The plant pathogen Pseudomonas syringae pv. tomato is genetically monomorphic and under strong selection to evade tomato immunity.

Recently, genome sequencing of many isolates of genetically monomorphic bacterial human pathogens has given new insights into pathogen microevolution and phylogeography. Here, we report a genome-based micro-evolutionary study of a bacterial plant pathogen, Pseudomonas syringae pv. tomato. Only 267 m...

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Autores principales: Rongman Cai, James Lewis, Shuangchun Yan, Haijie Liu, Christopher R Clarke, Francesco Campanile, Nalvo F Almeida, David J Studholme, Magdalen Lindeberg, David Schneider, Massimo Zaccardelli, Joao C Setubal, Nadia P Morales-Lizcano, Adriana Bernal, Gitta Coaker, Christy Baker, Carol L Bender, Scotland Leman, Boris A Vinatzer
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spelling oai:doaj.org-article:47692a6fef884abd9a4b90cc824ff6542021-11-18T06:03:06ZThe plant pathogen Pseudomonas syringae pv. tomato is genetically monomorphic and under strong selection to evade tomato immunity.1553-73661553-737410.1371/journal.ppat.1002130https://doaj.org/article/47692a6fef884abd9a4b90cc824ff6542011-08-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/21901088/?tool=EBIhttps://doaj.org/toc/1553-7366https://doaj.org/toc/1553-7374Recently, genome sequencing of many isolates of genetically monomorphic bacterial human pathogens has given new insights into pathogen microevolution and phylogeography. Here, we report a genome-based micro-evolutionary study of a bacterial plant pathogen, Pseudomonas syringae pv. tomato. Only 267 mutations were identified between five sequenced isolates in 3,543,009 nt of analyzed genome sequence, which suggests a recent evolutionary origin of this pathogen. Further analysis with genome-derived markers of 89 world-wide isolates showed that several genotypes exist in North America and in Europe indicating frequent pathogen movement between these world regions. Genome-derived markers and molecular analyses of key pathogen loci important for virulence and motility both suggest ongoing adaptation to the tomato host. A mutational hotspot was found in the type III-secreted effector gene hopM1. These mutations abolish the cell death triggering activity of the full-length protein indicating strong selection for loss of function of this effector, which was previously considered a virulence factor. Two non-synonymous mutations in the flagellin-encoding gene fliC allowed identifying a new microbe associated molecular pattern (MAMP) in a region distinct from the known MAMP flg22. Interestingly, the ancestral allele of this MAMP induces a stronger tomato immune response than the derived alleles. The ancestral allele has largely disappeared from today's Pto populations suggesting that flagellin-triggered immunity limits pathogen fitness even in highly virulent pathogens. An additional non-synonymous mutation was identified in flg22 in South American isolates. Therefore, MAMPs are more variable than expected differing even between otherwise almost identical isolates of the same pathogen strain.Rongman CaiJames LewisShuangchun YanHaijie LiuChristopher R ClarkeFrancesco CampanileNalvo F AlmeidaDavid J StudholmeMagdalen LindebergDavid SchneiderMassimo ZaccardelliJoao C SetubalNadia P Morales-LizcanoAdriana BernalGitta CoakerChristy BakerCarol L BenderScotland LemanBoris A VinatzerPublic Library of Science (PLoS)articleImmunologic diseases. AllergyRC581-607Biology (General)QH301-705.5ENPLoS Pathogens, Vol 7, Iss 8, p e1002130 (2011)
institution DOAJ
collection DOAJ
language EN
topic Immunologic diseases. Allergy
RC581-607
Biology (General)
QH301-705.5
spellingShingle Immunologic diseases. Allergy
RC581-607
Biology (General)
QH301-705.5
Rongman Cai
James Lewis
Shuangchun Yan
Haijie Liu
Christopher R Clarke
Francesco Campanile
Nalvo F Almeida
David J Studholme
Magdalen Lindeberg
David Schneider
Massimo Zaccardelli
Joao C Setubal
Nadia P Morales-Lizcano
Adriana Bernal
Gitta Coaker
Christy Baker
Carol L Bender
Scotland Leman
Boris A Vinatzer
The plant pathogen Pseudomonas syringae pv. tomato is genetically monomorphic and under strong selection to evade tomato immunity.
description Recently, genome sequencing of many isolates of genetically monomorphic bacterial human pathogens has given new insights into pathogen microevolution and phylogeography. Here, we report a genome-based micro-evolutionary study of a bacterial plant pathogen, Pseudomonas syringae pv. tomato. Only 267 mutations were identified between five sequenced isolates in 3,543,009 nt of analyzed genome sequence, which suggests a recent evolutionary origin of this pathogen. Further analysis with genome-derived markers of 89 world-wide isolates showed that several genotypes exist in North America and in Europe indicating frequent pathogen movement between these world regions. Genome-derived markers and molecular analyses of key pathogen loci important for virulence and motility both suggest ongoing adaptation to the tomato host. A mutational hotspot was found in the type III-secreted effector gene hopM1. These mutations abolish the cell death triggering activity of the full-length protein indicating strong selection for loss of function of this effector, which was previously considered a virulence factor. Two non-synonymous mutations in the flagellin-encoding gene fliC allowed identifying a new microbe associated molecular pattern (MAMP) in a region distinct from the known MAMP flg22. Interestingly, the ancestral allele of this MAMP induces a stronger tomato immune response than the derived alleles. The ancestral allele has largely disappeared from today's Pto populations suggesting that flagellin-triggered immunity limits pathogen fitness even in highly virulent pathogens. An additional non-synonymous mutation was identified in flg22 in South American isolates. Therefore, MAMPs are more variable than expected differing even between otherwise almost identical isolates of the same pathogen strain.
format article
author Rongman Cai
James Lewis
Shuangchun Yan
Haijie Liu
Christopher R Clarke
Francesco Campanile
Nalvo F Almeida
David J Studholme
Magdalen Lindeberg
David Schneider
Massimo Zaccardelli
Joao C Setubal
Nadia P Morales-Lizcano
Adriana Bernal
Gitta Coaker
Christy Baker
Carol L Bender
Scotland Leman
Boris A Vinatzer
author_facet Rongman Cai
James Lewis
Shuangchun Yan
Haijie Liu
Christopher R Clarke
Francesco Campanile
Nalvo F Almeida
David J Studholme
Magdalen Lindeberg
David Schneider
Massimo Zaccardelli
Joao C Setubal
Nadia P Morales-Lizcano
Adriana Bernal
Gitta Coaker
Christy Baker
Carol L Bender
Scotland Leman
Boris A Vinatzer
author_sort Rongman Cai
title The plant pathogen Pseudomonas syringae pv. tomato is genetically monomorphic and under strong selection to evade tomato immunity.
title_short The plant pathogen Pseudomonas syringae pv. tomato is genetically monomorphic and under strong selection to evade tomato immunity.
title_full The plant pathogen Pseudomonas syringae pv. tomato is genetically monomorphic and under strong selection to evade tomato immunity.
title_fullStr The plant pathogen Pseudomonas syringae pv. tomato is genetically monomorphic and under strong selection to evade tomato immunity.
title_full_unstemmed The plant pathogen Pseudomonas syringae pv. tomato is genetically monomorphic and under strong selection to evade tomato immunity.
title_sort plant pathogen pseudomonas syringae pv. tomato is genetically monomorphic and under strong selection to evade tomato immunity.
publisher Public Library of Science (PLoS)
publishDate 2011
url https://doaj.org/article/47692a6fef884abd9a4b90cc824ff654
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