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Deciphering the Role of Trehalose in Tripartite Symbiosis Among Rhizobia, Arbuscular Mycorrhizal Fungi, and Legumes for Enhancing Abiotic Stress Tolerance in Crop Plants

Drought is a critical factor limiting the productivity of legumes worldwide. Legumes can enter into a unique tripartite symbiotic relationship with root-nodulating bacteria of genera Rhizobium, Bradyrhizobium, or Sinorhizobium and colonization by arbuscular mycorrhizal fungi (AMF). Rhizobial symbios...

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Autores principales: Sharma, Mahaveer P., Grover, Minakshi, Chourasiya, Dipanti, Bharti, Abhishek, Agnihotri, Richa, Maheshwari, Hemant S., Pareek, Ashwani, Buyer, Jeffrey S., Sharma, Sushil K., Schütz, Lukas, Mathimaran, Natarajan, Singla-Pareek, Sneh L., Grossman, Julie M., Bagyaraj, Davis J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7527417/
https://www.ncbi.nlm.nih.gov/pubmed/33042042
http://dx.doi.org/10.3389/fmicb.2020.509919
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author Sharma, Mahaveer P.
Grover, Minakshi
Chourasiya, Dipanti
Bharti, Abhishek
Agnihotri, Richa
Maheshwari, Hemant S.
Pareek, Ashwani
Buyer, Jeffrey S.
Sharma, Sushil K.
Schütz, Lukas
Mathimaran, Natarajan
Singla-Pareek, Sneh L.
Grossman, Julie M.
Bagyaraj, Davis J.
author_facet Sharma, Mahaveer P.
Grover, Minakshi
Chourasiya, Dipanti
Bharti, Abhishek
Agnihotri, Richa
Maheshwari, Hemant S.
Pareek, Ashwani
Buyer, Jeffrey S.
Sharma, Sushil K.
Schütz, Lukas
Mathimaran, Natarajan
Singla-Pareek, Sneh L.
Grossman, Julie M.
Bagyaraj, Davis J.
author_sort Sharma, Mahaveer P.
collection PubMed
description Drought is a critical factor limiting the productivity of legumes worldwide. Legumes can enter into a unique tripartite symbiotic relationship with root-nodulating bacteria of genera Rhizobium, Bradyrhizobium, or Sinorhizobium and colonization by arbuscular mycorrhizal fungi (AMF). Rhizobial symbiosis provides nitrogen necessary for growth. AMF symbiosis enhances uptake of diffusion-limited nutrients such as P, Zn, Cu, etc., and also water from the soil via plant-associated fungal hyphae. Rhizobial and AMF symbioses can act synergistically in promoting plant growth and fitness, resulting in overall yield benefits under drought stress. One of the approaches that rhizobia use to survive under stress is the accumulation of compatible solutes, or osmolytes, such as trehalose. Trehalose is a non-reducing disaccharide and an osmolyte reported to accumulate in a range of organisms. High accumulation of trehalose in bacteroids during nodulation protects cells and proteins from osmotic shock, desiccation, and heat under drought stress. Manipulation of trehalose cell concentrations has been directly correlated with stress response in plants and other organisms, including AMF. However, the role of this compound in the tripartite symbiotic relationship is not fully explored. This review describes the biological importance and the role of trehalose in the tripartite symbiosis between plants, rhizobia, and AMF. In particular, we review the physiological functions and the molecular investigations of trehalose carried out using omics-based approaches. This review will pave the way for future studies investigating possible metabolic engineering of this biomolecule for enhancing abiotic stress tolerance in plants.
