Allelic variation in the indoleacetic acid-lysine synthase gene of the bacterial pathogen Pseudomonas savastanoi and its role in auxin production

Indole-3-acetic acid (IAA) production is a pathogenicity/virulence factor in the Pseudomonas syringae complex, including Pseudomonas savastanoi. P. savastanoi pathovars (pvs.) genomes contain the iaaL gene, encoding an enzyme that catalyzes the biosynthesis of the less biologically active compound 3...

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Autores: Pintado, Adrián, Domínguez-Cerván, Hilario, Pastor, Victoria, Vincent, Marissa, Lee, Soon Goo, Flors, Víctor, Ramos, Cayo
Tipo de recurso: artículo
Estado:Versión aceptada para publicación
Fecha de publicación:2023
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/371768
Acceso en línea:http://hdl.handle.net/10261/371768
https://api.elsevier.com/content/abstract/scopus_id/85162210316
Access Level:acceso abierto
Palabra clave:IAA - Indole-3-acetic acid
IAA-lysine synthase
Pseudomonas savastanoi
Pseudomonas syringae
allelic variation
auxin
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network_acronym_str ES
network_name_str España
repository_id_str
dc.title.none.fl_str_mv Allelic variation in the indoleacetic acid-lysine synthase gene of the bacterial pathogen Pseudomonas savastanoi and its role in auxin production
title Allelic variation in the indoleacetic acid-lysine synthase gene of the bacterial pathogen Pseudomonas savastanoi and its role in auxin production
spellingShingle Allelic variation in the indoleacetic acid-lysine synthase gene of the bacterial pathogen Pseudomonas savastanoi and its role in auxin production
Pintado, Adrián
IAA - Indole-3-acetic acid
IAA-lysine synthase
Pseudomonas savastanoi
Pseudomonas syringae
allelic variation
auxin
title_short Allelic variation in the indoleacetic acid-lysine synthase gene of the bacterial pathogen Pseudomonas savastanoi and its role in auxin production
title_full Allelic variation in the indoleacetic acid-lysine synthase gene of the bacterial pathogen Pseudomonas savastanoi and its role in auxin production
title_fullStr Allelic variation in the indoleacetic acid-lysine synthase gene of the bacterial pathogen Pseudomonas savastanoi and its role in auxin production
title_full_unstemmed Allelic variation in the indoleacetic acid-lysine synthase gene of the bacterial pathogen Pseudomonas savastanoi and its role in auxin production
title_sort Allelic variation in the indoleacetic acid-lysine synthase gene of the bacterial pathogen Pseudomonas savastanoi and its role in auxin production
dc.creator.none.fl_str_mv Pintado, Adrián
Domínguez-Cerván, Hilario
Pastor, Victoria
Vincent, Marissa
Lee, Soon Goo
Flors, Víctor
Ramos, Cayo
author Pintado, Adrián
author_facet Pintado, Adrián
Domínguez-Cerván, Hilario
Pastor, Victoria
Vincent, Marissa
Lee, Soon Goo
Flors, Víctor
Ramos, Cayo
author_role author
author2 Domínguez-Cerván, Hilario
Pastor, Victoria
Vincent, Marissa
Lee, Soon Goo
Flors, Víctor
Ramos, Cayo
author2_role author
author
author
author
author
author
dc.contributor.none.fl_str_mv Ministerio de Ciencia, Innovación y Universidades (España)
Generalitat Valenciana
North Carolina Biotechnology Center
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv IAA - Indole-3-acetic acid
IAA-lysine synthase
Pseudomonas savastanoi
Pseudomonas syringae
allelic variation
auxin
topic IAA - Indole-3-acetic acid
IAA-lysine synthase
Pseudomonas savastanoi
Pseudomonas syringae
allelic variation
auxin
description Indole-3-acetic acid (IAA) production is a pathogenicity/virulence factor in the Pseudomonas syringae complex, including Pseudomonas savastanoi. P. savastanoi pathovars (pvs.) genomes contain the iaaL gene, encoding an enzyme that catalyzes the biosynthesis of the less biologically active compound 3-indole-acetyl-ϵ-L-lysine (IAA-Lys). Previous studies have reported the identification of IAA-Lys in culture filtrates of P. savastanoi strains isolated from oleander (pv. nerii), but the conversion of IAA into a conjugate was not detectable in olive strains (pv. savastanoi). In this paper, we show the distribution of iaaL alleles in all available P. savastanoi genomes of strains isolated from woody hosts. Most strains encode two different paralogs, except for those isolated from broom (pv. retacarpa), which contain a single allele. In addition to the three previously reported iaaL alleles (iaaL Psv, iaaL Psn and iaaL Pto), we identified iaaL Psf, an exclusive allele of strains isolated from ash (pv. fraxini). We also found that the production of IAA-Lys in P. savastanoi pv. savastanoi and pv. nerii depends on a functional iaaL Psn allele, whereas in pv. fraxini depends on iaaL Psf. The production of IAA-Lys was detected in cultures of an olive strain heterologously expressing IaaLPsn-1, IaaLPsf-1 and IaaLPsf-3, but not when expressing IaaLPsv-1. In addition, Arabidopsis seedlings treated with the strains overproducing the conjugate, and thus reducing the free IAA content, alleviated the root elongation inhibitory effect of IAA. IAA-Lys synthase activity assays with purified allozymes confirmed the functionality and specificity of lysine as a substrate of IaaLPsn-1 and IaaLPsf-3, with IaaLPsf-3 showing the highest catalytic efficiency for both substrates. The IAA-Lys synthase activity of IaaLPsn-1 was abolished by the insertion of two additional tyrosine residues encoded in the inactive allozyme IaaLPsv-1. These results highlight the relevance of allelic variation in a phytohormone-related gene for the modulation of auxin production in a bacterial phytopathogen.
