The dual nature of trehalose in citrus canker disease: a virulence factor for Xanthomonas citri subsp. citri and a trigger for plant defence responses

Handle URI:
http://hdl.handle.net/10754/346976
Title:
The dual nature of trehalose in citrus canker disease: a virulence factor for Xanthomonas citri subsp. citri and a trigger for plant defence responses
Authors:
Piazza, A.; Zimaro, T.; Garavaglia, B. S.; Ficarra, F. A.; Thomas, L.; Marondedze, C.; Feil, R.; Lunn, J. E.; Gehring, Christoph A. ( 0000-0003-4355-4591 ) ; Ottado, J.; Gottig, N.
Abstract:
Xanthomonas citri subsp. citri (Xcc) is a bacterial pathogen that causes citrus canker in susceptible Citrus spp. The Xcc genome contains genes encoding enzymes from three separate pathways of trehalose biosynthesis. Expression of genes encoding trehalose-6-phosphate synthase (otsA) and trehalose phosphatase (otsB) was highly induced during canker development, suggesting that the two-step pathway of trehalose biosynthesis via trehalose-6-phosphate has a function in pathogenesis. This pathway was eliminated from the bacterium by deletion of the otsA gene. The resulting XccΔotsA mutant produced less trehalose than the wild-type strain, was less resistant to salt and oxidative stresses, and was less able to colonize plant tissues. Gene expression and proteomic analyses of infected leaves showed that infection with XccΔotsA triggered only weak defence responses in the plant compared with infection with Xcc, and had less impact on the host plant's metabolism than the wild-type strain. These results suggested that trehalose of bacterial origin, synthesized via the otsA-otsB pathway, in Xcc, plays a role in modifying the host plant's metabolism to its own advantage but is also perceived by the plant as a sign of pathogen attack. Thus, trehalose biosynthesis has both positive and negative consequences for Xcc. On the one hand, it enables this bacterial pathogen to survive in the inhospitable environment of the leaf surface before infection and exploit the host plant's resources after infection, but on the other hand, it is a tell-tale sign of the pathogen's presence that triggers the plant to defend itself against infection. © The Author 2015. Published by Oxford University Press on behalf of the Society for Experimental Biology.
KAUST Department:
Biological and Environmental Sciences and Engineering (BESE) Division
Citation:
The dual nature of trehalose in citrus canker disease: a virulence factor for Xanthomonas citri subsp. citri and a trigger for plant defence responses 2015 Journal of Experimental Botany
Publisher:
Oxford University Press (OUP)
Journal:
Journal of Experimental Botany
Issue Date:
14-Mar-2015
DOI:
10.1093/jxb/erv095
PubMed ID:
25770587
Type:
Article
ISSN:
0022-0957; 1460-2431
Additional Links:
http://jxb.oxfordjournals.org/lookup/doi/10.1093/jxb/erv095
Appears in Collections:
Articles; Biological and Environmental Sciences and Engineering (BESE) Division

Full metadata record

DC FieldValue Language
dc.contributor.authorPiazza, A.en
dc.contributor.authorZimaro, T.en
dc.contributor.authorGaravaglia, B. S.en
dc.contributor.authorFicarra, F. A.en
dc.contributor.authorThomas, L.en
dc.contributor.authorMarondedze, C.en
dc.contributor.authorFeil, R.en
dc.contributor.authorLunn, J. E.en
dc.contributor.authorGehring, Christoph A.en
dc.contributor.authorOttado, J.en
dc.contributor.authorGottig, N.en
dc.date.accessioned2015-03-23T08:06:44Zen
dc.date.available2015-03-23T08:06:44Zen
dc.date.issued2015-03-14en
dc.identifier.citationThe dual nature of trehalose in citrus canker disease: a virulence factor for Xanthomonas citri subsp. citri and a trigger for plant defence responses 2015 Journal of Experimental Botanyen
dc.identifier.issn0022-0957en
dc.identifier.issn1460-2431en
dc.identifier.pmid25770587-
dc.identifier.doi10.1093/jxb/erv095en
dc.identifier.urihttp://hdl.handle.net/10754/346976en
dc.description.abstractXanthomonas citri subsp. citri (Xcc) is a bacterial pathogen that causes citrus canker in susceptible Citrus spp. The Xcc genome contains genes encoding enzymes from three separate pathways of trehalose biosynthesis. Expression of genes encoding trehalose-6-phosphate synthase (otsA) and trehalose phosphatase (otsB) was highly induced during canker development, suggesting that the two-step pathway of trehalose biosynthesis via trehalose-6-phosphate has a function in pathogenesis. This pathway was eliminated from the bacterium by deletion of the otsA gene. The resulting XccΔotsA mutant produced less trehalose than the wild-type strain, was less resistant to salt and oxidative stresses, and was less able to colonize plant tissues. Gene expression and proteomic analyses of infected leaves showed that infection with XccΔotsA triggered only weak defence responses in the plant compared with infection with Xcc, and had less impact on the host plant's metabolism than the wild-type strain. These results suggested that trehalose of bacterial origin, synthesized via the otsA-otsB pathway, in Xcc, plays a role in modifying the host plant's metabolism to its own advantage but is also perceived by the plant as a sign of pathogen attack. Thus, trehalose biosynthesis has both positive and negative consequences for Xcc. On the one hand, it enables this bacterial pathogen to survive in the inhospitable environment of the leaf surface before infection and exploit the host plant's resources after infection, but on the other hand, it is a tell-tale sign of the pathogen's presence that triggers the plant to defend itself against infection. © The Author 2015. Published by Oxford University Press on behalf of the Society for Experimental Biology.en
dc.publisherOxford University Press (OUP)en
dc.relation.urlhttp://jxb.oxfordjournals.org/lookup/doi/10.1093/jxb/erv095en
dc.rightsThis is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.en
dc.titleThe dual nature of trehalose in citrus canker disease: a virulence factor for Xanthomonas citri subsp. citri and a trigger for plant defence responsesen
dc.typeArticleen
dc.contributor.departmentBiological and Environmental Sciences and Engineering (BESE) Divisionen
dc.identifier.journalJournal of Experimental Botanyen
dc.eprint.versionPublisher's Version/PDFen
dc.contributor.institutionInstituto de Biología Molecular y Celular de Rosario, Consejo Nacional de Investigaciones Científicas y Técnicas (IBR-CONICET) and Facultad de Ciencias Bioquímicas y Farmacéuticas, Universidad Nacional de Rosario, Ocampo y Esmeralda, Rosario 2000, Argentinaen
dc.contributor.institutionMax Planck Institute of Molecular Plant Physiology, Wissenschaftspark Golm, Am Mühlenberg 1, 14476 Potsdam (OT) Golm, Germanyen
dc.contributor.affiliationKing Abdullah University of Science and Technology (KAUST)en
kaust.authorThomas, Ludivineen
kaust.authorMarondedze, Claudiusen
kaust.authorGehring, Christoph A.en
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