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      The Impacts of Domestication and Breeding on Nitrogen Fixation Symbiosis in Legumes

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          Abstract

          Legumes are the second most important family of crop plants. One defining feature of legumes is their unique ability to establish a nitrogen-fixing root nodule symbiosis with soil bacteria known as rhizobia. Since domestication from their wild relatives, crop legumes have been under intensive breeding to improve yield and other agronomic traits but with little attention paid to the belowground symbiosis traits. Theoretical models predict that domestication and breeding processes, coupled with high−input agricultural practices, might have reduced the capacity of crop legumes to achieve their full potential of nitrogen fixation symbiosis. Testing this prediction requires characterizing symbiosis traits in wild and breeding populations under both natural and cultivated environments using genetic, genomic, and ecological approaches. However, very few experimental studies have been dedicated to this area of research. Here, we review how legumes regulate their interactions with soil rhizobia and how domestication, breeding and agricultural practices might have affected nodulation capacity, nitrogen fixation efficiency, and the composition and function of rhizobial community. We also provide a perspective on how to improve legume-rhizobial symbiosis in sustainable agricultural systems.

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          Most cited references54

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          Microbiota and Host Nutrition across Plant and Animal Kingdoms.

          Plants and animals each have evolved specialized organs dedicated to nutrient acquisition, and these harbor specific bacterial communities that extend the host's metabolic repertoire. Similar forces driving microbial community establishment in the gut and plant roots include diet/soil-type, host genotype, and immune system as well as microbe-microbe interactions. Here we show that there is no overlap of abundant bacterial taxa between the microbiotas of the mammalian gut and plant roots, whereas taxa overlap does exist between fish gut and plant root communities. A comparison of root and gut microbiota composition in multiple host species belonging to the same evolutionary lineage reveals host phylogenetic signals in both eukaryotic kingdoms. The reasons underlying striking differences in microbiota composition in independently evolved, yet functionally related, organs in plants and animals remain unclear but might include differences in start inoculum and niche-specific factors such as oxygen levels, temperature, pH, and organic carbon availability.
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            Rhizobia: from saprophytes to endosymbionts

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              Receptor-mediated exopolysaccharide perception controls bacterial infection.

              Surface polysaccharides are important for bacterial interactions with multicellular organisms, and some are virulence factors in pathogens. In the legume-rhizobium symbiosis, bacterial exopolysaccharides (EPS) are essential for the development of infected root nodules. We have identified a gene in Lotus japonicus, Epr3, encoding a receptor-like kinase that controls this infection. We show that epr3 mutants are defective in perception of purified EPS, and that EPR3 binds EPS directly and distinguishes compatible and incompatible EPS in bacterial competition studies. Expression of Epr3 in epidermal cells within the susceptible root zone shows that the protein is involved in bacterial entry, while rhizobial and plant mutant studies suggest that Epr3 regulates bacterial passage through the plant's epidermal cell layer. Finally, we show that Epr3 expression is inducible and dependent on host perception of bacterial nodulation (Nod) factors. Plant-bacterial compatibility and bacterial access to legume roots is thus regulated by a two-stage mechanism involving sequential receptor-mediated recognition of Nod factor and EPS signals.
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                Author and article information

                Contributors
                Journal
                Front Genet
                Front Genet
                Front. Genet.
                Frontiers in Genetics
                Frontiers Media S.A.
                1664-8021
                18 August 2020
                2020
                : 11
                : 00973
                Affiliations
                [1] 1Department of Plant and Soil Sciences, University of Kentucky , Lexington, KY, United States
                [2] 2Forage-Animal Production Research Unit, United States Department of Agriculture-Agricultural Research Service , Lexington, KY, United States
                Author notes

                Edited by: Gaofeng Zhou, Department of Primary Industries and Regional Development (DPIRD), Australia

                Reviewed by: Alessio Mengoni, University of Florence, Italy; Maria Eugenia Zanetti, National University of La Plata, Argentina; Hon-Ming Lam, The Chinese University of Hong Kong, China

                *Correspondence: Hongyan Zhu, hzhu4@ 123456uky.edu

                These authors have contributed equally to this work

                This article was submitted to Evolutionary and Population Genetics, a section of the journal Frontiers in Genetics

                Article
                10.3389/fgene.2020.00973
                7461779
                33014021
                818d970f-d168-46c6-b061-e45b795e268c
                Copyright © 2020 Liu, Yu, Qin, Dinkins and Zhu.

                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
                : 01 June 2020
                : 31 July 2020
                Page count
                Figures: 1, Tables: 1, Equations: 0, References: 68, Pages: 9, Words: 0
                Funding
                Funded by: National Science Foundation 10.13039/100000001
                Funded by: U.S. Department of Agriculture 10.13039/100000199
                Categories
                Genetics
                Mini Review

                Genetics
                legume,nodulation,nitrogen fixation,symbiosis,domestication,rhizobia
                Genetics
                legume, nodulation, nitrogen fixation, symbiosis, domestication, rhizobia

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