Kinome Expansion in the <named-content content-type="genus-species">Fusarium oxysporum</named-content> Species Complex Driven by Accessory Chromosomes

ABSTRACT The Fusarium oxysporum species complex (FOSC) is a group of soilborne pathogens causing severe disease in more than 100 plant hosts, while individual strains exhibit strong host specificity. Both chromosome transfer and comparative genomics experiments have demonstrated that lineage-specifi...

Full description

Bibliographic Details
Main Authors: Gregory A. DeIulio, Li Guo, Yong Zhang, Jonathan M. Goldberg, H. Corby Kistler, Li-Jun Ma
Format: Article
Language:English
Published: American Society for Microbiology 2018-06-01
Series:mSphere
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/mSphere.00231-18
_version_ 1818986990608056320
author Gregory A. DeIulio
Li Guo
Yong Zhang
Jonathan M. Goldberg
H. Corby Kistler
Li-Jun Ma
author_facet Gregory A. DeIulio
Li Guo
Yong Zhang
Jonathan M. Goldberg
H. Corby Kistler
Li-Jun Ma
author_sort Gregory A. DeIulio
collection DOAJ
description ABSTRACT The Fusarium oxysporum species complex (FOSC) is a group of soilborne pathogens causing severe disease in more than 100 plant hosts, while individual strains exhibit strong host specificity. Both chromosome transfer and comparative genomics experiments have demonstrated that lineage-specific (LS) chromosomes contribute to the host-specific pathogenicity. However, little is known about the functional importance of genes encoded in these LS chromosomes. Focusing on signaling transduction, this study compared the kinomes of 12 F. oxysporum isolates, including both plant and human pathogens and 1 nonpathogenic biocontrol strain, with 7 additional publicly available ascomycete genomes. Overall, F. oxysporum kinomes are the largest, facilitated in part by the acquisitions of the LS chromosomes. The comparative study identified 99 kinases that are present in almost all examined fungal genomes, forming the core signaling network of ascomycete fungi. Compared to the conserved ascomycete kinome, the expansion of the F. oxysporum kinome occurs in several kinase families such as histidine kinases that are involved in environmental signal sensing and target of rapamycin (TOR) kinase that mediates cellular responses. Comparative kinome analysis suggests a convergent evolution that shapes individual F. oxysporum isolates with an enhanced and unique capacity for environmental perception and associated downstream responses. IMPORTANCE Isolates of Fusarium oxysporum are adapted to survive a wide range of host and nonhost conditions. In addition, F. oxysporum was recently recognized as the top emerging opportunistic fungal pathogen infecting immunocompromised humans. The sensory and response networks of these fungi undoubtedly play a fundamental role in establishing the adaptability of this group. We have examined the kinomes of 12 F. oxysporum isolates and highlighted kinase families that distinguish F. oxysporum from other fungi, as well as different isolates from one another. The amplification of kinases involved in environmental signal relay and regulating downstream cellular responses clearly sets Fusarium apart from other Ascomycetes. Although the functions of many of these kinases are still unclear, their specific proliferation highlights them as a result of the evolutionary forces that have shaped this species complex and clearly marks them as targets for exploitation in order to combat disease.
first_indexed 2024-12-20T18:59:34Z
format Article
id doaj.art-d9a664ae35754c9e924e404b9e2e71bf
institution Directory Open Access Journal
issn 2379-5042
language English
last_indexed 2024-12-20T18:59:34Z
publishDate 2018-06-01
publisher American Society for Microbiology
record_format Article
series mSphere
spelling doaj.art-d9a664ae35754c9e924e404b9e2e71bf2022-12-21T19:29:26ZengAmerican Society for MicrobiologymSphere2379-50422018-06-013310.1128/mSphere.00231-18Kinome Expansion in the <named-content content-type="genus-species">Fusarium oxysporum</named-content> Species Complex Driven by Accessory ChromosomesGregory A. DeIulio0Li Guo1Yong Zhang2Jonathan M. Goldberg3H. Corby Kistler4Li-Jun Ma5Department of Biochemistry and Molecular Biology, University of Massachusetts Amherst, Amherst, Massachusetts, USADepartment of Biochemistry and Molecular Biology, University of Massachusetts Amherst, Amherst, Massachusetts, USADepartment of Biochemistry and Molecular Biology, University of Massachusetts Amherst, Amherst, Massachusetts, USAThe Broad Institute of MIT and Harvard, Cambridge, Massachusetts, USAUSDA ARS, Cereal Disease Laboratory, St. Paul, Minnesota, USADepartment of Biochemistry and Molecular Biology, University of Massachusetts Amherst, Amherst, Massachusetts, USAABSTRACT The Fusarium oxysporum species complex (FOSC) is a group of