. de Vries; C. Waalwijk; S.B. Ware; A. Wiebenga; L.H. Zwiers; R.P. Oliver; I.V. Grigoriev; G.H.J. Kema

doi:10.1371/journal.pgen.1002070

Finished Genome of the Fungal Wheat Pathogen Mycosphaerella graminicola Reveals Dispensome Structure, Chromosome Plasticity, and Stealth Pathogenesis

S.B. Goodwin, S. Ben M'Barek, B. Dhillon, A.H.J. Wittenberg, C.F. Crane, J.K. Hane, A.J. Foster, T.A.J. van der Lee, J. Grimwood, A. Aerts, J. Antoniw, A. Bailey, B. Bluhm, J.M. Bowler, J. Bristow, A. van der Burgt, B. Canto-Canché, A.C.L. Churchill, L. Conde-Ferràez, H.J. CoolsP.M. Coutinho, M. Csukai, P. Dehal, P. de Wit, B. Donzelli, H.G. Geest, R.C.H. van Ham, K.E. Hammond-Kosack, B. Henrissat, A. Kilian, A.K. Kobayashi, E. Koopmann, Y. Kourmpetis, A. Kuzniar, E. Lindquist, V. Lombard, C. Maliepaard, N. Martins, R. Mehrabi, J.P.H. Nap, A. Ponomarenko, J.J. Rudd, A. Salamov, J. Schmutz, H.J. Schouten, H. Shapiro, I. Stergiopoulos, S.F.F. Torriani, H. Tu, R.P. de Vries, C. Waalwijk, S.B. Ware, A. Wiebenga, L.H. Zwiers, R.P. Oliver, I.V. Grigoriev, G.H.J. Kema

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Abstract

The plant-pathogenic fungus Mycosphaerella graminicola causes septoria tritici blotch, one of the most economically important diseases of wheat worldwide and a potential threat to global food production. Unlike most other plant pathogens, M. graminicola has a long latent period during which it seems able to evade host defenses, and its genome appears to be unstable with many chromosomes that can change size or be lost during sexual reproduction. To understand its unusual mechanism of pathogenicity and high genomic plasticity, the genome of M. graminicola was sequenced more completely than that of any other filamentous fungus. The finished sequence contains 21 chromosomes, eight of which were different from those in the core genome and appear to have originated by ancient horizontal transfer from an unknown donor. The dispensable chromosomes collectively comprise the dispensome and showed extreme plasticity during sexual reproduction. A surprising feature of the M. graminicola genome was a low number of genes for enzymes that break down plant cell walls; this may represent an evolutionary response to evade detection by plant defense mechanisms. The stealth pathogenicity of M. graminicola may involve degradation of proteins rather than carbohydrates and could have evolved from an endophytic ancestor.

Original language	English
Pages (from-to)	1002070-1002070
Journal	PLoS Genetics
Volume	7
Issue number	6
DOIs	https://doi.org/10.1371/journal.pgen.1002070
Publication status	Published - 2011

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Goodwin, S. B., Ben M'Barek, S., Dhillon, B., Wittenberg, A. H. J., Crane, C. F., Hane, J. K., Foster, A. J., van der Lee, T. A. J., Grimwood, J., Aerts, A., Antoniw, J., Bailey, A., Bluhm, B., Bowler, J. M., Bristow, J., van der Burgt, A., Canto-Canché, B., Churchill, A. C. L., Conde-Ferràez, L., ... Kema, G. H. J. (2011). Finished Genome of the Fungal Wheat Pathogen Mycosphaerella graminicola Reveals Dispensome Structure, Chromosome Plasticity, and Stealth Pathogenesis. PLoS Genetics, 7(6), 1002070-1002070. https://doi.org/10.1371/journal.pgen.1002070

