Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium

Li Jun Ma; H. Charlotte Van Der Does; Katherine A. Borkovich; Jeffrey J. Coleman; Marie Josée Daboussi; Antonio Di Pietro; Marie Dufresne; Michael Freitag; Manfred Grabherr; Bernard Henrissat; Petra M. Houterman; Seogchan Kang; Won Bo Shim; Charles Woloshuk; Xiaohui Xie; Jin Rong Xu; John Antoniw; Scott E. Baker; Burton H. Bluhm; Andrew Breakspear; Daren W. Brown; Robert A.E. Butchko; Sinead Chapman; Richard Coulson; Pedro M. Coutinho; Etienne G.J. Danchin; Andrew Diener; Liane R. Gale; Donald M. Gardiner; Stephen Goff; Kim E. Hammond-Kosack; Karen Hilburn; Aurélie Hua-Van; Wilfried Jonkers; Kemal Kazan; Chinnappa D. Kodira; Michael Koehrsen; Lokesh Kumar; Yong Hwan Lee; Liande Li; John M. Manners; Diego Miranda-Saavedra; Mala Mukherjee; Gyungsoon Park; Jongsun Park; Sook Young Park; Robert H. Proctor; Aviv Regev; M. Carmen Ruiz-Roldan; Divya Sain; Sharadha Sakthikumar; Sean Sykes; David C. Schwartz; B. Gillian Turgeon; Ilan Wapinski; Olen Yoder; Sarah Young; Qiandong Zeng; Shiguo Zhou; James Galagan; Christina A. Cuomo; H. Corby Kistler; Martijn Rep

doi:10.1038/nature08850

Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium

Li Jun Ma, H. Charlotte Van Der Does, Katherine A. Borkovich, Jeffrey J. Coleman, Marie Josée Daboussi, Antonio Di Pietro, Marie Dufresne, Michael Freitag, Manfred Grabherr, Bernard Henrissat, Petra M. Houterman, Seogchan Kang, Won Bo Shim, Charles Woloshuk, Xiaohui Xie, Jin Rong Xu, John Antoniw, Scott E. Baker, Burton H. Bluhm, Andrew BreakspearDaren W. Brown, Robert A.E. Butchko, Sinead Chapman, Richard Coulson, Pedro M. Coutinho, Etienne G.J. Danchin, Andrew Diener, Liane R. Gale, Donald M. Gardiner, Stephen Goff, Kim E. Hammond-Kosack, Karen Hilburn, Aurélie Hua-Van, Wilfried Jonkers, Kemal Kazan, Chinnappa D. Kodira, Michael Koehrsen, Lokesh Kumar, Yong Hwan Lee, Liande Li, John M. Manners, Diego Miranda-Saavedra, Mala Mukherjee, Gyungsoon Park, Jongsun Park, Sook Young Park, Robert H. Proctor, Aviv Regev, M. Carmen Ruiz-Roldan, Divya Sain, Sharadha Sakthikumar, Sean Sykes, David C. Schwartz, B. Gillian Turgeon, Ilan Wapinski, Olen Yoder, Sarah Young, Qiandong Zeng, Shiguo Zhou, James Galagan, Christina A. Cuomo, H. Corby Kistler, Martijn Rep

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Abstract

Fusarium species are among the most important phytopathogenic and toxigenic fungi. To understand the molecular underpinnings of pathogenicity in the genus Fusarium, we compared the genomes of three phenotypically diverse species: Fusarium graminearum, Fusarium verticillioides and Fusarium oxysporum f. sp. lycopersici. Our analysis revealed lineage-specific (LS) genomic regions in F. oxysporum that include four entire chromosomes and account for more than one-quarter of the genome. LS regions are rich in transposons and genes with distinct evolutionary profiles but related to pathogenicity, indicative of horizontal acquisition. Experimentally, we demonstrate the transfer of two LS chromosomes between strains of F. oxysporum, converting a non-pathogenic strain into a pathogen. Transfer of LS chromosomes between otherwise genetically isolated strains explains the polyphyletic origin of host specificity and the emergence of new pathogenic lineages in F. oxysporum. These findings put the evolution of fungal pathogenicity into a new perspective.

