Unraveling the drought-responsive transcriptomes in nodules of two common bean genotypes during biological nitrogen fixation

Common bean (Phaseolus vulgaris) can efficiently fix atmospheric nitrogen when associated with Rhizobia. However, drought stress impairs plant metabolic processes, especially the biological nitrogen fixation (BNF). Here, we assessed transcriptional responses in nodules of two common bean genotypes t...

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Main Authors: Helder Anderson Pinto da Silva, Vanessa Santana Caetano, Daniella Duarte Villarinho Pessôa, Rafael Sanches Pacheco, Carlos Henrique S. G. Meneses, Jean Luiz Simões-Araújo
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-01-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2024.1345379/full
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author Helder Anderson Pinto da Silva
Vanessa Santana Caetano
Daniella Duarte Villarinho Pessôa
Rafael Sanches Pacheco
Carlos Henrique S. G. Meneses
Jean Luiz Simões-Araújo
Jean Luiz Simões-Araújo
Jean Luiz Simões-Araújo
author_facet Helder Anderson Pinto da Silva
Vanessa Santana Caetano
Daniella Duarte Villarinho Pessôa
Rafael Sanches Pacheco
Carlos Henrique S. G. Meneses
Jean Luiz Simões-Araújo
Jean Luiz Simões-Araújo
Jean Luiz Simões-Araújo
author_sort Helder Anderson Pinto da Silva
collection DOAJ
description Common bean (Phaseolus vulgaris) can efficiently fix atmospheric nitrogen when associated with Rhizobia. However, drought stress impairs plant metabolic processes, especially the biological nitrogen fixation (BNF). Here, we assessed transcriptional responses in nodules of two common bean genotypes to drought stress under BNF reliance. The RNA-Seq analysis yielded a total of 81,489,262 and 72,497,478 high quality reads for Negro Argel and BAT 477 genotypes, respectively. The reads were mapped to the Phaseolus vulgaris reference genome and expression analysis identified 145 and 1451 differentially expressed genes (DEGs) for Negro Argel and BAT 477 genotypes, respectively. Although BAT 477 had more DEGs, both genotypes shared certain drought-responsive genes, including an up-regulated heat shock protein (HSP) and a down-regulated peroxidase, indicating shared pathways activated during drought in nodule tissue. Functional analysis using MapMan software highlighted the up-regulation of genes involved in abiotic stress responses, such as HSPs and specific transcription factors (TFs), in both genotypes. There was a significant down-regulation in metabolic pathways related to antioxidant protection, hormone signaling, metabolism, and transcriptional regulation. To validate these findings, we conducted RT-qPCR experiments for ten DEGs in nodules from both genotypes, for which the expression profile was confirmed, thus reinforcing their functional relevance in the nodule responses to drought stress during BNF. BAT 477 genotype exhibited more pronounced response to drought, characterized by a high number of DEGs. The strong down-regulation of DEGs leads to transcriptional disturbances in several pathways related to stress acclimation such as hormone and antioxidant metabolism. Additionally, we identified several genes that are known to play key roles in enhancing drought tolerance, such as HSPs and crucial TFs. Our results provide new insights into the transcriptional responses in root-nodules, an underexplored tissue of plants mainly under drought conditions. This research paves the way for potential improvements in plant-bacteria interactions, contributing to common bean adaptations in the face of challenging environmental conditions.
