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Understanding plant–microbe interaction of rice and soybean with two contrasting diazotrophic bacteria through comparative transcriptome analysis

Understanding the beneficial plant–microbe interactions is becoming extremely critical for deploying microbes imparting plant fitness and achieving sustainability in agriculture. Diazotrophic bacteria have the unique ability to survive without external sources of nitrogen and simultaneously promote...

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Autores principales: Saini, Manish Ranjan, Chandran, Latha P., Barbadikar, Kalyani Makarand, Sevanthi, Amitha Mithra V., Chawla, Gautam, Kaushik, Megha, Mulani, Ekta, Phule, Amol Sarjerao, Govindannagari, Rajani, Sonth, Bandeppa, Sinha, Subodh Kumar, Sundaram, Raman Meenakshi, Mandal, Pranab Kumar
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9724235/
https://www.ncbi.nlm.nih.gov/pubmed/36483966
http://dx.doi.org/10.3389/fpls.2022.939395
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author Saini, Manish Ranjan
Chandran, Latha P.
Barbadikar, Kalyani Makarand
Sevanthi, Amitha Mithra V.
Chawla, Gautam
Kaushik, Megha
Mulani, Ekta
Phule, Amol Sarjerao
Govindannagari, Rajani
Sonth, Bandeppa
Sinha, Subodh Kumar
Sundaram, Raman Meenakshi
Mandal, Pranab Kumar
author_facet Saini, Manish Ranjan
Chandran, Latha P.
Barbadikar, Kalyani Makarand
Sevanthi, Amitha Mithra V.
Chawla, Gautam
Kaushik, Megha
Mulani, Ekta
Phule, Amol Sarjerao
Govindannagari, Rajani
Sonth, Bandeppa
Sinha, Subodh Kumar
Sundaram, Raman Meenakshi
Mandal, Pranab Kumar
author_sort Saini, Manish Ranjan
collection PubMed
description Understanding the beneficial plant–microbe interactions is becoming extremely critical for deploying microbes imparting plant fitness and achieving sustainability in agriculture. Diazotrophic bacteria have the unique ability to survive without external sources of nitrogen and simultaneously promote host plant growth, but the mechanisms of endophytic interaction in cereals and legumes have not been studied extensively. We have studied the early interaction of two diazotrophic bacteria, Gluconacetobacter diazotrophicus (GAB) and Bradyrhizobium japonicum (BRH), in 15-day-old seedlings of rice and soybean up to 120 h after inoculation (hai) under low-nitrogen medium. Root colonization of GAB in rice was higher than that of BRH, and BRH colonization was higher in soybean roots as observed from the scanning electron microscopy at 120 hai. Peroxidase enzyme was significantly higher at 24 hai but thereafter was reduced sharply in soybean and gradually in rice. The roots of rice and soybean inoculated with GAB and BRH harvested from five time points were pooled, and transcriptome analysis was executed along with control. Two pathways, “Plant pathogen interaction” and “MAPK signaling,” were specific to Rice-Gluconacetobacter (RG), whereas the pathways related to nitrogen metabolism and plant hormone signaling were specific to Rice-Bradyrhizobium (RB) in rice. Comparative transcriptome analysis of the root tissues revealed that several plant–diazotroph-specific differentially expressed genes (DEGs) and metabolic pathways of plant–diazotroph-specific transcripts, viz., chitinase, brassinosteroid, auxin, Myeloblastosis (MYB), nodulin, and nitrate transporter (NRT), were common in all plant–diazotroph combinations; three transcripts, viz., nitrate transport accessory protein (NAR), thaumatin, and thionin, were exclusive in rice and another three transcripts, viz., NAC (NAM: no apical meristem, ATAF: Arabidopsis thaliana activating factor, and CUC: cup-shaped cotyledon), ABA (abscisic acid), and ammonium transporter, were exclusive in soybean. Differential expression of these transcripts and reduction in pathogenesis-related (PR) protein expression show the early interaction. Based on the interaction, it can be inferred that the compatibility of rice and soybean is more with GAB and BRH, respectively. We propose that rice is unable to identify the diazotroph as a beneficial microorganism or a pathogen from an early response. So, it expressed the hypersensitivity-related transcripts along with PR proteins. The molecular mechanism of diazotrophic associations of GAB and BRH with rice vis-à-vis soybean will shed light on the basic understanding of host responses to beneficial microorganisms.
