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      Biological nitrogen fixation in cereal crops: Progress, strategies, and perspectives

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          Abstract

          Nitrogen is abundant in the atmosphere but is generally the most limiting nutrient for plants. The inability of many crop plants, such as cereals, to directly utilize freely available atmospheric nitrogen gas means that their growth and production often rely heavily on the application of chemical fertilizers, which leads to greenhouse gas emissions and the eutrophication of water. By contrast, legumes gain access to nitrogen through symbiotic association with rhizobia. These bacteria convert nitrogen gas into biologically available ammonia in nodules through a process termed symbiotic biological nitrogen fixation, which plays a decisive role in ecosystem functioning. Engineering cereal crops that can fix nitrogen like legumes or associate with nitrogen-fixing microbiomes could help to avoid the problems caused by the overuse of synthetic nitrogen fertilizer. With the development of synthetic biology, various efforts have been undertaken with the aim of creating so-called “N-self-fertilizing” crops capable of performing autonomous nitrogen fixation to avoid the need for chemical fertilizers. In this review, we briefly summarize the history and current status of engineering N-self-fertilizing crops. We also propose several potential biotechnological approaches for incorporating biological nitrogen fixation capacity into non-legume plants.

          Abstract

          Legumes can gain access to nitrogen through symbiotic association with rhizobia, whereas the growth and production of cereal crops often rely heavily on the application of chemical fertilizers. Engineering cereal crops that can fix nitrogen autonomously or that associate with nitrogen-fixing bacteria through a synthetic biology approach would reduce the use of synthetic nitrogen fertilizers. This review summarizes the history and current status of engineering biological nitrogen fixation in cereal plants.

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          Most cited references120

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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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            The SHORT-ROOT gene controls radial patterning of the Arabidopsis root through radial signaling.

            Asymmetric cell divisions play an important role in the establishment and propagation of the cellular pattern of plant tissues. The SHORT-ROOT (SHR) gene is required for the asymmetric cell division responsible for formation of ground tissue (endodermis and cortex) as well as specification of endodermis in the Arabidopsis root. We show that SHR encodes a putative transcription factor with homology to SCARECROW (SCR). From analyses of gene expression and cell identity in genetically stable and unstable alleles of shr, we conclude that SHR functions upstream of SCR and participates in a radial signaling pathway. Consistent with a regulatory role in radial patterning, ectopic expression of SHR results in supernumerary cell divisions and abnormal cell specification in the root meristem.
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              The SCARECROW gene regulates an asymmetric cell division that is essential for generating the radial organization of the Arabidopsis root.

              In the Arabidopsis root meristem, initial cells undergo asymmetric divisions to generate the cell lineages of the root. The scarecrow mutation results in roots that are missing one cell layer owing to the disruption of an asymmetric division that normally generates cortex and endodermis. Tissue-specific markers indicate that a heterogeneous cell type is formed in the mutant. The deduced amino acid sequence of SCARECROW (SCR) suggests that it is a member of a novel family of putative transcription factors. SCR is expressed in the cortex/endodermal initial cells and in the endodermal cell lineage. Tissue-specific expression is regulated at the transcriptional level. These results indicate a key role for SCR in regulating the radial organization of the root.
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                Author and article information

                Contributors
                Journal
                Plant Commun
                Plant Commun
                Plant Communications
                Elsevier
                2590-3462
                28 November 2022
                13 March 2023
                28 November 2022
                : 4
                : 2
                : 100499
                Affiliations
                [1 ]Shanghai Key Laboratory of Plant Molecular Sciences, College of Life Sciences, Shanghai Normal University, Shanghai 200234, China
                [2 ]National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai 200032, China
                [3 ]School of Life Sciences, Shanghai Key Laboratory of Bioenergy Crops, Shanghai University, Shanghai 200444, China
                Author notes
                []Corresponding author nyu@ 123456shnu.edu.cn
                [∗∗ ]Corresponding author liluo@ 123456shu.edu.cn
                [∗∗∗ ]Corresponding author etwang@ 123456cemps.ac.cn
                [4]

                These authors contributed equally to this article.

                Article
                S2590-3462(22)00346-7 100499
                10.1016/j.xplc.2022.100499
                10030364
                36447432
                341fd1e1-6789-432a-969d-8f330d15b7b0
                © 2022 The Author(s)

                This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

                History
                : 9 September 2022
                : 7 November 2022
                : 28 November 2022
                Categories
                Review Article

                biological nitrogen fixation,cereal plants,self-fertilizing crops,microbiome

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