Bacterial auxin catabolism as a driver of plant growth promotion and rhizosphere colonization fitness

Inter-kingdom communication between plants and their associated microbiota is central to plant development and environmental adaptation. Indole-3-acetic acid (IAA) is the primary auxin in plants and regulates plant growth and development, while also modulating bacterial physiology and behavior. The...

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Detalles Bibliográficos
Autores: Roca, Amalia, Gorts, Juan, Matilla, Miguel A.
Tipo de recurso: artículo
Fecha de publicación:2026
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:dnet:digitalcsic_::8833cd9cad6f7599b20c21f3ccf1a082
Acceso en línea:http://hdl.handle.net/10261/428376
Access Level:acceso abierto
Palabra clave:Pseudomonas putida
Signaling
AuxinIndole-3-acetic acid
Rhizosphere
Plant growth promotion
Catabolism
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spelling Bacterial auxin catabolism as a driver of plant growth promotion and rhizosphere colonization fitnessRoca, AmaliaGorts, JuanMatilla, Miguel A.Pseudomonas putidaSignalingAuxinIndole-3-acetic acidRhizospherePlant growth promotionCatabolismInter-kingdom communication between plants and their associated microbiota is central to plant development and environmental adaptation. Indole-3-acetic acid (IAA) is the primary auxin in plants and regulates plant growth and development, while also modulating bacterial physiology and behavior. The concentration at which IAA exerts its biological effects in plants is critical and maintaining auxin homeostasis is essential. Although IAA production by plant growth-promoting bacteria typically stimulates plant growth, excessive IAA levels can be detrimental to plant physiology. Here, we investigate the in planta functional role of bacterial IAA catabolism using Pseudomonas putida 1290, a model plant-associated bacterium that degrades IAA through the Iac aerobic pathway. By constructing a mutant strain defective in the iac gene cluster, we show that IAA catabolism is essential for reversing auxin-mediated growth inhibition in tomato and maize, both in vitro and in microcosms. In addition, bacterial IAA degradation also prevented the formation of IAA-induced tumor-like structures in maize roots. Moreover, competitive colonization assays revealed that IAA catabolism enhances bacterial fitness in the rhizosphere, particularly under high-auxin conditions. Our findings establish bacterial IAA catabolism as a mechanism of metabolic signal interference that maintains auxin homeostasis in planta and promotes successful rhizosphere colonization. This work highlights the significance of microbial auxin metabolism in shaping plant–microbe interactions and its potential for application in sustainable agriculture strategies.This study was supported through grants from the Spanish Ministry for Science, Innovation and Universities/Agencia Estatal de Investigación 10.13039/501100011033 and FEDER-EU (PID2023-146281NB-I00 to A.R. and M.A.M.) A.R. was supported by the Ramon y Cajal R&D&i Programme (RYC2019–026481-I) from the Spanish Ministry for Science and Innovation/Agencia Estatal de Investigación 10.13039/501100011033 y FSE 'El FSE invierte en tu futuro'. We thank Alicia Rodríguez-Sánchez and Rafael Núñez-Gómez from the Microscopy and Scientific Instrumentation Services at Estación Experimental del Zaidín (CSIC) for their invaluable technical assistance.ElsevierMinisterio de Ciencia, Innovación y Universidades (España)Agencia Estatal de Investigación (España)European CommissionMinisterio de Ciencia e Innovación (España)Matilla, Miguel A. [0000-0002-8468-9604]Roca, Amalia [0000-0003-2332-3112]Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]2026202620262026info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501http://hdl.handle.net/10261/428376reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)#PLACEHOLDER_PARENT_METADATA_VALUE#info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2021-2023/PID2023-146281NB-I00http://dx.doi.org/10.1016/j.micres.2025.128431Síinfo:eu-repo/semantics/openAccessoai:dnet:digitalcsic_::8833cd9cad6f7599b20c21f3ccf1a0822026-05-22T06:33:51Z
dc.title.none.fl_str_mv Bacterial auxin catabolism as a driver of plant growth promotion and rhizosphere colonization fitness
title Bacterial auxin catabolism as a driver of plant growth promotion and rhizosphere colonization fitness
spellingShingle Bacterial auxin catabolism as a driver of plant growth promotion and rhizosphere colonization fitness
Roca, Amalia
Pseudomonas putida
Signaling
AuxinIndole-3-acetic acid
Rhizosphere
Plant growth promotion
Catabolism
title_short Bacterial auxin catabolism as a driver of plant growth promotion and rhizosphere colonization fitness
title_full Bacterial auxin catabolism as a driver of plant growth promotion and rhizosphere colonization fitness
title_fullStr Bacterial auxin catabolism as a driver of plant growth promotion and rhizosphere colonization fitness
title_full_unstemmed Bacterial auxin catabolism as a driver of plant growth promotion and rhizosphere colonization fitness
title_sort Bacterial auxin catabolism as a driver of plant growth promotion and rhizosphere colonization fitness
dc.creator.none.fl_str_mv Roca, Amalia
Gorts, Juan
Matilla, Miguel A.