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spelling pubmed-97242352022-12-07 Understanding plant–microbe interaction of rice and soybean with two contrasting diazotrophic bacteria through comparative transcriptome analysis Saini, Manish Ranjan Chandran, Latha P. Barbadikar, Kalyani Makarand Sevanthi, Amitha Mithra V. Chawla, Gautam Kaushik, Megha Mulani, Ekta Phule, Amol Sarjerao Govindannagari, Rajani Sonth, Bandeppa Sinha, Subodh Kumar Sundaram, Raman Meenakshi Mandal, Pranab Kumar Front Plant Sci Plant Science Understanding the beneficial plant–microbe interactions is becoming extremely critical for deploying microbes imparting plant fitness and achieving sustainability in agriculture. Diazotrophic bacteria have the unique ability to survive without external sources of nitrogen and simultaneously promote host plant growth, but the mechanisms of endophytic interaction in cereals and legumes have not been studied extensively. We have studied the early interaction of two diazotrophic bacteria, Gluconacetobacter diazotrophicus (GAB) and Bradyrhizobium japonicum (BRH), in 15-day-old seedlings of rice and soybean up to 120 h after inoculation (hai) under low-nitrogen medium. Root colonization of GAB in rice was higher than that of BRH, and BRH colonization was higher in soybean roots as observed from the scanning electron microscopy at 120 hai. Peroxidase enzyme was significantly higher at 24 hai but thereafter was reduced sharply in soybean and gradually in rice. The roots of rice and soybean inoculated with GAB and BRH harvested from five time points were pooled, and transcriptome analysis was executed along with control. Two pathways, “Plant pathogen interaction” and “MAPK signaling,” were specific to Rice-Gluconacetobacter (RG), whereas the pathways related to nitrogen metabolism and plant hormone signaling were specific to Rice-Bradyrhizobium (RB) in rice. Comparative transcriptome analysis of the root tissues revealed that several plant–diazotroph-specific differentially expressed genes (DEGs) and metabolic pathways of plant–diazotroph-specific transcripts, viz., chitinase, brassinosteroid, auxin, Myeloblastosis (MYB), nodulin, and nitrate transporter (NRT), were common in all plant–diazotroph combinations; three transcripts, viz., nitrate transport accessory protein (NAR), thaumatin, and thionin, were exclusive in rice and another three transcripts, viz., NAC (NAM: no apical meristem, ATAF: Arabidopsis thaliana activating factor, and CUC: cup-shaped cotyledon), ABA (abscisic acid), and ammonium transporter, were exclusive in soybean. Differential expression of these transcripts and reduction in pathogenesis-related (PR) protein expression show the early interaction. Based on the interaction, it can be inferred that the compatibility of rice and soybean is more with GAB and BRH, respectively. We propose that rice is unable to identify the diazotroph as a beneficial microorganism or a pathogen from an early response. So, it expressed the hypersensitivity-related transcripts along with PR proteins. The molecular mechanism of diazotrophic associations of GAB and BRH with rice vis-à-vis soybean will shed light on the basic understanding of host responses to beneficial microorganisms. Frontiers Media S.A. 2022-11-18 /pmc/articles/PMC9724235/ /pubmed/36483966 http://dx.doi.org/10.3389/fpls.2022.939395 Text en Copyright © 2022 Saini, Chandran, Barbadikar, Sevanthi, Chawla, Kaushik, Mulani, Phule, Govindannagari, Sonth, Sinha, Sundaram and Mandal https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
Saini, Manish Ranjan
Chandran, Latha P.
Barbadikar, Kalyani Makarand
Sevanthi, Amitha Mithra V.
Chawla, Gautam
Kaushik, Megha
Mulani, Ekta
Phule, Amol Sarjerao
Govindannagari, Rajani
Sonth, Bandeppa
Sinha, Subodh Kumar
Sundaram, Raman Meenakshi
Mandal, Pranab Kumar
Understanding plant–microbe interaction of rice and soybean with two contrasting diazotrophic bacteria through comparative transcriptome analysis
title Understanding plant–microbe interaction of rice and soybean with two contrasting diazotrophic bacteria through comparative transcriptome analysis
title_full Understanding plant–microbe interaction of rice and soybean with two contrasting diazotrophic bacteria through comparative transcriptome analysis
title_fullStr Understanding plant–microbe interaction of rice and soybean with two contrasting diazotrophic bacteria through comparative transcriptome analysis
title_full_unstemmed Understanding plant–microbe interaction of rice and soybean with two contrasting diazotrophic bacteria through comparative transcriptome analysis
title_short Understanding plant–microbe interaction of rice and soybean with two contrasting diazotrophic bacteria through comparative transcriptome analysis
title_sort understanding plant–microbe interaction of rice and soybean with two contrasting diazotrophic bacteria through comparative transcriptome analysis
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9724235/
https://www.ncbi.nlm.nih.gov/pubmed/36483966
http://dx.doi.org/10.3389/fpls.2022.939395
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