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

Research output: Contribution to journalArticle

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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 languageEnglish (US)
Pages (from-to)367-373
Number of pages7
JournalNature
Volume464
Issue number7287
DOIs
StatePublished - Mar 18 2010

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Fusarium
Genomics
Virulence
Chromosomes
Genome
Host Specificity
Fungi
Genes

All Science Journal Classification (ASJC) codes

  • General

Cite this

Ma, L. J., Van Der Does, H. C., Borkovich, K. A., Coleman, J. J., Daboussi, M. J., Di Pietro, A., ... Rep, M. (2010). Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature, 464(7287), 367-373. https://doi.org/10.1038/nature08850
Ma, Li Jun ; Van Der Does, H. Charlotte ; Borkovich, Katherine A. ; Coleman, Jeffrey J. ; Daboussi, Marie Josée ; Di Pietro, Antonio ; Dufresne, Marie ; Freitag, Michael ; Grabherr, Manfred ; Henrissat, Bernard ; Houterman, Petra M. ; Kang, Seogchan ; Shim, Won Bo ; Woloshuk, Charles ; Xie, Xiaohui ; Xu, Jin Rong ; Antoniw, John ; Baker, Scott E. ; Bluhm, Burton H. ; Breakspear, Andrew ; Brown, Daren W. ; Butchko, Robert A.E. ; Chapman, Sinead ; Coulson, Richard ; Coutinho, Pedro M. ; Danchin, Etienne G.J. ; Diener, Andrew ; Gale, Liane R. ; Gardiner, Donald M. ; Goff, Stephen ; Hammond-Kosack, Kim E. ; Hilburn, Karen ; Hua-Van, Aurélie ; Jonkers, Wilfried ; Kazan, Kemal ; Kodira, Chinnappa D. ; Koehrsen, Michael ; Kumar, Lokesh ; Lee, Yong Hwan ; Li, Liande ; Manners, John M. ; Miranda-Saavedra, Diego ; Mukherjee, Mala ; Park, Gyungsoon ; Park, Jongsun ; Park, Sook Young ; Proctor, Robert H. ; Regev, Aviv ; Ruiz-Roldan, M. Carmen ; Sain, Divya ; Sakthikumar, Sharadha ; Sykes, Sean ; Schwartz, David C. ; Turgeon, B. Gillian ; Wapinski, Ilan ; Yoder, Olen ; Young, Sarah ; Zeng, Qiandong ; Zhou, Shiguo ; Galagan, James ; Cuomo, Christina A. ; Kistler, H. Corby ; Rep, Martijn. / Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. In: Nature. 2010 ; Vol. 464, No. 7287. pp. 367-373.
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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.",
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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

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

In: Nature, Vol. 464, No. 7287, 18.03.2010, p. 367-373.

Research output: Contribution to journalArticle

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

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.

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Ma LJ, Van Der Does HC, Borkovich KA, Coleman JJ, Daboussi MJ, Di Pietro A et al. Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature. 2010 Mar 18;464(7287):367-373. https://doi.org/10.1038/nature08850