publishDate 2023
dc.date.none.fl_str_mv 2023
2024
2024
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http://purl.org/coar/resource_type/c_6501
Postprint
info:eu-repo/semantics/acceptedVersion
format article
status_str acceptedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/371768
https://api.elsevier.com/content/abstract/scopus_id/85162210316
url http://hdl.handle.net/10261/371768
https://api.elsevier.com/content/abstract/scopus_id/85162210316
dc.language.none.fl_str_mv Inglés
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info:eu-repo/grantAgreement/MECD//FPU14%2F05551
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info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2020-115177RB-C21
info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/RTI2018-094350-B-C33
Frontiers in plant science
https://doi.org/10.3389/fpls.2023.1176705
Sí
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dc.publisher.none.fl_str_mv Frontiers Media
publisher.none.fl_str_mv Frontiers Media
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instname:Consejo Superior de Investigaciones Científicas (CSIC)
instname_str Consejo Superior de Investigaciones Científicas (CSIC)
reponame_str DIGITAL.CSIC. Repositorio Institucional del CSIC
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spelling Allelic variation in the indoleacetic acid-lysine synthase gene of the bacterial pathogen Pseudomonas savastanoi and its role in auxin productionPintado, AdriánDomínguez-Cerván, HilarioPastor, VictoriaVincent, MarissaLee, Soon GooFlors, VíctorRamos, CayoIAA - Indole-3-acetic acidIAA-lysine synthasePseudomonas savastanoiPseudomonas syringaeallelic variationauxinIndole-3-acetic acid (IAA) production is a pathogenicity/virulence factor in the Pseudomonas syringae complex, including Pseudomonas savastanoi. P. savastanoi pathovars (pvs.) genomes contain the iaaL gene, encoding an enzyme that catalyzes the biosynthesis of the less biologically active compound 3-indole-acetyl-ϵ-L-lysine (IAA-Lys). Previous studies have reported the identification of IAA-Lys in culture filtrates of P. savastanoi strains isolated from oleander (pv. nerii), but the conversion of IAA into a conjugate was not detectable in olive strains (pv. savastanoi). In this paper, we show the distribution of iaaL alleles in all available P. savastanoi genomes of strains isolated from woody hosts. Most strains encode two different paralogs, except for those isolated from broom (pv. retacarpa), which contain a single allele. In addition to the three previously reported iaaL alleles (iaaL Psv, iaaL Psn and iaaL Pto), we identified iaaL Psf, an exclusive allele of strains isolated from ash (pv. fraxini). We also found that the production of IAA-Lys in P. savastanoi pv. savastanoi and pv. nerii depends on a functional iaaL Psn allele, whereas in pv. fraxini depends on iaaL Psf. The production of IAA-Lys was detected in cultures of an olive strain heterologously expressing IaaLPsn-1, IaaLPsf-1 and IaaLPsf-3, but not when expressing IaaLPsv-1. In addition, Arabidopsis seedlings treated with the strains overproducing the conjugate, and thus reducing the free IAA content, alleviated the root elongation inhibitory effect of IAA. IAA-Lys synthase activity assays with purified allozymes confirmed the functionality and specificity of lysine as a substrate of IaaLPsn-1 and IaaLPsf-3, with IaaLPsf-3 showing the highest catalytic efficiency for both substrates. The IAA-Lys synthase activity of IaaLPsn-1 was abolished by the insertion of two additional tyrosine residues encoded in the inactive allozyme IaaLPsv-1. These results highlight the relevance of allelic variation in a phytohormone-related gene for the modulation of auxin production in a bacterial phytopathogen.AP and HD-C were supported by the FPU14/05551 and PRE2021-099113 predoctoral grants, respectively. CR was supported by the AGL2017-82492-C2-1-R and PID2020-115177RB-C21 project grants from the Spanish Ministry of Science, Innovation and Universities (Spain), co-financed by the European Regional Development Fund (ERDF). VP and VF were supported by the GV/2018/115 and CIACO/2021/092 grant projects from Generalitat Valenciana and the RTI2018-094350-B-C33 grant from the Spanish Ministry of Science, Innovation and Universities. MV and SL were supported by project grant A20-0079 from The North Carolina Biotechnology Center (NCBC).Peer reviewedFrontiers MediaMinisterio de Ciencia, Innovación y Universidades (España)Generalitat ValencianaNorth Carolina Biotechnology CenterConsejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]202420242023info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Postprintinfo:eu-repo/semantics/acceptedVersionhttp://hdl.handle.net/10261/371768https://api.elsevier.com/content/abstract/scopus_id/85162210316reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Inglés#PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE#info:eu-repo/grantAgreement/MECD//FPU14%2F05551info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016/AGL2017-82492-C2-1-Rinfo:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2020-115177RB-C21info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/RTI2018-094350-B-C33Frontiers in plant sciencehttps://doi.org/10.3389/fpls.2023.1176705Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/3717682026-05-22T06:33:51Z
score 15,811543

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