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      Plant beneficial microbiome a boon for improving multiple stress tolerance in plants

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          Abstract

          Beneficial microbes or their products have been key drivers for improving adaptive and growth features in plants under biotic and abiotic stress conditions. However, the majority of these studies so far have been utilized against individual stressors. In comparison to individual stressors, the combination of many environmental stresses that plants experience has a greater detrimental effect on them and poses a threat to their existence. Therefore, there is a need to explore the beneficial microbiota against combined stressors or multiple stressors, as this will offer new possibilities for improving plant growth and multiple adaptive traits. However, recognition of the multifaceted core beneficial microbiota from plant microbiome under stress combinations will require a thorough understanding of the functional and mechanistic facets of plant microbiome interactions under different environmental conditions in addition to agronomic management practices. Also, the development of tailored beneficial multiple stress tolerant microbiota in sustainable agriculture necessitates new model systems and prioritizes agricultural microbiome research. In this review, we provided an update on the effect of combined stressors on plants and their microbiome structure. Next, we discussed the role of beneficial microbes in plant growth promotion and stress adaptation. We also discussed how plant-beneficial microbes can be utilized for mitigating multiple stresses in plants. Finally, we have highlighted some key points that warrant future investigation for exploring plant microbiome interactions under multiple stressors.

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          Most cited references76

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          Structure, variation, and assembly of the root-associated microbiomes of rice.

          Plants depend upon beneficial interactions between roots and microbes for nutrient availability, growth promotion, and disease suppression. High-throughput sequencing approaches have provided recent insights into root microbiomes, but our current understanding is still limited relative to animal microbiomes. Here we present a detailed characterization of the root-associated microbiomes of the crop plant rice by deep sequencing, using plants grown under controlled conditions as well as field cultivation at multiple sites. The spatial resolution of the study distinguished three root-associated compartments, the endosphere (root interior), rhizoplane (root surface), and rhizosphere (soil close to the root surface), each of which was found to harbor a distinct microbiome. Under controlled greenhouse conditions, microbiome composition varied with soil source and genotype. In field conditions, geographical location and cultivation practice, namely organic vs. conventional, were factors contributing to microbiome variation. Rice cultivation is a major source of global methane emissions, and methanogenic archaea could be detected in all spatial compartments of field-grown rice. The depth and scale of this study were used to build coabundance networks that revealed potential microbial consortia, some of which were involved in methane cycling. Dynamic changes observed during microbiome acquisition, as well as steady-state compositions of spatial compartments, support a multistep model for root microbiome assembly from soil wherein the rhizoplane plays a selective gating role. Similarities in the distribution of phyla in the root microbiomes of rice and other plants suggest that conclusions derived from this study might be generally applicable to land plants.
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            Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota.

            The plant root defines the interface between a multicellular eukaryote and soil, one of the richest microbial ecosystems on Earth. Notably, soil bacteria are able to multiply inside roots as benign endophytes and modulate plant growth and development, with implications ranging from enhanced crop productivity to phytoremediation. Endophytic colonization represents an apparent paradox of plant innate immunity because plant cells can detect an array of microbe-associated molecular patterns (also known as MAMPs) to initiate immune responses to terminate microbial multiplication. Several studies attempted to describe the structure of bacterial root endophytes; however, different sampling protocols and low-resolution profiling methods make it difficult to infer general principles. Here we describe methodology to characterize and compare soil- and root-inhabiting bacterial communities, which reveals not only a function for metabolically active plant cells but also for inert cell-wall features in the selection of soil bacteria for host colonization. We show that the roots of Arabidopsis thaliana, grown in different natural soils under controlled environmental conditions, are preferentially colonized by Proteobacteria, Bacteroidetes and Actinobacteria, and each bacterial phylum is represented by a dominating class or family. Soil type defines the composition of root-inhabiting bacterial communities and host genotype determines their ribotype profiles to a limited extent. The identification of soil-type-specific members within the root-inhabiting assemblies supports our conclusion that these represent soil-derived root endophytes. Surprisingly, plant cell-wall features of other tested plant species seem to provide a sufficient cue for the assembly of approximately 40% of the Arabidopsis bacterial root-inhabiting microbiota, with a bias for Betaproteobacteria. Thus, this root sub-community may not be Arabidopsis-specific but saprophytic bacteria that would naturally be found on any plant root or plant debris in the tested soils. By contrast, colonization of Arabidopsis roots by members of the Actinobacteria depends on other cues from metabolically active host cells.
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              Abiotic and biotic stress combinations.