Original language	English (US)
Pages (from-to)	367-373
Number of pages	7
Journal	Nature
Volume	464
Issue number	7287
DOIs	https://doi.org/10.1038/nature08850
State	Published - Mar 18 2010

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Ma, L. J., Van Der Does, H. C., Borkovich, K. A., Coleman, J. J., Daboussi, M. J., Di Pietro, A., Dufresne, M., Freitag, M., Grabherr, M., Henrissat, B., Houterman, P. M., Kang, S., Shim, W. B., Woloshuk, C., Xie, X., Xu, J. R., Antoniw, J., Baker, S. E., Bluhm, B. H., ... Rep, M. (2010). Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature, 464(7287), 367-373. https://doi.org/10.1038/nature08850

@article{d3780fc4fac34e1ba7b5116d3d2732a3,

title = "Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium",

abstract = "Fusarium species are among the most important phytopathogenic and toxigenic fungi. To understand the molecular underpinnings of pathogenicity in the genus Fusarium, we compared the genomes of three phenotypically diverse species: Fusarium graminearum, Fusarium verticillioides and Fusarium oxysporum f. sp. lycopersici. Our analysis revealed lineage-specific (LS) genomic regions in F. oxysporum that include four entire chromosomes and account for more than one-quarter of the genome. LS regions are rich in transposons and genes with distinct evolutionary profiles but related to pathogenicity, indicative of horizontal acquisition. Experimentally, we demonstrate the transfer of two LS chromosomes between strains of F. oxysporum, converting a non-pathogenic strain into a pathogen. Transfer of LS chromosomes between otherwise genetically isolated strains explains the polyphyletic origin of host specificity and the emergence of new pathogenic lineages in F. oxysporum. These findings put the evolution of fungal pathogenicity into a new perspective.",

author = "Ma, {Li Jun} and {Van Der Does}, {H. Charlotte} and Borkovich, {Katherine A.} and Coleman, {Jeffrey J.} and Daboussi, {Marie Jos{\'e}e} and {Di Pietro}, Antonio and Marie Dufresne and Michael Freitag and Manfred Grabherr and Bernard Henrissat and Houterman, {Petra M.} and Seogchan Kang and Shim, {Won Bo} and Charles Woloshuk and Xiaohui Xie and Xu, {Jin Rong} and John Antoniw and Baker, {Scott E.} and Bluhm, {Burton H.} and Andrew Breakspear and Brown, {Daren W.} and Butchko, {Robert A.E.} and Sinead Chapman and Richard Coulson and Coutinho, {Pedro M.} and Danchin, {Etienne G.J.} and Andrew Diener and Gale, {Liane R.} and Gardiner, {Donald M.} and Stephen Goff and Hammond-Kosack, {Kim E.} and Karen Hilburn and Aur{\'e}lie Hua-Van and Wilfried Jonkers and Kemal Kazan and Kodira, {Chinnappa D.} and Michael Koehrsen and Lokesh Kumar and Lee, {Yong Hwan} and Liande Li and Manners, {John M.} and Diego Miranda-Saavedra and Mala Mukherjee and Gyungsoon Park and Jongsun Park and Park, {Sook Young} and Proctor, {Robert H.} and Aviv Regev and Ruiz-Roldan, {M. Carmen} and Divya Sain and Sharadha Sakthikumar and Sean Sykes and Schwartz, {David C.} and Turgeon, {B. Gillian} and Ilan Wapinski and Olen Yoder and Sarah Young and Qiandong Zeng and Shiguo Zhou and James Galagan and Cuomo, {Christina A.} and Kistler, {H. Corby} and Martijn Rep",

