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Sensing and adhesion are adaptive functions in the plant pathogenic xanthomonads
Bacterial plant pathogens belonging to the Xanthomonas genus are tightly adapted to their host plants and are not known to colonise other environments. The host range of each strain is usually restricted to a few host plant species. Bacterial strains responsible for the same type of symptoms on the...
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Published in: | BMC evolutionary biology 2011-03, Vol.11 (1), p.67-67, Article 67 |
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description | Bacterial plant pathogens belonging to the Xanthomonas genus are tightly adapted to their host plants and are not known to colonise other environments. The host range of each strain is usually restricted to a few host plant species. Bacterial strains responsible for the same type of symptoms on the same host range cluster in a pathovar. The phyllosphere is a highly stressful environment, but it provides a selective habitat and a source of substrates for these bacteria. Xanthomonads colonise host phylloplane before entering leaf tissues and engaging in an invasive pathogenic phase. Hence, these bacteria are likely to have evolved strategies to adapt to life in this environment. We hypothesised that determinants responsible for bacterial host adaptation are expressed starting from the establishment of chemotactic attraction and adhesion on host tissue.
We established the distribution of 70 genes coding sensors and adhesins in a large collection of xanthomonad strains. These 173 strains belong to different pathovars of Xanthomonas spp and display different host ranges. Candidate genes are involved in chemotactic attraction (25 genes), chemical environment sensing (35 genes), and adhesion (10 genes). Our study revealed that candidate gene repertoires comprised core and variable gene suites that likely have distinct roles in host adaptation. Most pathovars were characterized by unique repertoires of candidate genes, highlighting a correspondence between pathovar clustering and repertoires of sensors and adhesins. To further challenge our hypothesis, we tested for molecular signatures of selection on candidate genes extracted from sequenced genomes of strains belonging to different pathovars. We found strong evidence of adaptive divergence acting on most candidate genes.
These data provide insight into the potential role played by sensors and adhesins in the adaptation of xanthomonads to their host plants. The correspondence between repertoires of sensor and adhesin genes and pathovars and the rapid evolution of sensors and adhesins shows that, for plant pathogenic xanthomonads, events leading to host specificity may occur as early as chemotactic attraction by host and adhesion to tissues. |
doi_str_mv | 10.1186/1471-2148-11-67 |
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We established the distribution of 70 genes coding sensors and adhesins in a large collection of xanthomonad strains. These 173 strains belong to different pathovars of Xanthomonas spp and display different host ranges. Candidate genes are involved in chemotactic attraction (25 genes), chemical environment sensing (35 genes), and adhesion (10 genes). Our study revealed that candidate gene repertoires comprised core and variable gene suites that likely have distinct roles in host adaptation. Most pathovars were characterized by unique repertoires of candidate genes, highlighting a correspondence between pathovar clustering and repertoires of sensors and adhesins. To further challenge our hypothesis, we tested for molecular signatures of selection on candidate genes extracted from sequenced genomes of strains belonging to different pathovars. We found strong evidence of adaptive divergence acting on most candidate genes.
These data provide insight into the potential role played by sensors and adhesins in the adaptation of xanthomonads to their host plants. The correspondence between repertoires of sensor and adhesin genes and pathovars and the rapid evolution of sensors and adhesins shows that, for plant pathogenic xanthomonads, events leading to host specificity may occur as early as chemotactic attraction by host and adhesion to tissues.</description><identifier>ISSN: 1471-2148</identifier><identifier>EISSN: 1471-2148</identifier><identifier>DOI: 10.1186/1471-2148-11-67</identifier><identifier>PMID: 21396107</identifier><language>eng</language><publisher>England: BioMed Central Ltd</publisher><subject>Adaptation, Physiological - genetics ; Adhesins, Bacterial - genetics ; Adhesion ; Bacteria ; Bacterial Adhesion ; Biodiversity and Ecology ; Chemotaxis - genetics ; Data Mining ; DNA, Bacterial - genetics ; Environmental Sciences ; Genes ; Genes, Bacterial ; Genetic aspects ; Genomes ; Microbiology ; Microorganisms ; Mutation ; Plants - microbiology ; Selection, Genetic ; Sequence Alignment ; Studies ; Xanthomonas ; Xanthomonas - genetics ; Xanthomonas - pathogenicity ; Xanthomonas - physiology</subject><ispartof>BMC evolutionary biology, 2011-03, Vol.11 (1), p.67-67, Article 67</ispartof><rights>COPYRIGHT 2011 BioMed Central Ltd.</rights><rights>2011 Mhedbi-Hajri et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><rights>Copyright ©2011 Mhedbi-Hajri et al; licensee BioMed Central Ltd. 2011 Mhedbi-Hajri et al; licensee BioMed Central Ltd.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-b711t-1e3804bc1e2af2404966943d5a629e5541e3cd9267051ddf85167748ea96d1663</citedby><cites>FETCH-LOGICAL-b711t-1e3804bc1e2af2404966943d5a629e5541e3cd9267051ddf85167748ea96d1663</cites><orcidid>0000-0002-9334-5862 ; 0000-0002-8162-3343 ; 0000-0002-1442-917X ; 0000-0001-6518-8401</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3063832/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/901978126?