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      Plants and Associated Soil Microbiota Cooperatively Suppress Plant-Parasitic Nematodes

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          Abstract

          Disease suppressive soils with specific suppression of soil-borne pathogens and parasites have been long studied and are most often of microbiological origin. As for the plant-parasitic nematodes (PPN), which represent a huge threat to agricultural crops and which successfully defy many conventional control methods, soil progression from conducive to suppressive state is accompanied by the enrichment of specific antagonistic microbial consortia. However, a few microbial groups have come to the fore in diminishing PPN in disease suppressive soils using culture-dependent methods. Studies with cultured strains resulted in understanding the mechanisms by which nematodes are antagonized by microorganisms. Recent culture-independent studies on the microbiome associated with soil, plant roots, and PPN contributed to a better understanding of the functional potential of disease suppressive microbial cohort. Plant root exudation is an important pathway determining host-microbe communication and plays a key role in selection and enrichment of a specific set of microbial antagonists in the rhizosphere as first line of defense against crop pathogens or parasites. Root exudates comprising primary metabolites such as amino acids, sugars, organic acids, and secondary metabolites can also cause modifications in the nematode surface and subsequently affect microbial attachment. A positive interaction between hosts and their beneficial root microbiota is correlated with a low nematode performance on the host. In this review, we first summarized the historical records of nematode-suppressive soils and then focused on more recent studies in this aspect, emphasizing the advances in studying nematode-microbe interactions over time. We highlighted nematode biocontrol mechanisms, especially parasitism, induced systemic resistance, and volatile organic compounds using microbial consortia, or bacterial strains of the genera Pasteuria, Bacillus, Pseudomonas, Rhizobium, Streptomyces, Arthrobacter, and Variovorax, or fungal isolates of Pochonia, Dactylella, Nematophthora, Purpureocillium, Trichoderma, Hirsutella, Arthrobotrys, and Mortierella. We discussed the importance of root exudates in plant communication with PPN and soil microorganisms, emphasizing their role in microbial attachment to the nematode surface and subsequent events of nematode parasitism. Comprehensive understanding of the plant-beneficial microbial consortia and the mechanisms underlying disease suppression may help to develop synthetic microbial communities for biocontrol of PPN, thereby reducing nematicides and fertilizers inputs.

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          Regulation and function of root exudates

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            Microbial diversity in soil: selection microbial populations by plant and soil type and implications for disease suppressiveness.

            An increasing interest has emerged with respect to the importance of microbial diversity in soil habitats. The extent of the diversity of microorganisms in soil is seen to be critical to the maintenance of soil health and quality, as a wide range of microorganisms is involved in important soil functions. This review focuses on recent data relating how plant type, soil type, and soil management regime affect the microbial diversity of soil and the implication for the soil's disease suppressiveness. The two main drivers of soil microbial community structure, i.e., plant type and soil type, are thought to exert their function in a complex manner. We propose that the fact that in some situations the soil and in others the plant type is the key factor determining soil microbial diversity is related to the complexity of the microbial interactions in soil, including interactions between microorganisms and soil and microorganisms and plants. A conceptual framework, based on the relative strengths of the shaping forces exerted by plant and soil versus the ecological behavior of microorganisms, is proposed.
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              The Soil-Borne Legacy

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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
                28 February 2020
                2020
                : 11
                : 313
                Affiliations
                [1] 1Institute for Epidemiology and Pathogen Diagnostics, Julius Kühn-Institut, Federal Research Centre for Cultivated Plants , Braunschweig, Germany
                [2] 2State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences , Chaoyang, China
                Author notes

                Edited by: Dilantha Fernando, University of Manitoba, Canada

                Reviewed by: Zafar Ahmad Handoo, Agricultural Research Service (USDA), United States; Sofia R. Costa, University of Minho, Portugal; Krzysztof Wieczorek, University of Natural Resources and Life Sciences, Vienna, Austria

                *Correspondence: Muzammil Hussain, muzammil0991@ 123456gmail.com

                These authors have contributed equally to this work

                This article was submitted to Plant Microbe Interactions, a section of the journal Frontiers in Microbiology

                Article
                10.3389/fmicb.2020.00313
                7058703
                32184773
                c394fd73-a58e-4d19-888e-7a8fbdcb646d
                Copyright © 2020 Topalović, Hussain and Heuer.

                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 August 2019
                : 12 February 2020
                Page count
                Figures: 2, Tables: 1, Equations: 0, References: 159, Pages: 15, Words: 0
                Funding
                Funded by: Deutsche Forschungsgemeinschaft 10.13039/501100001659
                Categories
                Microbiology
                Review

                Microbiology & Virology
                disease-suppressive soils,plant-parasitic nematodes,root exudates,rhizosphere microbiome,root endophytes,nematode antagonists,induced systemic resistance

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