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title = "Finished Genome of the Fungal Wheat Pathogen Mycosphaerella graminicola Reveals Dispensome Structure, Chromosome Plasticity, and Stealth Pathogenesis",

abstract = "The plant-pathogenic fungus Mycosphaerella graminicola causes septoria tritici blotch, one of the most economically important diseases of wheat worldwide and a potential threat to global food production. Unlike most other plant pathogens, M. graminicola has a long latent period during which it seems able to evade host defenses, and its genome appears to be unstable with many chromosomes that can change size or be lost during sexual reproduction. To understand its unusual mechanism of pathogenicity and high genomic plasticity, the genome of M. graminicola was sequenced more completely than that of any other filamentous fungus. The finished sequence contains 21 chromosomes, eight of which were different from those in the core genome and appear to have originated by ancient horizontal transfer from an unknown donor. The dispensable chromosomes collectively comprise the dispensome and showed extreme plasticity during sexual reproduction. A surprising feature of the M. graminicola genome was a low number of genes for enzymes that break down plant cell walls; this may represent an evolutionary response to evade detection by plant defense mechanisms. The stealth pathogenicity of M. graminicola may involve degradation of proteins rather than carbohydrates and could have evolved from an endophytic ancestor.",

author = "S.B. Goodwin and {Ben M'Barek}, S. and B. Dhillon and A.H.J. Wittenberg and C.F. Crane and J.K. Hane and A.J. Foster and {van der Lee}, T.A.J. and J. Grimwood and A. Aerts and J. Antoniw and A. Bailey and B. Bluhm and J.M. Bowler and J. Bristow and {van der Burgt}, A. and B. Canto-Canch{\'e} and A.C.L. Churchill and L. Conde-Ferr{\`a}ez and H.J. Cools and P.M. Coutinho and M. Csukai and P. Dehal and {de Wit}, P. and B. Donzelli and H.G. Geest and {van Ham}, R.C.H. and K.E. Hammond-Kosack and B. Henrissat and A. Kilian and A.K. Kobayashi and E. Koopmann and Y. Kourmpetis and A. Kuzniar and E. Lindquist and V. Lombard and C. Maliepaard and N. Martins and R. Mehrabi and J.P.H. Nap and A. Ponomarenko and J.J. Rudd and A. Salamov and J. Schmutz and H.J. Schouten and H. Shapiro and I. Stergiopoulos and S.F.F. Torriani and H. Tu and {de Vries}, R.P. and C. Waalwijk and S.B. Ware and A. Wiebenga and L.H. Zwiers and R.P. Oliver and I.V. Grigoriev and G.H.J. Kema",

note = "Reporting year: 2011",

year = "2011",

doi = "10.1371/journal.pgen.1002070",

language = "English",

volume = "7",

pages = "1002070--1002070",

journal = "PLoS Genetics",

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publisher = "Public Library of Science",

number = "6",

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Goodwin, SB, Ben M'Barek, S, Dhillon, B, Wittenberg, AHJ, Crane, CF, Hane, JK, Foster, AJ, van der Lee, TAJ, Grimwood, J, Aerts, A, Antoniw, J, Bailey, A, Bluhm, B, Bowler, JM, Bristow, J, van der Burgt, A, Canto-Canché, B, Churchill, ACL, Conde-Ferràez, L, Cools, HJ, Coutinho, PM, Csukai, M, Dehal, P, de Wit, P, Donzelli, B, Geest, HG, van Ham, RCH, Hammond-Kosack, KE, Henrissat, B, Kilian, A, Kobayashi, AK, Koopmann, E, Kourmpetis, Y, Kuzniar, A, Lindquist, E, Lombard, V, Maliepaard, C, Martins, N, Mehrabi, R, Nap, JPH, Ponomarenko, A, Rudd, JJ, Salamov, A, Schmutz, J, Schouten, HJ, Shapiro, H, Stergiopoulos, I, Torriani, SFF, Tu, H, de Vries, RP, Waalwijk, C, Ware, SB, Wiebenga, A, Zwiers, LH, Oliver, RP, Grigoriev, IV & Kema, GHJ 2011, 'Finished Genome of the Fungal Wheat Pathogen Mycosphaerella graminicola Reveals Dispensome Structure, Chromosome Plasticity, and Stealth Pathogenesis', PLoS Genetics, vol. 7, no. 6, pp. 1002070-1002070. https://doi.org/10.1371/journal.pgen.1002070

TY - JOUR

T1 - Finished Genome of the Fungal Wheat Pathogen Mycosphaerella graminicola Reveals Dispensome Structure, Chromosome Plasticity, and Stealth Pathogenesis

AU - Goodwin, S.B.

AU - Ben M'Barek, S.

AU - Dhillon, B.

AU - Wittenberg, A.H.J.

AU - Crane, C.F.

AU - Hane, J.K.