note = "Funding Information: Acknowledgements The 43 sequence of F. verticillioides was provided by Syngenta Biotechnology Inc. Generation of the other 43 sequence of F. verticillioides and 6.83 sequence of F. oxysporum f. sp. lycopersici was funded by the National Research Initiative of USDA{\textquoteright}s National Institute of Food and Agriculture through the Microbial Genome Sequencing Program (2005-35600-16405) and conducted by the Broad Institute Sequencing Platform. Wayne Xu and the Minnesota Supercomputing Institute for Advanced Computational Research are also acknowledged for their support. The authors thank Leslie Gaffney at the Broad Institute for graphic design and editing and Tracy E. Anderson of the University of Minnesota, College of Biological Sciences Imaging Center for spore micrographs.",

year = "2010",

month = mar,

day = "18",

doi = "10.1038/nature08850",

language = "English (US)",

volume = "464",

pages = "367--373",

journal = "Nature",

issn = "0028-0836",

publisher = "Nature Publishing Group",

number = "7287",

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Ma, LJ, Van Der Does, HC, Borkovich, KA, Coleman, JJ, Daboussi, MJ, Di Pietro, A, Dufresne, M, Freitag, M, Grabherr, M, Henrissat, B, Houterman, PM, Kang, S, Shim, WB, Woloshuk, C, Xie, X, Xu, JR, Antoniw, J, Baker, SE, Bluhm, BH, Breakspear, A, Brown, DW, Butchko, RAE, Chapman, S, Coulson, R, Coutinho, PM, Danchin, EGJ, Diener, A, Gale, LR, Gardiner, DM, Goff, S, Hammond-Kosack, KE, Hilburn, K, Hua-Van, A, Jonkers, W, Kazan, K, Kodira, CD, Koehrsen, M, Kumar, L, Lee, YH, Li, L, Manners, JM, Miranda-Saavedra, D, Mukherjee, M, Park, G, Park, J, Park, SY, Proctor, RH, Regev, A, Ruiz-Roldan, MC, Sain, D, Sakthikumar, S, Sykes, S, Schwartz, DC, Turgeon, BG, Wapinski, I, Yoder, O, Young, S, Zeng, Q, Zhou, S, Galagan, J, Cuomo, CA, Kistler, HC & Rep, M 2010, 'Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium', Nature, vol. 464, no. 7287, pp. 367-373. https://doi.org/10.1038/nature08850

TY - JOUR

T1 - Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium

AU - Ma, Li Jun

AU - Van Der Does, H. Charlotte

AU - Borkovich, Katherine A.

AU - Coleman, Jeffrey J.

AU - Daboussi, Marie Josée

AU - Di Pietro, Antonio

AU - Dufresne, Marie

AU - Freitag, Michael

AU - Grabherr, Manfred

AU - Henrissat, Bernard

AU - Houterman, Petra M.

AU - Kang, Seogchan

AU - Shim, Won Bo

AU - Woloshuk, Charles

AU - Xie, Xiaohui

AU - Xu, Jin Rong

AU - Antoniw, John

AU - Baker, Scott E.

AU - Bluhm, Burton H.

AU - Breakspear, Andrew

AU - Brown, Daren W.

AU - Butchko, Robert A.E.

AU - Chapman, Sinead

AU - Coulson, Richard

AU - Coutinho, Pedro M.

AU - Danchin, Etienne G.J.

AU - Diener, Andrew

AU - Gale, Liane R.

AU - Gardiner, Donald M.

AU - Goff, Stephen

AU - Hammond-Kosack, Kim E.

AU - Hilburn, Karen

AU - Hua-Van, Aurélie

AU - Jonkers, Wilfried

AU - Kazan, Kemal

AU - Kodira, Chinnappa D.

AU - Koehrsen, Michael

AU - Kumar, Lokesh

AU - Lee, Yong Hwan

AU - Li, Liande

AU - Manners, John M.

