Comparative genomics yields insights into niche adaptation of plant vascular wilt pathogens

Steven J. Klosterman, Krishna V. Subbarao, Seogchan Kang, Paola Veronese, Scott E. Gold, Bart P.H.J. Thomma, Zehua Chen, Bernard Henrissat, Yong Hwan Lee, Jongsun Park, Maria D. Garcia-Pedrajas, Dez J. Barbara, Amy Anchieta, Ronnie de Jonge, Parthasarathy Santhanam, Karunakaran Maruthachalam, Zahi Atallah, Stefan G. Amyotte, Zahi Paz, Patrik InderbitzinRyan J. Hayes, David I. Heiman, Sarah Young, Qiandong Zeng, Reinhard Engels, James Galagan, Christina A. Cuomo, Katherine F. Dobinson, Li Jun Ma

Research output: Contribution to journalArticle

234 Citations (Scopus)

Abstract

The vascular wilt fungi Verticillium dahliae and V. albo-atrum infect over 200 plant species, causing billions of dollars in annual crop losses. The characteristic wilt symptoms are a result of colonization and proliferation of the pathogens in the xylem vessels, which undergo fluctuations in osmolarity. To gain insights into the mechanisms that confer the organisms' pathogenicity and enable them to proliferate in the unique ecological niche of the plant vascular system, we sequenced the genomes of V. dahliae and V. albo-atrum and compared them to each other, and to the genome of Fusarium oxysporum, another fungal wilt pathogen. Our analyses identified a set of proteins that are shared among all three wilt pathogens, and present in few other fungal species. One of these is a homolog of a bacterial glucosyltransferase that synthesizes virulence-related osmoregulated periplasmic glucans in bacteria. Pathogenicity tests of the corresponding V. dahliae glucosyltransferase gene deletion mutants indicate that the gene is required for full virulence in the Australian tobacco species Nicotiana benthamiana. Compared to other fungi, the two sequenced Verticillium genomes encode more pectin-degrading enzymes and other carbohydrate-active enzymes, suggesting an extraordinary capacity to degrade plant pectin barricades. The high level of synteny between the two Verticillium assemblies highlighted four flexible genomic islands in V. dahliae that are enriched for transposable elements, and contain duplicated genes and genes that are important in signaling/transcriptional regulation and iron/lipid metabolism. Coupled with an enhanced capacity to degrade plant materials, these genomic islands may contribute to the expanded genetic diversity and virulence of V. dahliae, the primary causal agent of Verticillium wilts. Significantly, our study reveals insights into the genetic mechanisms of niche adaptation of fungal wilt pathogens, advances our understanding of the evolution and development of their pathogenesis, and sheds light on potential avenues for the development of novel disease management strategies to combat destructive wilt diseases.

Original languageEnglish (US)
Article numbere1002137
JournalPLoS pathogens
Volume7
Issue number7
DOIs
StatePublished - Jul 1 2011

Fingerprint

Verticillium
Genomics
Blood Vessels
Virulence
Glucosyltransferases
Genomic Islands
Genome
Tobacco
Fungi
Genes
Synteny
Xylem
DNA Transposable Elements
Glucans
Gene Deletion
Fusarium
Enzymes
Disease Management
Lipid Metabolism
Osmolar Concentration

All Science Journal Classification (ASJC) codes

  • Parasitology
  • Microbiology
  • Immunology
  • Molecular Biology
  • Genetics
  • Virology