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,25753,27924,27925,37012,37013,44590,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/21396107$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.inrae.fr/hal-02649867$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Mhedbi-Hajri, Nadia</creatorcontrib><creatorcontrib>Darrasse, Armelle</creatorcontrib><creatorcontrib>Pigné, Sandrine</creatorcontrib><creatorcontrib>Durand, Karine</creatorcontrib><creatorcontrib>Fouteau, Stéphanie</creatorcontrib><creatorcontrib>Barbe, Valérie</creatorcontrib><creatorcontrib>Manceau, Charles</creatorcontrib><creatorcontrib>Lemaire, Christophe</creatorcontrib><creatorcontrib>Jacques, Marie-Agnès</creatorcontrib><title>Sensing and adhesion are adaptive functions in the plant pathogenic xanthomonads</title><title>BMC evolutionary biology</title><addtitle>BMC Evol Biol</addtitle><description>Bacterial plant pathogens belonging to the Xanthomonas genus are tightly adapted to their host plants and are not known to colonise other environments. The host range of each strain is usually restricted to a few host plant species. Bacterial strains responsible for the same type of symptoms on the same host range cluster in a pathovar. The phyllosphere is a highly stressful environment, but it provides a selective habitat and a source of substrates for these bacteria. Xanthomonads colonise host phylloplane before entering leaf tissues and engaging in an invasive pathogenic phase. Hence, these bacteria are likely to have evolved strategies to adapt to life in this environment. We hypothesised that determinants responsible for bacterial host adaptation are expressed starting from the establishment of chemotactic attraction and adhesion on host tissue.
We established the distribution of 70 genes coding sensors and adhesins in a large collection of xanthomonad strains. These 173 strains belong to different pathovars of Xanthomonas spp and display different host ranges. Candidate genes are involved in chemotactic attraction (25 genes), chemical environment sensing (35 genes), and adhesion (10 genes). Our study revealed that candidate gene repertoires comprised core and variable gene suites that likely have distinct roles in host adaptation. Most pathovars were characterized by unique repertoires of candidate genes, highlighting a correspondence between pathovar clustering and repertoires of sensors and adhesins. To further challenge our hypothesis, we tested for molecular signatures of selection on candidate genes extracted from sequenced genomes of strains belonging to different pathovars. We found strong evidence of adaptive divergence acting on most candidate genes.
These data provide insight into the potential role played by sensors and adhesins in the adaptation of xanthomonads to their host plants. 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The host range of each strain is usually restricted to a few host plant species. Bacterial strains responsible for the same type of symptoms on the same host range cluster in a pathovar. The phyllosphere is a highly stressful environment, but it provides a selective habitat and a source of substrates for these bacteria. Xanthomonads colonise host phylloplane before entering leaf tissues and engaging in an invasive pathogenic phase. Hence, these bacteria are likely to have evolved strategies to adapt to life in this environment. We hypothesised that determinants responsible for bacterial host adaptation are expressed starting from the establishment of chemotactic attraction and adhesion on host tissue.
We established the distribution of 70 genes coding sensors and adhesins in a large collection of xanthomonad strains. These 173 strains belong to different pathovars of Xanthomonas spp and display different host ranges. Candidate genes are involved in chemotactic attraction (25 genes), chemical environment sensing (35 genes), and adhesion (10 genes). Our study revealed that candidate gene repertoires comprised core and variable gene suites that likely have distinct roles in host adaptation. Most pathovars were characterized by unique repertoires of candidate genes, highlighting a correspondence between pathovar clustering and repertoires of sensors and adhesins. To further challenge our hypothesis, we tested for molecular signatures of selection on candidate genes extracted from sequenced genomes of strains belonging to different pathovars. We found strong evidence of adaptive divergence acting on most candidate genes.
These data provide insight into the potential role played by sensors and adhesins in the adaptation of xanthomonads to their host plants. The correspondence between repertoires of sensor and adhesin genes and pathovars and the rapid evolution of sensors and adhesins shows that, for plant pathogenic xanthomonads, events leading to host specificity may occur as early as chemotactic attraction by host and adhesion to tissues.</abstract><cop>England</cop><pub>BioMed Central Ltd</pub><pmid>21396107</pmid><doi>10.1186/1471-2148-11-67</doi><tpages>1</tpages><orcidid>https://orcid.org/0000-0002-9334-5862</orcidid><orcidid>https://orcid.org/0000-0002-8162-3343</orcidid><orcidid>https://orcid.org/0000-0002-1442-917X</orcidid><orcidid>https://orcid.org/0000-0001-6518-8401</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Adaptation, Physiological - genetics Adhesins, Bacterial - genetics Adhesion Bacteria Bacterial Adhesion Biodiversity and Ecology Chemotaxis - genetics Data Mining DNA, Bacterial - genetics Environmental Sciences Genes Genes, Bacterial Genetic aspects Genomes Microbiology Microorganisms Mutation Plants - microbiology Selection, Genetic Sequence Alignment Studies Xanthomonas Xanthomonas - genetics Xanthomonas - pathogenicity Xanthomonas - physiology |
title | Sensing and adhesion are adaptive functions in the plant pathogenic xanthomonads |
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