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spelling doaj.art-7dbdc44e057e41d1bdc4f460727377932024-01-26T04:44:57ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2024-01-011510.3389/fpls.2024.13453791345379Unraveling the drought-responsive transcriptomes in nodules of two common bean genotypes during biological nitrogen fixationHelder Anderson Pinto da Silva0Vanessa Santana Caetano1Daniella Duarte Villarinho Pessôa2Rafael Sanches Pacheco3Carlos Henrique S. G. Meneses4Jean Luiz Simões-Araújo5Jean Luiz Simões-Araújo6Jean Luiz Simões-Araújo7Programa de Pós-Graduação em Biotecnologia Vegetal, Centro de Ciências da Saúde (CCS), Universidade Federal do Rio de Janeiro (UFRJ), Rio de Janeiro, BrazilPrograma de Pós-Graduação em Biotecnologia Vegetal, Centro de Ciências da Saúde (CCS), Universidade Federal do Rio de Janeiro (UFRJ), Rio de Janeiro, BrazilPrograma de Pós-Graduação em Biotecnologia Vegetal, Centro de Ciências da Saúde (CCS), Universidade Federal do Rio de Janeiro (UFRJ), Rio de Janeiro, BrazilPrograma de Pós-graduação em Fitossanidade e Biotecnologia Aplicada, Universidade Federal Rural do Rio de Janeiro (UFRRJ), Seropédica, RJ, BrazilDepartamento de Biologia, Centro de Ciências Biológicas e da Saúde, Universidade Estadual da Paraíba, Campina Grande, BrazilPrograma de Pós-Graduação em Biotecnologia Vegetal, Centro de Ciências da Saúde (CCS), Universidade Federal do Rio de Janeiro (UFRJ), Rio de Janeiro, BrazilPrograma de Pós-graduação em Fitossanidade e Biotecnologia Aplicada, Universidade Federal Rural do Rio de Janeiro (UFRRJ), Seropédica, RJ, BrazilCentro Nacional de Pesquisa de Agrobiologia, CNPAB – Embrapa, Laboratório de Genética e Bioquímica, Seropédica, RJ, BrazilCommon bean (Phaseolus vulgaris) can efficiently fix atmospheric nitrogen when associated with Rhizobia. However, drought stress impairs plant metabolic processes, especially the biological nitrogen fixation (BNF). Here, we assessed transcriptional responses in nodules of two common bean genotypes to drought stress under BNF reliance. The RNA-Seq analysis yielded a total of 81,489,262 and 72,497,478 high quality reads for Negro Argel and BAT 477 genotypes, respectively. The reads were mapped to the Phaseolus vulgaris reference genome and expression analysis identified 145 and 1451 differentially expressed genes (DEGs) for Negro Argel and BAT 477 genotypes, respectively. Although BAT 477 had more DEGs, both genotypes shared certain drought-responsive genes, including an up-regulated heat shock protein (HSP) and a down-regulated peroxidase, indicating shared pathways activated during drought in nodule tissue. Functional analysis using MapMan software highlighted the up-regulation of genes involved in abiotic stress responses, such as HSPs and specific transcription factors (TFs), in both genotypes. There was a significant down-regulation in metabolic pathways related to antioxidant protection, hormone signaling, metabolism, and transcriptional regulation. To validate these findings, we conducted RT-qPCR experiments for ten DEGs in nodules from both genotypes, for which the expression profile was confirmed, thus reinforcing their functional relevance in the nodule responses to drought stress during BNF. BAT 477 genotype exhibited more pronounced response to drought, characterized by a high number of DEGs. The strong down-regulation of DEGs leads to transcriptional disturbances in several pathways related to stress acclimation such as hormone and antioxidant metabolism. Additionally, we identified several genes that are known to play key roles in enhancing drought tolerance, such as HSPs and crucial TFs. Our results provide new insights into the transcriptional responses in root-nodules, an underexplored tissue of plants mainly under drought conditions. This research paves the way for potential improvements in plant-bacteria interactions, contributing to common bean adaptations in the face of challenging environmental conditions.https://www.frontiersin.org/articles/10.3389/fpls.2024.1345379/fullsymbiotic nitrogen assimilationwater deficitgenetic transcript profileRT-qPCRcandidate genes
spellingShingle Helder Anderson Pinto da Silva
Vanessa Santana Caetano
Daniella Duarte Villarinho Pessôa
Rafael Sanches Pacheco
Carlos Henrique S. G. Meneses
Jean Luiz Simões-Araújo
Jean Luiz Simões-Araújo
Jean Luiz Simões-Araújo
Unraveling the drought-responsive transcriptomes in nodules of two common bean genotypes during biological nitrogen fixation
Frontiers in Plant Science
symbiotic nitrogen assimilation
water deficit
genetic transcript profile
RT-qPCR
candidate genes
title Unraveling the drought-responsive transcriptomes in nodules of two common bean genotypes during biological nitrogen fixation
title_full Unraveling the drought-responsive transcriptomes in nodules of two common bean genotypes during biological nitrogen fixation
title_fullStr Unraveling the drought-responsive transcriptomes in nodules of two common bean genotypes during biological nitrogen fixation
title_full_unstemmed Unraveling the drought-responsive transcriptomes in nodules of two common bean genotypes during biological nitrogen fixation
title_short Unraveling the drought-responsive transcriptomes in nodules of two common bean genotypes during biological nitrogen fixation
title_sort unraveling the drought responsive transcriptomes in nodules of two common bean genotypes during biological nitrogen fixation
topic symbiotic nitrogen assimilation
water deficit
genetic transcript profile
RT-qPCR
candidate genes
url https://www.frontiersin.org/articles/10.3389/fpls.2024.1345379/full
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