Cite this

Klosterman, S. J., Subbarao, K. V., Kang, S., Veronese, P., Gold, S. E., Thomma, B. P. H. J., ... Ma, L. J. (2011). Comparative genomics yields insights into niche adaptation of plant vascular wilt pathogens. PLoS pathogens, 7(7), [e1002137]. https://doi.org/10.1371/journal.ppat.1002137
Klosterman, Steven J. ; Subbarao, Krishna V. ; Kang, Seogchan ; Veronese, Paola ; Gold, Scott E. ; Thomma, Bart P.H.J. ; Chen, Zehua ; Henrissat, Bernard ; Lee, Yong Hwan ; Park, Jongsun ; Garcia-Pedrajas, Maria D. ; Barbara, Dez J. ; Anchieta, Amy ; de Jonge, Ronnie ; Santhanam, Parthasarathy ; Maruthachalam, Karunakaran ; Atallah, Zahi ; Amyotte, Stefan G. ; Paz, Zahi ; Inderbitzin, Patrik ; Hayes, Ryan J. ; Heiman, David I. ; Young, Sarah ; Zeng, Qiandong ; Engels, Reinhard ; Galagan, James ; Cuomo, Christina A. ; Dobinson, Katherine F. ; Ma, Li Jun. / Comparative genomics yields insights into niche adaptation of plant vascular wilt pathogens. In: PLoS pathogens. 2011 ; Vol. 7, No. 7.
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abstract = "The vascular wilt fungi Verticillium dahliae and V. albo-atrum infect over 200 plant species, causing billions of dollars in annual crop losses. The characteristic wilt symptoms are a result of colonization and proliferation of the pathogens in the xylem vessels, which undergo fluctuations in osmolarity. To gain insights into the mechanisms that confer the organisms' pathogenicity and enable them to proliferate in the unique ecological niche of the plant vascular system, we sequenced the genomes of V. dahliae and V. albo-atrum and compared them to each other, and to the genome of Fusarium oxysporum, another fungal wilt pathogen. Our analyses identified a set of proteins that are shared among all three wilt pathogens, and present in few other fungal species. One of these is a homolog of a bacterial glucosyltransferase that synthesizes virulence-related osmoregulated periplasmic glucans in bacteria. Pathogenicity tests of the corresponding V. dahliae glucosyltransferase gene deletion mutants indicate that the gene is required for full virulence in the Australian tobacco species Nicotiana benthamiana. Compared to other fungi, the two sequenced Verticillium genomes encode more pectin-degrading enzymes and other carbohydrate-active enzymes, suggesting an extraordinary capacity to degrade plant pectin barricades. The high level of synteny between the two Verticillium assemblies highlighted four flexible genomic islands in V. dahliae that are enriched for transposable elements, and contain duplicated genes and genes that are important in signaling/transcriptional regulation and iron/lipid metabolism. Coupled with an enhanced capacity to degrade plant materials, these genomic islands may contribute to the expanded genetic diversity and virulence of V. dahliae, the primary causal agent of Verticillium wilts. Significantly, our study reveals insights into the genetic mechanisms of niche adaptation of fungal wilt pathogens, advances our understanding of the evolution and development of their pathogenesis, and sheds light on potential avenues for the development of novel disease management strategies to combat destructive wilt diseases.",
author = "Klosterman, {Steven J.} and Subbarao, {Krishna V.} and Seogchan Kang and Paola Veronese and Gold, {Scott E.} and Thomma, {Bart P.H.J.} and Zehua Chen and Bernard Henrissat and Lee, {Yong Hwan} and Jongsun Park and Garcia-Pedrajas, {Maria D.} and Barbara, {Dez J.} and Amy Anchieta and {de Jonge}, Ronnie and Parthasarathy Santhanam and Karunakaran Maruthachalam and Zahi Atallah and Amyotte, {Stefan G.} and Zahi Paz and Patrik Inderbitzin and Hayes, {Ryan J.} and Heiman, {David I.} and Sarah Young and Qiandong Zeng and Reinhard Engels and James Galagan and Cuomo, {Christina A.} and Dobinson, {Katherine F.} and Ma, {Li Jun}",
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Klosterman, SJ, Subbarao, KV, Kang, S, Veronese, P, Gold, SE, Thomma, BPHJ, Chen, Z, Henrissat, B, Lee, YH, Park, J, Garcia-Pedrajas, MD, Barbara, DJ, Anchieta, A, de Jonge, R, Santhanam, P, Maruthachalam, K, Atallah, Z, Amyotte, SG, Paz, Z, Inderbitzin, P, Hayes, RJ, Heiman, DI, Young, S, Zeng, Q, Engels, R, Galagan, J, Cuomo, CA, Dobinson, KF & Ma, LJ 2011, 'Comparative genomics yields insights into niche adaptation of plant vascular wilt pathogens', PLoS pathogens, vol. 7, no. 7, e1002137. https://doi.org/10.1371/journal.ppat.1002137

Comparative genomics yields insights into niche adaptation of plant vascular wilt pathogens. / Klosterman, Steven J.; Subbarao, Krishna V.; Kang, Seogchan; Veronese, Paola; Gold, Scott E.; Thomma, Bart P.H.J.; Chen, Zehua; Henrissat, Bernard; Lee, Yong Hwan; Park, Jongsun; Garcia-Pedrajas, Maria D.; Barbara, Dez J.; Anchieta, Amy; de Jonge, Ronnie; Santhanam, Parthasarathy; Maruthachalam, Karunakaran; Atallah, Zahi; Amyotte, Stefan G.; Paz, Zahi; Inderbitzin, Patrik; Hayes, Ryan J.; Heiman, David I.; Young, Sarah; Zeng, Qiandong; Engels, Reinhard; Galagan, James; Cuomo, Christina A.; Dobinson, Katherine F.; Ma, Li Jun.

In: PLoS pathogens, Vol. 7, No. 7, e1002137, 01.07.2011.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Comparative genomics yields insights into niche adaptation of plant vascular wilt pathogens

AU - Klosterman, Steven J.

