Survival trade-offs in plant roots during colonization by closely related beneficial and pathogenic fungi

Stéphane Hacquard; Barbara Kracher; Kei Hiruma; Philipp C Münch; Ruben Garrido-Oter; Michael R Thon; Aaron Weimann; U. Damm; Jean-Félix Dallery; Matthieu Hainaut; Bernard Henrissat; Olivier Lespinet; Soledad Sacristán; Emiel Ver Loren van Themaat; Eric Kemen; Alice C McHardy; Paul Schulze-Lefert; Richard J O'Connell

doi:10.1038/ncomms11362

Survival trade-offs in plant roots during colonization by closely related beneficial and pathogenic fungi

Stéphane Hacquard, Barbara Kracher, Kei Hiruma, Philipp C Münch, Ruben Garrido-Oter, Michael R Thon, Aaron Weimann, U. Damm, Jean-Félix Dallery, Matthieu Hainaut, Bernard Henrissat, Olivier Lespinet, Soledad Sacristán, Emiel Ver Loren van Themaat, Eric Kemen, Alice C McHardy, Paul Schulze-Lefert, Richard J O'Connell

Onderzoeksoutput: Bijdrage aan wetenschappelijk tijdschrift/periodieke uitgave › Artikel › Wetenschappelijk › peer review

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The sessile nature of plants forced them to evolve mechanisms to prioritize their responses to simultaneous stresses, including colonization by microbes or nutrient starvation. Here, we compare the genomes of a beneficial root endophyte, Colletotrichum tofieldiae and its pathogenic relative C. incanum, and examine the transcriptomes of both fungi and their plant host Arabidopsis during phosphate starvation. Although the two species diverged only 8.8 million years ago and have similar gene arsenals, we identify genomic signatures indicative of an evolutionary transition from pathogenic to beneficial lifestyles, including a narrowed repertoire of secreted effector proteins, expanded families of chitin-binding and secondary metabolism-related proteins, and limited activation of pathogenicity-related genes in planta. We show that beneficial responses are prioritized in C. tofieldiae-colonized roots under phosphate-deficient conditions, whereas defense responses are activated under phosphate-sufficient conditions. These immune responses are retained in phosphate-starved roots colonized by pathogenic C. incanum, illustrating the ability of plants to maximize survival in response to conflicting stresses.

Originele taal-2	Engels
Artikelnummer	11362
Aantal pagina's	12
Tijdschrift	Nature Communications
Volume	7
DOI's	https://doi.org/10.1038/ncomms11362
Status	Gepubliceerd - 06 mei 2016

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10.1038/ncomms11362

http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4859067/

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Hacquard, S., Kracher, B., Hiruma, K., Münch, P. C., Garrido-Oter, R., Thon, M. R., Weimann, A., Damm, U., Dallery, J-F., Hainaut, M., Henrissat, B., Lespinet, O., Sacristán, S., Ver Loren van Themaat, E., Kemen, E., McHardy, A. C., Schulze-Lefert, P., & O'Connell, R. J. (2016). Survival trade-offs in plant roots during colonization by closely related beneficial and pathogenic fungi. Nature Communications, 7, [11362]. https://doi.org/10.1038/ncomms11362

Hacquard, Stéphane ; Kracher, Barbara ; Hiruma, Kei ; Münch, Philipp C ; Garrido-Oter, Ruben ; Thon, Michael R ; Weimann, Aaron ; Damm, U. ; Dallery, Jean-Félix ; Hainaut, Matthieu ; Henrissat, Bernard ; Lespinet, Olivier ; Sacristán, Soledad ; Ver Loren van Themaat, Emiel ; Kemen, Eric ; McHardy, Alice C ; Schulze-Lefert, Paul ; O'Connell, Richard J. / Survival trade-offs in plant roots during colonization by closely related beneficial and pathogenic fungi. In: Nature Communications. 2016 ; Vol. 7.

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title = "Survival trade-offs in plant roots during colonization by closely related beneficial and pathogenic fungi",

abstract = "The sessile nature of plants forced them to evolve mechanisms to prioritize their responses to simultaneous stresses, including colonization by microbes or nutrient starvation. Here, we compare the genomes of a beneficial root endophyte, Colletotrichum tofieldiae and its pathogenic relative C. incanum, and examine the transcriptomes of both fungi and their plant host Arabidopsis during phosphate starvation. Although the two species diverged only 8.8 million years ago and have similar gene arsenals, we identify genomic signatures indicative of an evolutionary transition from pathogenic to beneficial lifestyles, including a narrowed repertoire of secreted effector proteins, expanded families of chitin-binding and secondary metabolism-related proteins, and limited activation of pathogenicity-related genes in planta. We show that beneficial responses are prioritized in C. tofieldiae-colonized roots under phosphate-deficient conditions, whereas defense responses are activated under phosphate-sufficient conditions. These immune responses are retained in phosphate-starved roots colonized by pathogenic C. incanum, illustrating the ability of plants to maximize survival in response to conflicting stresses.",

