An NADPH oxidase regulates carbon metabolism and the cell cycle during root nodule symbiosis in common bean (Phaseolus vulgaris)

Abstract Background Rhizobium–legume symbiosis is a specific, coordinated interaction that results in the formation of a root nodule, where biological nitrogen fixation occurs. NADPH oxidases, or Respiratory Burst Oxidase Homologs (RBOHs) in plants, are enzymes that generate superoxide (O2 •−). Supe...

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Main Authors: Citlali Fonseca-García, Noreide Nava, Miguel Lara, Carmen Quinto
Format: Article
Language:English
Published: BMC 2021-06-01
Series:BMC Plant Biology
Subjects:
Online Access:https://doi.org/10.1186/s12870-021-03060-z
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author Citlali Fonseca-García
Noreide Nava
Miguel Lara
Carmen Quinto
author_facet Citlali Fonseca-García
Noreide Nava
Miguel Lara
Carmen Quinto
author_sort Citlali Fonseca-García
collection DOAJ
description Abstract Background Rhizobium–legume symbiosis is a specific, coordinated interaction that results in the formation of a root nodule, where biological nitrogen fixation occurs. NADPH oxidases, or Respiratory Burst Oxidase Homologs (RBOHs) in plants, are enzymes that generate superoxide (O2 •−). Superoxide produces other reactive oxygen species (ROS); these ROS regulate different stages of mutualistic interactions. For example, changes in ROS levels are thought to induce ROS scavenging, cell wall remodeling, and changes in phytohormone homeostasis during symbiotic interactions. In common bean (Phaseolus vulgaris), PvRbohB plays a key role in the early stages of nodulation. Results In this study, to explore the role of PvRbohB in root nodule symbiosis, we analyzed transcriptomic data from the roots of common bean under control conditions (transgenic roots without construction) and roots with downregulated expression of PvRbohB (by RNA interference) non-inoculated and inoculated with R. tropici. Our results suggest that ROS produced by PvRBOHB play a central role in infection thread formation and nodule organogenesis through crosstalk with flavonoids, carbon metabolism, cell cycle regulation, and the plant hormones auxin and cytokinin during the early stages of this process. Conclusions Our findings provide important insight into the multiple roles of ROS in regulating rhizobia–legume symbiosis.
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spelling doaj.art-f94e1b266b564838a1935b30ae243a852022-12-21T20:25:19ZengBMCBMC Plant Biology1471-22292021-06-0121111610.1186/s12870-021-03060-zAn NADPH oxidase regulates carbon metabolism and the cell cycle during root nodule symbiosis in common bean (Phaseolus vulgaris)Citlali Fonseca-García0Noreide Nava1Miguel Lara2Carmen Quinto3Departamento de Biología Molecular de Plantas, Instituto de Biotecnología, Universidad Nacional Autónoma de México, Avenida UniversidadDepartamento de Biología Molecular de Plantas, Instituto de Biotecnología, Universidad Nacional Autónoma de México, Avenida UniversidadDepartamento de Biología Molecular de Plantas, Instituto de Biotecnología, Universidad Nacional Autónoma de México, Avenida UniversidadDepartamento de Biología Molecular de Plantas, Instituto de Biotecnología, Universidad Nacional Autónoma de México, Avenida UniversidadAbstract Background Rhizobium–legume symbiosis is a specific, coordinated interaction that results in the formation of a root nodule, where biological nitrogen fixation occurs. NADPH oxidases, or Respiratory Burst Oxidase Homologs (RBOHs) in plants, are enzymes that generate superoxide (O2 •−). Superoxide produces other reactive oxygen species (ROS); these ROS regulate different stages of mutualistic interactions. For example, changes in ROS levels are thought to induce ROS scavenging, cell wall remodeling, and changes in phytohormone homeostasis during symbiotic interactions. In common bean (Phaseolus vulgaris), PvRbohB plays a key role in the early stages of nodulation. Results In this study, to explore the role of PvRbohB in root nodule symbiosis, we analyzed transcriptomic data from the roots of common bean under control conditions (transgenic roots without construction) and roots with downregulated expression of PvRbohB (by RNA interference) non-inoculated and inoculated with R. tropici. Our results suggest that ROS produced by PvRBOHB play a central role in infection thread formation and nodule organogenesis through crosstalk with flavonoids, carbon metabolism, cell cycle regulation, and the plant hormones auxin and cytokinin during the early stages of this process. Conclusions Our findings provide important insight into the multiple roles of ROS in regulating rhizobia–legume symbiosis.https://doi.org/10.1186/s12870-021-03060-zTranscriptomeCommon beanPvRbohBNodulationSymbiosis
spellingShingle Citlali Fonseca-García
Noreide Nava
Miguel Lara
Carmen Quinto
An NADPH oxidase regulates carbon metabolism and the cell cycle during root nodule symbiosis in common bean (Phaseolus vulgaris)
BMC Plant Biology
Transcriptome
Common bean
PvRbohB
Nodulation
Symbiosis
title An NADPH oxidase regulates carbon metabolism and the cell cycle during root nodule symbiosis in common bean (Phaseolus vulgaris)
title_full An NADPH oxidase regulates carbon metabolism and the cell cycle during root nodule symbiosis in common bean (Phaseolus vulgaris)
title_fullStr An NADPH oxidase regulates carbon metabolism and the cell cycle during root nodule symbiosis in common bean (Phaseolus vulgaris)
title_full_unstemmed An NADPH oxidase regulates carbon metabolism and the cell cycle during root nodule symbiosis in common bean (Phaseolus vulgaris)
title_short An NADPH oxidase regulates carbon metabolism and the cell cycle during root nodule symbiosis in common bean (Phaseolus vulgaris)
title_sort nadph oxidase regulates carbon metabolism and the cell cycle during root nodule symbiosis in common bean phaseolus vulgaris
topic Transcriptome
Common bean
PvRbohB
Nodulation
Symbiosis
url https://doi.org/10.1186/s12870-021-03060-z
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