author Roca, Amalia
author_facet Roca, Amalia
Gorts, Juan
Matilla, Miguel A.
author_role author
author2 Gorts, Juan
Matilla, Miguel A.
author2_role author
author
dc.contributor.none.fl_str_mv Ministerio de Ciencia, Innovación y Universidades (España)
Agencia Estatal de Investigación (España)
European Commission
Ministerio de Ciencia e Innovación (España)
Matilla, Miguel A. [0000-0002-8468-9604]
Roca, Amalia [0000-0003-2332-3112]
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Pseudomonas putida
Signaling
AuxinIndole-3-acetic acid
Rhizosphere
Plant growth promotion
Catabolism
topic Pseudomonas putida
Signaling
AuxinIndole-3-acetic acid
Rhizosphere
Plant growth promotion
Catabolism
description Inter-kingdom communication between plants and their associated microbiota is central to plant development and environmental adaptation. Indole-3-acetic acid (IAA) is the primary auxin in plants and regulates plant growth and development, while also modulating bacterial physiology and behavior. The concentration at which IAA exerts its biological effects in plants is critical and maintaining auxin homeostasis is essential. Although IAA production by plant growth-promoting bacteria typically stimulates plant growth, excessive IAA levels can be detrimental to plant physiology. Here, we investigate the in planta functional role of bacterial IAA catabolism using Pseudomonas putida 1290, a model plant-associated bacterium that degrades IAA through the Iac aerobic pathway. By constructing a mutant strain defective in the iac gene cluster, we show that IAA catabolism is essential for reversing auxin-mediated growth inhibition in tomato and maize, both in vitro and in microcosms. In addition, bacterial IAA degradation also prevented the formation of IAA-induced tumor-like structures in maize roots. Moreover, competitive colonization assays revealed that IAA catabolism enhances bacterial fitness in the rhizosphere, particularly under high-auxin conditions. Our findings establish bacterial IAA catabolism as a mechanism of metabolic signal interference that maintains auxin homeostasis in planta and promotes successful rhizosphere colonization. This work highlights the significance of microbial auxin metabolism in shaping plant–microbe interactions and its potential for application in sustainable agriculture strategies.
publishDate 2026
dc.date.none.fl_str_mv 2026
2026
2026
2026
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
format article
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/428376
url http://hdl.handle.net/10261/428376
dc.relation.none.fl_str_mv #PLACEHOLDER_PARENT_METADATA_VALUE#
info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2021-2023/PID2023-146281NB-I00
http://dx.doi.org/10.1016/j.micres.2025.128431
Sí
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv Elsevier
publisher.none.fl_str_mv Elsevier
dc.source.none.fl_str_mv reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC
instname:Consejo Superior de Investigaciones Científicas (CSIC)
instname_str Consejo Superior de Investigaciones Científicas (CSIC)
reponame_str DIGITAL.CSIC. Repositorio Institucional del CSIC
collection DIGITAL.CSIC. Repositorio Institucional del CSIC
repository.name.fl_str_mv
repository.mail.fl_str_mv
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