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      Functionally-explicit sampling can answer key questions about the specificity of plant–microbe interactions

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          Abstract

          The rhizosphere is a nexus for plant–microbe interactions and, as a host-structured environment, a location of high activity for distinct microbes and plant species. Although our insights into this habitat have exploded in recent years, we are still limited in our ability to answer key questions about the specificity of these root-microbial relationships. In particular, it can be difficult to confirm or reject microbiome heritability in many plant systems and to pinpoint which microbial taxa are key to plant functioning. Like other host-structured environments, the rhizosphere is structurally, chemically, and biologically complex, driven largely by differences in root anatomy, location, and function. In this Correspondence, we describe a review of 377 “rhizosphere microbiome” research papers and demonstrate how matching a sampling method to the biological question can advance our understanding of host-microbe interactions in a functionally heterogeneous environment. We found that the vast majority of studies (92%) pool all roots from a root system during sampling, ignoring variation in microbial composition between roots of different function and limiting insight into key root-microbial relationships. Furthermore, approaches for removing root-associated microbes are highly variable and non-standard, complicating multi-study analyses. Our understanding of the strength and nature of host-microbe relationships in heterogenous host-microbiome environments can be clarified by targeting sampling to locations of high interaction. While the high complexity of the rhizosphere creates logistical challenges, we suggest that unambiguous language and refined approaches will improve our ability to match methods to research questions and advance our understanding of the specificity of plant-microbial interactions.

          Supplementary Information

          The online version contains supplementary material available at 10.1186/s40793-022-00445-x.

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          Most cited references36

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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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              Going back to the roots: the microbial ecology of the rhizosphere.

              The rhizosphere is the interface between plant roots and soil where interactions among a myriad of microorganisms and invertebrates affect biogeochemical cycling, plant growth and tolerance to biotic and abiotic stress. The rhizosphere is intriguingly complex and dynamic, and understanding its ecology and evolution is key to enhancing plant productivity and ecosystem functioning. Novel insights into key factors and evolutionary processes shaping the rhizosphere microbiome will greatly benefit from integrating reductionist and systems-based approaches in both agricultural and natural ecosystems. Here, we discuss recent developments in rhizosphere research in relation to assessing the contribution of the micro- and macroflora to sustainable agriculture, nature conservation, the development of bio-energy crops and the mitigation of climate change.
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                Author and article information

                Contributors
                suf44@psu.edu
                dme9@psu.edu
                thb15@psu.edu
                mzc22@psu.edu
                Journal
                Environ Microbiome
                Environ Microbiome
                Environmental Microbiome
                BioMed Central (London )
                2524-6372
                11 October 2022
                11 October 2022
                2022
                : 17
                : 51
                Affiliations
                [1 ]GRID grid.29857.31, ISNI 0000 0001 2097 4281, Department of Plant Science, , The Pennsylvania State University, ; University Park, PA 16802 USA
                [2 ]GRID grid.29857.31, ISNI 0000 0001 2097 4281, Department of Ecosystem Science and Management, , The Pennsylvania State University, ; University Park, PA 16802 USA
                [3 ]GRID grid.29857.31, ISNI 0000 0001 2097 4281, Department of Plant Pathology and Environmental Microbiology, , The Pennsylvania State University, ; University Park, PA 16802 USA
                [4 ]GRID grid.29857.31, ISNI 0000 0001 2097 4281, Graduate Program in Ecology, , The Pennsylvania State University, ; University Park, PA 16802 USA
                Article
                445
                10.1186/s40793-022-00445-x
                9555203
                36221138
                08955705-d16a-4d7f-ad5e-52f7c3b7f7dc
                © The Author(s) 2022

                Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

                History
                : 11 February 2022
                : 26 September 2022
                Funding
                Funded by: National Institute of Food and Agriculture
                Award ID: Accession #1014758
                Award ID: Accession #1014758
                Award ID: Accession #1014758
                Award ID: Accession #1014758
                Award Recipient :
                Categories
                Correspondence
                Custom metadata
                © The Author(s) 2022

                rhizosphere,microbiome,root function,heritability,root traits,specificity,absorptive roots,review

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