AU - Miranda-Saavedra, Diego

AU - Mukherjee, Mala

AU - Park, Gyungsoon

AU - Park, Jongsun

AU - Park, Sook Young

AU - Proctor, Robert H.

AU - Regev, Aviv

AU - Ruiz-Roldan, M. Carmen

AU - Sain, Divya

AU - Sakthikumar, Sharadha

AU - Sykes, Sean

AU - Schwartz, David C.

AU - Turgeon, B. Gillian

AU - Wapinski, Ilan

AU - Yoder, Olen

AU - Young, Sarah

AU - Zeng, Qiandong

AU - Zhou, Shiguo

AU - Galagan, James

AU - Cuomo, Christina A.

AU - Kistler, H. Corby

AU - Rep, Martijn

N1 - Funding Information: Acknowledgements The 43 sequence of F. verticillioides was provided by Syngenta Biotechnology Inc. Generation of the other 43 sequence of F. verticillioides and 6.83 sequence of F. oxysporum f. sp. lycopersici was funded by the National Research Initiative of USDA’s National Institute of Food and Agriculture through the Microbial Genome Sequencing Program (2005-35600-16405) and conducted by the Broad Institute Sequencing Platform. Wayne Xu and the Minnesota Supercomputing Institute for Advanced Computational Research are also acknowledged for their support. The authors thank Leslie Gaffney at the Broad Institute for graphic design and editing and Tracy E. Anderson of the University of Minnesota, College of Biological Sciences Imaging Center for spore micrographs.

PY - 2010/3/18

Y1 - 2010/3/18

N2 - Fusarium species are among the most important phytopathogenic and toxigenic fungi. To understand the molecular underpinnings of pathogenicity in the genus Fusarium, we compared the genomes of three phenotypically diverse species: Fusarium graminearum, Fusarium verticillioides and Fusarium oxysporum f. sp. lycopersici. Our analysis revealed lineage-specific (LS) genomic regions in F. oxysporum that include four entire chromosomes and account for more than one-quarter of the genome. LS regions are rich in transposons and genes with distinct evolutionary profiles but related to pathogenicity, indicative of horizontal acquisition. Experimentally, we demonstrate the transfer of two LS chromosomes between strains of F. oxysporum, converting a non-pathogenic strain into a pathogen. Transfer of LS chromosomes between otherwise genetically isolated strains explains the polyphyletic origin of host specificity and the emergence of new pathogenic lineages in F. oxysporum. These findings put the evolution of fungal pathogenicity into a new perspective.

AB - Fusarium species are among the most important phytopathogenic and toxigenic fungi. To understand the molecular underpinnings of pathogenicity in the genus Fusarium, we compared the genomes of three phenotypically diverse species: Fusarium graminearum, Fusarium verticillioides and Fusarium oxysporum f. sp. lycopersici. Our analysis revealed lineage-specific (LS) genomic regions in F. oxysporum that include four entire chromosomes and account for more than one-quarter of the genome. LS regions are rich in transposons and genes with distinct evolutionary profiles but related to pathogenicity, indicative of horizontal acquisition. Experimentally, we demonstrate the transfer of two LS chromosomes between strains of F. oxysporum, converting a non-pathogenic strain into a pathogen. Transfer of LS chromosomes between otherwise genetically isolated strains explains the polyphyletic origin of host specificity and the emergence of new pathogenic lineages in F. oxysporum. These findings put the evolution of fungal pathogenicity into a new perspective.

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UR - http://www.scopus.com/inward/citedby.url?scp=77949714038&partnerID=8YFLogxK

U2 - 10.1038/nature08850

DO - 10.1038/nature08850

M3 - Article

C2 - 20237561

AN - SCOPUS:77949714038

SN - 0028-0836

VL - 464

SP - 367

EP - 373

JO - Nature

JF - Nature

IS - 7287

ER -

Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium

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