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spelling pubmed-75274172020-10-09 Deciphering the Role of Trehalose in Tripartite Symbiosis Among Rhizobia, Arbuscular Mycorrhizal Fungi, and Legumes for Enhancing Abiotic Stress Tolerance in Crop Plants Sharma, Mahaveer P. Grover, Minakshi Chourasiya, Dipanti Bharti, Abhishek Agnihotri, Richa Maheshwari, Hemant S. Pareek, Ashwani Buyer, Jeffrey S. Sharma, Sushil K. Schütz, Lukas Mathimaran, Natarajan Singla-Pareek, Sneh L. Grossman, Julie M. Bagyaraj, Davis J. Front Microbiol Microbiology Drought is a critical factor limiting the productivity of legumes worldwide. Legumes can enter into a unique tripartite symbiotic relationship with root-nodulating bacteria of genera Rhizobium, Bradyrhizobium, or Sinorhizobium and colonization by arbuscular mycorrhizal fungi (AMF). Rhizobial symbiosis provides nitrogen necessary for growth. AMF symbiosis enhances uptake of diffusion-limited nutrients such as P, Zn, Cu, etc., and also water from the soil via plant-associated fungal hyphae. Rhizobial and AMF symbioses can act synergistically in promoting plant growth and fitness, resulting in overall yield benefits under drought stress. One of the approaches that rhizobia use to survive under stress is the accumulation of compatible solutes, or osmolytes, such as trehalose. Trehalose is a non-reducing disaccharide and an osmolyte reported to accumulate in a range of organisms. High accumulation of trehalose in bacteroids during nodulation protects cells and proteins from osmotic shock, desiccation, and heat under drought stress. Manipulation of trehalose cell concentrations has been directly correlated with stress response in plants and other organisms, including AMF. However, the role of this compound in the tripartite symbiotic relationship is not fully explored. This review describes the biological importance and the role of trehalose in the tripartite symbiosis between plants, rhizobia, and AMF. In particular, we review the physiological functions and the molecular investigations of trehalose carried out using omics-based approaches. This review will pave the way for future studies investigating possible metabolic engineering of this biomolecule for enhancing abiotic stress tolerance in plants. Frontiers Media S.A. 2020-09-17 /pmc/articles/PMC7527417/ /pubmed/33042042 http://dx.doi.org/10.3389/fmicb.2020.509919 Text en Copyright © 2020 Sharma, Grover, Chourasiya, Bharti, Agnihotri, Maheshwari, Pareek, Buyer, Sharma, Schütz, Mathimaran, Singla-Pareek, Grossman and Bagyaraj. http://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 Microbiology
Sharma, Mahaveer P.
Grover, Minakshi
Chourasiya, Dipanti
Bharti, Abhishek
Agnihotri, Richa
Maheshwari, Hemant S.
Pareek, Ashwani
Buyer, Jeffrey S.
Sharma, Sushil K.
Schütz, Lukas
Mathimaran, Natarajan
Singla-Pareek, Sneh L.
Grossman, Julie M.
Bagyaraj, Davis J.
Deciphering the Role of Trehalose in Tripartite Symbiosis Among Rhizobia, Arbuscular Mycorrhizal Fungi, and Legumes for Enhancing Abiotic Stress Tolerance in Crop Plants
title Deciphering the Role of Trehalose in Tripartite Symbiosis Among Rhizobia, Arbuscular Mycorrhizal Fungi, and Legumes for Enhancing Abiotic Stress Tolerance in Crop Plants
title_full Deciphering the Role of Trehalose in Tripartite Symbiosis Among Rhizobia, Arbuscular Mycorrhizal Fungi, and Legumes for Enhancing Abiotic Stress Tolerance in Crop Plants
title_fullStr Deciphering the Role of Trehalose in Tripartite Symbiosis Among Rhizobia, Arbuscular Mycorrhizal Fungi, and Legumes for Enhancing Abiotic Stress Tolerance in Crop Plants
title_full_unstemmed Deciphering the Role of Trehalose in Tripartite Symbiosis Among Rhizobia, Arbuscular Mycorrhizal Fungi, and Legumes for Enhancing Abiotic Stress Tolerance in Crop Plants
title_short Deciphering the Role of Trehalose in Tripartite Symbiosis Among Rhizobia, Arbuscular Mycorrhizal Fungi, and Legumes for Enhancing Abiotic Stress Tolerance in Crop Plants
title_sort deciphering the role of trehalose in tripartite symbiosis among rhizobia, arbuscular mycorrhizal fungi, and legumes for enhancing abiotic stress tolerance in crop plants
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7527417/
https://www.ncbi.nlm.nih.gov/pubmed/33042042
http://dx.doi.org/10.3389/fmicb.2020.509919
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