author = "St{\'e}phane Hacquard and Barbara Kracher and Kei Hiruma and M{\"u}nch, {Philipp C} and Ruben Garrido-Oter and Thon, {Michael R} and Aaron Weimann and U. Damm and Jean-F{\'e}lix Dallery and Matthieu Hainaut and Bernard Henrissat and Olivier Lespinet and Soledad Sacrist{\'a}n and {Ver Loren van Themaat}, Emiel and Eric Kemen and McHardy, {Alice C} and Paul Schulze-Lefert and O'Connell, {Richard J}",

year = "2016",

month = may,

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Hacquard, S, Kracher, B, Hiruma, K, Münch, PC, Garrido-Oter, R, Thon, MR, Weimann, A, Damm, U, Dallery, J-F, Hainaut, M, Henrissat, B, Lespinet, O, Sacristán, S, Ver Loren van Themaat, E, Kemen, E, McHardy, AC, Schulze-Lefert, P & O'Connell, RJ 2016, 'Survival trade-offs in plant roots during colonization by closely related beneficial and pathogenic fungi', Nature Communications, vol. 7, 11362. https://doi.org/10.1038/ncomms11362

Survival trade-offs in plant roots during colonization by closely related beneficial and pathogenic fungi. / Hacquard, Stéphane; Kracher, Barbara; Hiruma, Kei; Münch, Philipp C; Garrido-Oter, Ruben; Thon, Michael R; Weimann, Aaron; Damm, U.; Dallery, Jean-Félix; Hainaut, Matthieu; Henrissat, Bernard; Lespinet, Olivier; Sacristán, Soledad; Ver Loren van Themaat, Emiel; Kemen, Eric; McHardy, Alice C; Schulze-Lefert, Paul; O'Connell, Richard J.

In: Nature Communications, Vol. 7, 11362, 06.05.2016.

Onderzoeksoutput: Bijdrage aan wetenschappelijk tijdschrift/periodieke uitgave › Artikel › Wetenschappelijk › peer review

TY - JOUR

T1 - Survival trade-offs in plant roots during colonization by closely related beneficial and pathogenic fungi

AU - Hacquard, Stéphane

AU - Kracher, Barbara

AU - Hiruma, Kei

AU - Münch, Philipp C

AU - Garrido-Oter, Ruben

AU - Thon, Michael R

AU - Weimann, Aaron

AU - Damm, U.

AU - Dallery, Jean-Félix

AU - Hainaut, Matthieu

AU - Henrissat, Bernard

AU - Lespinet, Olivier

AU - Sacristán, Soledad

AU - Ver Loren van Themaat, Emiel

AU - Kemen, Eric

AU - McHardy, Alice C

AU - Schulze-Lefert, Paul

AU - O'Connell, Richard J

PY - 2016/5/6

Y1 - 2016/5/6

N2 - The sessile nature of plants forced them to evolve mechanisms to prioritize their responses to simultaneous stresses, including colonization by microbes or nutrient starvation. Here, we compare the genomes of a beneficial root endophyte, Colletotrichum tofieldiae and its pathogenic relative C. incanum, and examine the transcriptomes of both fungi and their plant host Arabidopsis during phosphate starvation. Although the two species diverged only 8.8 million years ago and have similar gene arsenals, we identify genomic signatures indicative of an evolutionary transition from pathogenic to beneficial lifestyles, including a narrowed repertoire of secreted effector proteins, expanded families of chitin-binding and secondary metabolism-related proteins, and limited activation of pathogenicity-related genes in planta. We show that beneficial responses are prioritized in C. tofieldiae-colonized roots under phosphate-deficient conditions, whereas defense responses are activated under phosphate-sufficient conditions. These immune responses are retained in phosphate-starved roots colonized by pathogenic C. incanum, illustrating the ability of plants to maximize survival in response to conflicting stresses.

AB - The sessile nature of plants forced them to evolve mechanisms to prioritize their responses to simultaneous stresses, including colonization by microbes or nutrient starvation. Here, we compare the genomes of a beneficial root endophyte, Colletotrichum tofieldiae and its pathogenic relative C. incanum, and examine the transcriptomes of both fungi and their plant host Arabidopsis during phosphate starvation. Although the two species diverged only 8.8 million years ago and have similar gene arsenals, we identify genomic signatures indicative of an evolutionary transition from pathogenic to beneficial lifestyles, including a narrowed repertoire of secreted effector proteins, expanded families of chitin-binding and secondary metabolism-related proteins, and limited activation of pathogenicity-related genes in planta. We show that beneficial responses are prioritized in C. tofieldiae-colonized roots under phosphate-deficient conditions, whereas defense responses are activated under phosphate-sufficient conditions. These immune responses are retained in phosphate-starved roots colonized by pathogenic C. incanum, illustrating the ability of plants to maximize survival in response to conflicting stresses.

U2 - 10.1038/ncomms11362

DO - 10.1038/ncomms11362

M3 - Article

VL - 7

JO - Nature Communications

JF - Nature Communications

SN - 2041-1723

M1 - 11362

ER -

Survival trade-offs in plant roots during colonization by closely related beneficial and pathogenic fungi

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