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

Autores
Piazza, Ainelén Melanie; Zimaro, Tamara; Garavaglia, Betiana Soledad; Ficarra, Florencia Andrea; Thomas, Ludivine; Marondedze, Claudius; Feil, Regina; Lunn, John E.; Gehring, Chris; Ottado, Jorgelina; Gottig Schor, Natalia
Año de publicación
2015
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
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.
Fil: Piazza, Ainelén Melanie. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; Argentina
Fil: Zimaro, Tamara. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; Argentina
Fil: Garavaglia, Betiana Soledad. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; Argentina
Fil: Ficarra, Florencia Andrea. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; Argentina
Fil: Thomas, Ludivine. King Abdullah University of Science and Technology; Arabia Saudita
Fil: Marondedze, Claudius. King Abdullah University of Science and Technology; Arabia Saudita
Fil: Feil, Regina. Max Planck Institute of Molecular Plant Physiology; Alemania
Fil: Lunn, John E.. Max Planck Institute of Molecular Plant Physiology; Alemania
Fil: Gehring, Chris. King Abdullah University of Science and Technology; Arabia Saudita
Fil: Ottado, Jorgelina. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; Argentina
Fil: Gottig Schor, Natalia. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; Argentina
Materia
CANKER
CITRUS
DEFENCE
OTSA
TREHALOSE
XANTHOMONAS
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/50487
Acceder
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repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling The dual nature of trehalose in citrus canker disease: A virulence factor for Xanthomonas citri subsp. citri and a trigger for plant defence responsesPiazza, Ainelén MelanieZimaro, TamaraGaravaglia, Betiana SoledadFicarra, Florencia AndreaThomas, LudivineMarondedze, ClaudiusFeil, ReginaLunn, John E.Gehring, ChrisOttado, JorgelinaGottig Schor, NataliaCANKERCITRUSDEFENCEOTSATREHALOSEXANTHOMONAShttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Xanthomonas 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.Fil: Piazza, Ainelén Melanie. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; ArgentinaFil: Zimaro, Tamara. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; ArgentinaFil: Garavaglia, Betiana Soledad. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; ArgentinaFil: Ficarra, Florencia Andrea. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; ArgentinaFil: Thomas, Ludivine. King Abdullah University of Science and Technology; Arabia SauditaFil: Marondedze, Claudius. King Abdullah University of Science and Technology; Arabia SauditaFil: Feil, Regina. Max Planck Institute of Molecular Plant Physiology; AlemaniaFil: Lunn, John E.. Max Planck Institute of Molecular Plant Physiology; AlemaniaFil: Gehring, Chris. King Abdullah University of Science and Technology; Arabia SauditaFil: Ottado, Jorgelina. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; ArgentinaFil: Gottig Schor, Natalia. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; ArgentinaOxford University Press2015-05info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfapplication/pdfapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/50487Piazza, Ainelén Melanie; Zimaro, Tamara; Garavaglia, Betiana Soledad; Ficarra, Florencia Andrea; Thomas, Ludivine; et al.; The dual nature of trehalose in citrus canker disease: A virulence factor for Xanthomonas citri subsp. citri and a trigger for plant defence responses; Oxford University Press; Journal of Experimental Botany; 66; 9; 5-2015; 2795-28110022-09571460-2431CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/http://jxb.oxfordjournals.org/content/early/2015/03/13/jxb.erv095.full.pdf+htmlinfo:eu-repo/semantics/altIdentifier/doi/10.1093/jxb/erv095info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-03T09:45:02Zoai:ri.conicet.gov.ar:11336/50487instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-09-03 09:45:02.338CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv The dual nature of trehalose in citrus canker disease: A virulence factor for Xanthomonas citri subsp. citri and a trigger for plant defence responses
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
spellingShingle The dual nature of trehalose in citrus canker disease: A virulence factor for Xanthomonas citri subsp. citri and a trigger for plant defence responses
Piazza, Ainelén Melanie
CANKER
CITRUS
DEFENCE
OTSA
TREHALOSE
XANTHOMONAS
title_short The dual nature of trehalose in citrus canker disease: A virulence factor for Xanthomonas citri subsp. citri and a trigger for plant defence responses
title_full The dual nature of trehalose in citrus canker disease: A virulence factor for Xanthomonas citri subsp. citri and a trigger for plant defence responses
title_fullStr The dual nature of trehalose in citrus canker disease: A virulence factor for Xanthomonas citri subsp. citri and a trigger for plant defence responses
title_full_unstemmed The dual nature of trehalose in citrus canker disease: A virulence factor for Xanthomonas citri subsp. citri and a trigger for plant defence responses
title_sort The dual nature of trehalose in citrus canker disease: A virulence factor for Xanthomonas citri subsp. citri and a trigger for plant defence responses
dc.creator.none.fl_str_mv Piazza, Ainelén Melanie
Zimaro, Tamara
Garavaglia, Betiana Soledad
Ficarra, Florencia Andrea
Thomas, Ludivine
Marondedze, Claudius
Feil, Regina
Lunn, John E.