AU - Foster, A.J.

AU - van der Lee, T.A.J.

AU - Grimwood, J.

AU - Aerts, A.

AU - Antoniw, J.

AU - Bailey, A.

AU - Bluhm, B.

AU - Bowler, J.M.

AU - Bristow, J.

AU - van der Burgt, A.

AU - Canto-Canché, B.

AU - Churchill, A.C.L.

AU - Conde-Ferràez, L.

AU - Cools, H.J.

AU - Coutinho, P.M.

AU - Csukai, M.

AU - Dehal, P.

AU - de Wit, P.

AU - Donzelli, B.

AU - Geest, H.G.

AU - van Ham, R.C.H.

AU - Hammond-Kosack, K.E.

AU - Henrissat, B.

AU - Kilian, A.

AU - Kobayashi, A.K.

AU - Koopmann, E.

AU - Kourmpetis, Y.

AU - Kuzniar, A.

AU - Lindquist, E.

AU - Lombard, V.

AU - Maliepaard, C.

AU - Martins, N.

AU - Mehrabi, R.

AU - Nap, J.P.H.

AU - Ponomarenko, A.

AU - Rudd, J.J.

AU - Salamov, A.

AU - Schmutz, J.

AU - Schouten, H.J.

AU - Shapiro, H.

AU - Stergiopoulos, I.

AU - Torriani, S.F.F.

AU - Tu, H.

AU - de Vries, R.P.

AU - Waalwijk, C.

AU - Ware, S.B.

AU - Wiebenga, A.

AU - Zwiers, L.H.

AU - Oliver, R.P.

AU - Grigoriev, I.V.

AU - Kema, G.H.J.

N1 - Reporting year: 2011

PY - 2011

Y1 - 2011

N2 - The plant-pathogenic fungus Mycosphaerella graminicola causes septoria tritici blotch, one of the most economically important diseases of wheat worldwide and a potential threat to global food production. Unlike most other plant pathogens, M. graminicola has a long latent period during which it seems able to evade host defenses, and its genome appears to be unstable with many chromosomes that can change size or be lost during sexual reproduction. To understand its unusual mechanism of pathogenicity and high genomic plasticity, the genome of M. graminicola was sequenced more completely than that of any other filamentous fungus. The finished sequence contains 21 chromosomes, eight of which were different from those in the core genome and appear to have originated by ancient horizontal transfer from an unknown donor. The dispensable chromosomes collectively comprise the dispensome and showed extreme plasticity during sexual reproduction. A surprising feature of the M. graminicola genome was a low number of genes for enzymes that break down plant cell walls; this may represent an evolutionary response to evade detection by plant defense mechanisms. The stealth pathogenicity of M. graminicola may involve degradation of proteins rather than carbohydrates and could have evolved from an endophytic ancestor.

AB - The plant-pathogenic fungus Mycosphaerella graminicola causes septoria tritici blotch, one of the most economically important diseases of wheat worldwide and a potential threat to global food production. Unlike most other plant pathogens, M. graminicola has a long latent period during which it seems able to evade host defenses, and its genome appears to be unstable with many chromosomes that can change size or be lost during sexual reproduction. To understand its unusual mechanism of pathogenicity and high genomic plasticity, the genome of M. graminicola was sequenced more completely than that of any other filamentous fungus. The finished sequence contains 21 chromosomes, eight of which were different from those in the core genome and appear to have originated by ancient horizontal transfer from an unknown donor. The dispensable chromosomes collectively comprise the dispensome and showed extreme plasticity during sexual reproduction. A surprising feature of the M. graminicola genome was a low number of genes for enzymes that break down plant cell walls; this may represent an evolutionary response to evade detection by plant defense mechanisms. The stealth pathogenicity of M. graminicola may involve degradation of proteins rather than carbohydrates and could have evolved from an endophytic ancestor.

U2 - 10.1371/journal.pgen.1002070

DO - 10.1371/journal.pgen.1002070

M3 - Article

SN - 1553-7404

VL - 7

SP - 1002070

EP - 1002070

JO - PLoS Genetics

JF - PLoS Genetics

IS - 6

ER -

Finished Genome of the Fungal Wheat Pathogen Mycosphaerella graminicola Reveals Dispensome Structure, Chromosome Plasticity, and Stealth Pathogenesis

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