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      Interkingdom multi-omics analysis reveals the effects of nitrogen application on growth and rhizosphere microbial community of Tartary buckwheat

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          Abstract

          Tartary buckwheat ( Fagopyrum tataricum Gaertn.) is an important pseudocereal crop with excellent edible, nutritional and medicinal values. However, the yield of Tartary buckwheat (TB) is very low due to old-fashioned cultivation techniques, particularly unreasonable application of nitrogen fertilizer. To improve the understanding on the theories of nitrogen use in TB, the effects of nitrogen application on growth, as well as chemical properties and microbial community of rhizosphere soil were investigated in this study. Nitrogen application could promote the plant height, stem diameter, nitrogen accumulation and yield of TB. The relative abundance and diversity of bacteria and fungi in the rhizosphere soil of TB were improved by nitrogen fertilizer. Nitrogen application increased the abundance of beneficial bacteria such as Lysobacter and Sphingomonas in rhizosphere soil, and decreased the abundance of pathogenic fungi such as Fusarium and Plectosphaerella. The results indicated that nitrogen application changed the distribution of microbial communities in TB rhizosphere soil. Furthermore, the specific enriched or depleted microorganisms in the rhizosphere soil of four TB varieties were analyzed at OTU level. 87 specific nitrogen-responsive genes with sequence variation were identified in four varieties by integrating genomic re-sequencing and transcriptome analysis, and these genes may involve in the recruitment of specific rhizosphere microorganisms in different TB varieties. This study provided new insights into the effects of nitrogen application on TB growth and rhizosphere microbial community, and improved the understanding on the mechanisms of TB root–microbe interactions.

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          Most cited references64

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          Plant–microbiome interactions: from community assembly to plant health

          Healthy plants host diverse but taxonomically structured communities of microorganisms, the plant microbiota, that colonize every accessible plant tissue. Plant-associated microbiomes confer fitness advantages to the plant host, including growth promotion, nutrient uptake, stress tolerance and resistance to pathogens. In this Review, we explore how plant microbiome research has unravelled the complex network of genetic, biochemical, physical and metabolic interactions among the plant, the associated microbial communities and the environment. We also discuss how those interactions shape the assembly of plant-associated microbiomes and modulate their beneficial traits, such as nutrient acquisition and plant health, in addition to highlighting knowledge gaps and future directions.
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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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              Nramp5 is a major transporter responsible for manganese and cadmium uptake in rice.

              Paddy rice (Oryza sativa) is able to accumulate high concentrations of Mn without showing toxicity; however, the molecular mechanisms underlying Mn uptake are unknown. Here, we report that a member of the Nramp (for the Natural Resistance-Associated Macrophage Protein) family, Nramp5, is involved in Mn uptake and subsequently the accumulation of high concentrations of Mn in rice. Nramp5 was constitutively expressed in the roots and encodes a plasma membrane-localized protein. Nramp5 was polarly localized at the distal side of both exodermis and endodermis cells. Knockout of Nramp5 resulted in a significant reduction in growth and grain yield, especially when grown at low Mn concentrations. This growth reduction could be partially rescued by supplying high concentrations of Mn but not by the addition of Fe. Mineral analysis showed that the concentration of Mn and Cd in both the roots and shoots was lower in the knockout line than in wild-type rice. A short-term uptake experiment revealed that the knockout line lost the ability to take up Mn and Cd. Taken together, Nramp5 is a major transporter of Mn and Cd and is responsible for the transport of Mn and Cd from the external solution to root cells.
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                Author and article information

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                14 September 2023
                2023
                : 14
                : 1240029
                Affiliations
                [1] 1Key Laboratory of Coarse Cereal Processing, Ministry of Agriculture and Rural Affairs, Sichuan Engineering and Technology Research Center of Coarse Cereal Industralization, Chengdu University , Chengdu, China
                [2] 2School of Food and Biological Engineering, Chengdu University , Chengdu, China
                [3] 3Guizhou Academy of Tobacco Science , Guiyang, China
                Author notes

                Edited by: Francisca Suárez-Estrella, University of Almería, Spain

                Reviewed by: Volker Siegfried Brozel, South Dakota State University, United States; Fenghua Wang, Chinese Academy of Sciences (CAS), China

                *Correspondence: Changying Liu, lcyswu@ 123456163.com
                Article
                10.3389/fmicb.2023.1240029
                10536138
                37779724
                e08e8aad-30e1-4d50-b1ad-7c1f3842ee81
                Copyright © 2023 Qiu, Xiang, Li, Wang, Wan, Wu, Ye, Jiang, Fan, Liu, Liu, Li and Liu.

                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
                : 14 June 2023
                : 31 August 2023
                Page count
                Figures: 7, Tables: 0, Equations: 0, References: 64, Pages: 14, Words: 9615
                Funding
                This research was supported by the Sichuan Science and Technology Program (Nos. 2022NSFSC1706, 2022NSFSC1725, 2022NSFSC1773, 2022YFQ0041, and 2023NSFSC0214), the China Agriculture Research System (No. CARS-07-B-1), the Science and Technology Project of Guizhou Branch of China Tobacco Corporation (Nos. 2021XM18 and 2023XM08), and the Science and Technology Project of China Tobacco Corporation (No. 110202202015).
                Categories
                Microbiology
                Original Research
                Custom metadata
                Microbe and Virus Interactions with Plants

                Microbiology & Virology
                tartary buckwheat,nitrogen,rhizosphere bacteria,rhizosphere fungi,interkingdom multi-omics

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