              Environmental stress conditions such as drought, heat, salinity, cold, or pathogen infection can have a devastating impact on plant growth and yield under field conditions. Nevertheless, the effects of these stresses on plants are typically being studied under controlled growth conditions in the laboratory. The field environment is very different from the controlled conditions used in laboratory studies, and often involves the simultaneous exposure of plants to more than one abiotic and/or biotic stress condition, such as a combination of drought and heat, drought and cold, salinity and heat, or any of the major abiotic stresses combined with pathogen infection. Recent studies have revealed that the response of plants to combinations of two or more stress conditions is unique and cannot be directly extrapolated from the response of plants to each of the different stresses applied individually. Moreover, the simultaneous occurrence of different stresses results in a high degree of complexity in plant responses, as the responses to the combined stresses are largely controlled by different, and sometimes opposing, signaling pathways that may interact and inhibit each other. In this review, we will provide an update on recent studies focusing on the response of plants to a combination of different stresses. In particular, we will address how different stress responses are integrated and how they impact plant growth and physiological traits. © 2014 The Authors. New Phytologist © 2014 New Phytologist Trust.
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                Author and article information

                Contributors
                URI : https://loop.frontiersin.org/people/1453906Role: Role: Role: Role: Role: Role: Role:
                URI : https://loop.frontiersin.org/people/368605Role: Role: Role: Role: Role:
                URI : https://loop.frontiersin.org/people/1585212Role: Role:
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                URI : https://loop.frontiersin.org/people/2341363Role: Role:
                URI : https://loop.frontiersin.org/people/1620363Role: Role: Role: Role:
                Journal
                Front Plant Sci
                Front Plant Sci
                Front. Plant Sci.
                Frontiers in Plant Science
                Frontiers Media S.A.
                1664-462X
                11 September 2023
                2023
                : 14
                : 1266182
                Affiliations
                [1] 1 Department of Biotechnology, Yeungnam University , Gyeongsan, Gyeongbuk, Republic of Korea
                [2] 2 Department of Biotechnology, Central University of Kashmir , Ganderbal, India
                [3] 3 Department of Biological Sciences, Faculty of Science, King Abdulaziz University (KAU) , Jeddah, Saudi Arabia
                [4] 4 Directorate of Programs, International Center for Biosaline Agriculture , Dubai, United Arab Emirates
                Author notes

                Edited by: Kanika Khanna, Guru Nanak Dev University, India

                Reviewed by: Javaid Akhter Bhat, Nanjing Agricultural University, China; Muhammad Shoib Nawaz, Clemson University, United States; Tariq Shah, North Carolina State University, United States

                *Correspondence: Sajad Ali, sajadmicro@ 123456yu.ac.kr ; Irfan A. Rather, ammm@ 123456kau.edu.sa ; Henda Mahmoudi, HMJ@ 123456biosaline.org.ae

                †These authors have contributed equally to this work

                Article
                10.3389/fpls.2023.1266182
                10520250
                37767298
                ccc37522-47c2-4a25-8ffd-6368086a027f
                Copyright © 2023 Ali, Tyagi, Mir, Rather, Anwar and Mahmoudi

                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.

                History
                : 24 July 2023
                : 28 August 2023
                Page count
                Figures: 2, Tables: 1, Equations: 0, References: 76, Pages: 9, Words: 3766
                Funding
                This research work was funded by Institutional Fund Projects, under grant number (IFPRP:119-130-1442). Therefore, authors gratefully acknowledge technical and financial support from the Ministry of Education and King Abdulaziz University, DSR, Jeddah, Saudi Arabia.
                Categories
                Plant Science
                Mini Review
                Custom metadata
                Plant Symbiotic Interactions

                Plant science & Botany
                beneficial microbes,abiotic stressors,combined stress,climate change,tailored microbiota

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