Gehring, Chris
Ottado, Jorgelina
Gottig Schor, Natalia
author Piazza, Ainelén Melanie
author_facet Piazza, Ainelén Melanie
Zimaro, Tamara
Garavaglia, Betiana Soledad
Ficarra, Florencia Andrea
Thomas, Ludivine
Marondedze, Claudius
Feil, Regina
Lunn, John E.
Gehring, Chris
Ottado, Jorgelina
Gottig Schor, Natalia
author_role author
author2 Zimaro, Tamara
Garavaglia, Betiana Soledad
Ficarra, Florencia Andrea
Thomas, Ludivine
Marondedze, Claudius
Feil, Regina
Lunn, John E.
Gehring, Chris
Ottado, Jorgelina
Gottig Schor, Natalia
author2_role author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv CANKER
CITRUS
DEFENCE
OTSA
TREHALOSE
XANTHOMONAS
topic CANKER
CITRUS
DEFENCE
OTSA
TREHALOSE
XANTHOMONAS
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv 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.
Fil: Piazza, Ainelén Melanie. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; Argentina
Fil: Zimaro, Tamara. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; Argentina
Fil: Garavaglia, Betiana Soledad. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; Argentina
Fil: Ficarra, Florencia Andrea. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; Argentina
Fil: Thomas, Ludivine. King Abdullah University of Science and Technology; Arabia Saudita
Fil: Marondedze, Claudius. King Abdullah University of Science and Technology; Arabia Saudita
Fil: Feil, Regina. Max Planck Institute of Molecular Plant Physiology; Alemania
Fil: Lunn, John E.. Max Planck Institute of Molecular Plant Physiology; Alemania
Fil: Gehring, Chris. King Abdullah University of Science and Technology; Arabia Saudita
Fil: Ottado, Jorgelina. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; Argentina
Fil: Gottig Schor, Natalia. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; Argentina
description 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.
publishDate 2015
dc.date.none.fl_str_mv 2015-05
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/50487
Piazza, Ainelén Melanie; Zimaro, Tamara; Garavaglia, Betiana Soledad; Ficarra, Florencia Andrea; Thomas, Ludivine; et al.; The dual nature of trehalose in citrus canker disease: A virulence factor for Xanthomonas citri subsp. citri and a trigger for plant defence responses; Oxford University Press; Journal of Experimental Botany; 66; 9; 5-2015; 2795-2811
0022-0957
1460-2431
CONICET Digital
CONICET
url http://hdl.handle.net/11336/50487
identifier_str_mv Piazza, Ainelén Melanie; Zimaro, Tamara; Garavaglia, Betiana Soledad; Ficarra, Florencia Andrea; Thomas, Ludivine; et al.; The dual nature of trehalose in citrus canker disease: A virulence factor for Xanthomonas citri subsp. citri and a trigger for plant defence responses; Oxford University Press; Journal of Experimental Botany; 66; 9; 5-2015; 2795-2811
0022-0957
1460-2431
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/url/http://jxb.oxfordjournals.org/content/early/2015/03/13/jxb.erv095.full.pdf+html
info:eu-repo/semantics/altIdentifier/doi/10.1093/jxb/erv095
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
application/pdf
application/pdf
application/pdf
dc.publisher.none.fl_str_mv Oxford University Press
publisher.none.fl_str_mv Oxford University Press
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
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instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
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