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      Modulation of the Root Microbiome by Plant Molecules: The Basis for Targeted Disease Suppression and Plant Growth Promotion

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          Abstract

          Plants host a mesmerizing diversity of microbes inside and around their roots, known as the microbiome. The microbiome is composed mostly of fungi, bacteria, oomycetes, and archaea that can be either pathogenic or beneficial for plant health and fitness. To grow healthy, plants need to surveil soil niches around the roots for the detection of pathogenic microbes, and in parallel maximize the services of beneficial microbes in nutrients uptake and growth promotion. Plants employ a palette of mechanisms to modulate their microbiome including structural modifications, the exudation of secondary metabolites and the coordinated action of different defence responses. Here, we review the current understanding on the composition and activity of the root microbiome and how different plant molecules can shape the structure of the root-associated microbial communities. Examples are given on interactions that occur in the rhizosphere between plants and soilborne fungi. We also present some well-established examples of microbiome harnessing to highlight how plants can maximize their fitness by selecting their microbiome. Understanding how plants manipulate their microbiome can aid in the design of next-generation microbial inoculants for targeted disease suppression and enhanced plant growth.

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          Most cited references186

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          Induced systemic resistance by beneficial microbes.

          Beneficial microbes in the microbiome of plant roots improve plant health. Induced systemic resistance (ISR) emerged as an important mechanism by which selected plant growth-promoting bacteria and fungi in the rhizosphere prime the whole plant body for enhanced defense against a broad range of pathogens and insect herbivores. A wide variety of root-associated mutualists, including Pseudomonas, Bacillus, Trichoderma, and mycorrhiza species sensitize the plant immune system for enhanced defense without directly activating costly defenses. This review focuses on molecular processes at the interface between plant roots and ISR-eliciting mutualists, and on the progress in our understanding of ISR signaling and systemic defense priming. The central role of the root-specific transcription factor MYB72 in the onset of ISR and the role of phytohormones and defense regulatory proteins in the expression of ISR in aboveground plant parts are highlighted. Finally, the ecological function of ISR-inducing microbes in the root microbiome is discussed.
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            Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi.

            Arbuscular mycorrhizal (AM) fungi form mutualistic, symbiotic associations with the roots of more than 80% of land plants. The fungi are incapable of completing their life cycle in the absence of a host root. Their spores can germinate and grow in the absence of a host, but their hyphal growth is very limited. Little is known about the molecular mechanisms that govern signalling and recognition between AM fungi and their host plants. In one of the first stages of host recognition, the hyphae of AM fungi show extensive branching in the vicinity of host roots before formation of the appressorium, the structure used to penetrate the plant root. Host roots are known to release signalling molecules that trigger hyphal branching, but these branching factors have not been isolated. Here we have isolated a branching factor from the root exudates of Lotus japonicus and used spectroscopic analysis and chemical synthesis to identify it as a strigolactone, 5-deoxy-strigol. Strigolactones are a group of sesquiterpene lactones, previously isolated as seed-germination stimulants for the parasitic weeds Striga and Orobanche. The natural strigolactones 5-deoxy-strigol, sorgolactone and strigol, and a synthetic analogue, GR24, induced extensive hyphal branching in germinating spores of the AM fungus Gigaspora margarita at very low concentrations.
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              Feed Your Friends: Do Plant Exudates Shape the Root Microbiome?

              Plant health in natural environments depends on interactions with complex and dynamic communities comprising macro- and microorganisms. While many studies have provided insights into the composition of rhizosphere microbiomes (rhizobiomes), little is known about whether plants shape their rhizobiomes. Here, we discuss physiological factors of plants that may govern plant-microbe interactions, focusing on root physiology and the role of root exudates. Given that only a few plant transport proteins are known to be involved in root metabolite export, we suggest novel families putatively involved in this process. Finally, building off of the features discussed in this review, and in analogy to well-known symbioses, we elaborate on a possible sequence of events governing rhizobiome assembly.
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                Author and article information

                Contributors
                Journal
                Front Plant Sci
                Front Plant Sci
                Front. Plant Sci.
                Frontiers in Plant Science
                Frontiers Media S.A.
                1664-462X
                24 January 2020
                2019
                : 10
                : 1741
                Affiliations
                [1] 1 Department of Agricultural Sciences, University of Naples Federico II , Naples, Italy
                [2] 2 Department of Ecological and Biological Sciences, University of Tuscia , Viterbo, Italy
                [3] 3 Department of Agricultural Sciences, Biotechnology and Food Science, Cyprus University of Technology , Limassol, Cyprus
                [4] 4 Plant-Microbe Interactions, Department of Biology, Science4Life, Utrecht University , Utrecht, Netherlands
                Author notes

                Edited by: Paulo José Pereira Lima Teixeira, University of São Paulo, Brazil

                Reviewed by: Ka Wai Ma, Max Planck Institute for Plant Breeding Research, Germany; Kei Hiruma, Nara Institute of Science and Technology (NAIST), Japan

                *Correspondence: Iakovos S. Pantelides, iakovos.pantelides@ 123456cut.ac.cy ; Ioannis A. Stringlis, I.Stringlis@ 123456uu.nl

                †These authors share first authorship.

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

                Article
                10.3389/fpls.2019.01741
                6992662
                32038698
                b578e970-1e4a-4d02-ba2d-cbdb0c2a3b99
                Copyright © 2020 Pascale, Proietti, Pantelides and Stringlis

                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
                : 30 September 2019
                : 11 December 2019
                Page count
                Figures: 2, Tables: 1, Equations: 0, References: 270, Pages: 23, Words: 12877
                Funding
                Funded by: Ministero dell’Istruzione, dell’Università e della Ricerca 10.13039/501100003407
                Categories
                Plant Science
                Review

                Plant science & Botany
                plant defense,plant growth promotion,plant molecules,root exudation,root microbiome,microbiota,disease suppression,microbial inoculants

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