soilborne pathogens causing severe disease in more than 100 plant hosts, while individual strains exhibit strong host specificity. Both chromosome transfer and comparative genomics experiments have demonstrated that lineage-specific (LS) chromosomes contribute to the host-specific pathogenicity. However, little is known about the functional importance of genes encoded in these LS chromosomes. Focusing on signaling transduction, this study compared the kinomes of 12 F. oxysporum isolates, including both plant and human pathogens and 1 nonpathogenic biocontrol strain, with 7 additional publicly available ascomycete genomes. Overall, F. oxysporum kinomes are the largest, facilitated in part by the acquisitions of the LS chromosomes. The comparative study identified 99 kinases that are present in almost all examined fungal genomes, forming the core signaling network of ascomycete fungi. Compared to the conserved ascomycete kinome, the expansion of the F. oxysporum kinome occurs in several kinase families such as histidine kinases that are involved in environmental signal sensing and target of rapamycin (TOR) kinase that mediates cellular responses. Comparative kinome analysis suggests a convergent evolution that shapes individual F. oxysporum isolates with an enhanced and unique capacity for environmental perception and associated downstream responses. IMPORTANCE Isolates of Fusarium oxysporum are adapted to survive a wide range of host and nonhost conditions. In addition, F. oxysporum was recently recognized as the top emerging opportunistic fungal pathogen infecting immunocompromised humans. The sensory and response networks of these fungi undoubtedly play a fundamental role in establishing the adaptability of this group. We have examined the kinomes of 12 F. oxysporum isolates and highlighted kinase families that distinguish F. oxysporum from other fungi, as well as different isolates from one another. The amplification of kinases involved in environmental signal relay and regulating downstream cellular responses clearly sets Fusarium apart from other Ascomycetes. Although the functions of many of these kinases are still unclear, their specific proliferation highlights them as a result of the evolutionary forces that have shaped this species complex and clearly marks them as targets for exploitation in order to combat disease.https://journals.asm.org/doi/10.1128/mSphere.00231-18Fusarium oxysporum species complexTOR kinaseaccessory chromosomehistidine kinasekinome
spellingShingle Gregory A. DeIulio
Li Guo
Yong Zhang
Jonathan M. Goldberg
H. Corby Kistler
Li-Jun Ma
Kinome Expansion in the <named-content content-type="genus-species">Fusarium oxysporum</named-content> Species Complex Driven by Accessory Chromosomes
mSphere
Fusarium oxysporum species complex
TOR kinase
accessory chromosome
histidine kinase
kinome
title Kinome Expansion in the <named-content content-type="genus-species">Fusarium oxysporum</named-content> Species Complex Driven by Accessory Chromosomes
title_full Kinome Expansion in the <named-content content-type="genus-species">Fusarium oxysporum</named-content> Species Complex Driven by Accessory Chromosomes
title_fullStr Kinome Expansion in the <named-content content-type="genus-species">Fusarium oxysporum</named-content> Species Complex Driven by Accessory Chromosomes
title_full_unstemmed Kinome Expansion in the <named-content content-type="genus-species">Fusarium oxysporum</named-content> Species Complex Driven by Accessory Chromosomes
title_short Kinome Expansion in the <named-content content-type="genus-species">Fusarium oxysporum</named-content> Species Complex Driven by Accessory Chromosomes
title_sort kinome expansion in the named content content type genus species fusarium oxysporum named content species complex driven by accessory chromosomes
topic Fusarium oxysporum species complex
TOR kinase
accessory chromosome
histidine kinase
kinome
url https://journals.asm.org/doi/10.1128/mSphere.00231-18
work_keys_str_mv AT gregoryadeiulio kinomeexpansioninthenamedcontentcontenttypegenusspeciesfusariumoxysporumnamedcontentspeciescomplexdrivenbyaccessorychromosomes
AT liguo kinomeexpansioninthenamedcontentcontenttypegenusspeciesfusariumoxysporumnamedcontentspeciescomplexdrivenbyaccessorychromosomes
AT yongzhang kinomeexpansioninthenamedcontentcontenttypegenusspeciesfusariumoxysporumnamedcontentspeciescomplexdrivenbyaccessorychromosomes
AT jonathanmgoldberg kinomeexpansioninthenamedcontentcontenttypegenusspeciesfusariumoxysporumnamedcontentspeciescomplexdrivenbyaccessorychromosomes
AT hcorbykistler kinomeexpansioninthenamedcontentcontenttypegenusspeciesfusariumoxysporumnamedcontentspeciescomplexdrivenbyaccessorychromosomes
AT lijunma kinomeexpansioninthenamedcontentcontenttypegenusspeciesfusariumoxysporumnamedcontentspeciescomplexdrivenbyaccessorychromosomes