AU - Subbarao, Krishna V.

AU - Kang, Seogchan

AU - Veronese, Paola

AU - Gold, Scott E.

AU - Thomma, Bart P.H.J.

AU - Chen, Zehua

AU - Henrissat, Bernard

AU - Lee, Yong Hwan

AU - Park, Jongsun

AU - Garcia-Pedrajas, Maria D.

AU - Barbara, Dez J.

AU - Anchieta, Amy

AU - de Jonge, Ronnie

AU - Santhanam, Parthasarathy

AU - Maruthachalam, Karunakaran

AU - Atallah, Zahi

AU - Amyotte, Stefan G.

AU - Paz, Zahi

AU - Inderbitzin, Patrik

AU - Hayes, Ryan J.

AU - Heiman, David I.

AU - Young, Sarah

AU - Zeng, Qiandong

AU - Engels, Reinhard

AU - Galagan, James

AU - Cuomo, Christina A.

AU - Dobinson, Katherine F.

AU - Ma, Li Jun

PY - 2011/7/1

Y1 - 2011/7/1

N2 - The vascular wilt fungi Verticillium dahliae and V. albo-atrum infect over 200 plant species, causing billions of dollars in annual crop losses. The characteristic wilt symptoms are a result of colonization and proliferation of the pathogens in the xylem vessels, which undergo fluctuations in osmolarity. To gain insights into the mechanisms that confer the organisms' pathogenicity and enable them to proliferate in the unique ecological niche of the plant vascular system, we sequenced the genomes of V. dahliae and V. albo-atrum and compared them to each other, and to the genome of Fusarium oxysporum, another fungal wilt pathogen. Our analyses identified a set of proteins that are shared among all three wilt pathogens, and present in few other fungal species. One of these is a homolog of a bacterial glucosyltransferase that synthesizes virulence-related osmoregulated periplasmic glucans in bacteria. Pathogenicity tests of the corresponding V. dahliae glucosyltransferase gene deletion mutants indicate that the gene is required for full virulence in the Australian tobacco species Nicotiana benthamiana. Compared to other fungi, the two sequenced Verticillium genomes encode more pectin-degrading enzymes and other carbohydrate-active enzymes, suggesting an extraordinary capacity to degrade plant pectin barricades. The high level of synteny between the two Verticillium assemblies highlighted four flexible genomic islands in V. dahliae that are enriched for transposable elements, and contain duplicated genes and genes that are important in signaling/transcriptional regulation and iron/lipid metabolism. Coupled with an enhanced capacity to degrade plant materials, these genomic islands may contribute to the expanded genetic diversity and virulence of V. dahliae, the primary causal agent of Verticillium wilts. Significantly, our study reveals insights into the genetic mechanisms of niche adaptation of fungal wilt pathogens, advances our understanding of the evolution and development of their pathogenesis, and sheds light on potential avenues for the development of novel disease management strategies to combat destructive wilt diseases.

AB - The vascular wilt fungi Verticillium dahliae and V. albo-atrum infect over 200 plant species, causing billions of dollars in annual crop losses. The characteristic wilt symptoms are a result of colonization and proliferation of the pathogens in the xylem vessels, which undergo fluctuations in osmolarity. To gain insights into the mechanisms that confer the organisms' pathogenicity and enable them to proliferate in the unique ecological niche of the plant vascular system, we sequenced the genomes of V. dahliae and V. albo-atrum and compared them to each other, and to the genome of Fusarium oxysporum, another fungal wilt pathogen. Our analyses identified a set of proteins that are shared among all three wilt pathogens, and present in few other fungal species. One of these is a homolog of a bacterial glucosyltransferase that synthesizes virulence-related osmoregulated periplasmic glucans in bacteria. Pathogenicity tests of the corresponding V. dahliae glucosyltransferase gene deletion mutants indicate that the gene is required for full virulence in the Australian tobacco species Nicotiana benthamiana. Compared to other fungi, the two sequenced Verticillium genomes encode more pectin-degrading enzymes and other carbohydrate-active enzymes, suggesting an extraordinary capacity to degrade plant pectin barricades. The high level of synteny between the two Verticillium assemblies highlighted four flexible genomic islands in V. dahliae that are enriched for transposable elements, and contain duplicated genes and genes that are important in signaling/transcriptional regulation and iron/lipid metabolism. Coupled with an enhanced capacity to degrade plant materials, these genomic islands may contribute to the expanded genetic diversity and virulence of V. dahliae, the primary causal agent of Verticillium wilts. Significantly, our study reveals insights into the genetic mechanisms of niche adaptation of fungal wilt pathogens, advances our understanding of the evolution and development of their pathogenesis, and sheds light on potential avenues for the development of novel disease management strategies to combat destructive wilt diseases.

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