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      The Multiple Facets of Plant–Fungal Interactions Revealed Through Plant and Fungal Secretomics

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          Abstract

          The plant secretome is usually considered in the frame of proteomics, aiming at characterizing extracellular proteins, their biological roles and the mechanisms accounting for their secretion in the extracellular space. In this review, we aim to highlight recent results pertaining to secretion through the conventional and unconventional protein secretion pathways notably those involving plant exosomes or extracellular vesicles. Furthermore, plants are well known to actively secrete a large array of different molecules from polymers (e.g. extracellular RNA and DNA) to small compounds (e.g. ATP, phytochemicals, secondary metabolites, phytohormones). All of these play pivotal roles in plant-fungi (or oomycetes) interactions, both for beneficial (mycorrhizal fungi) and deleterious outcomes (pathogens) for the plant. For instance, recent work reveals that such secretion of small molecules by roots is of paramount importance to sculpt the rhizospheric microbiota. Our aim in this review is to extend the definition of the plant and fungal secretomes to a broader sense to better understand the functioning of the plant/microorganisms holobiont. Fundamental perspectives will be brought to light along with the novel tools that should support establishing an environment-friendly and sustainable agriculture.

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          Most cited references163

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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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            Fungal secondary metabolism - from biochemistry to genomics.

            Much of natural product chemistry concerns a group of compounds known as secondary metabolites. These low-molecular-weight metabolites often have potent physiological activities. Digitalis, morphine and quinine are plant secondary metabolites, whereas penicillin, cephalosporin, ergotrate and the statins are equally well known fungal secondary metabolites. Although chemically diverse, all secondary metabolites are produced by a few common biosynthetic pathways, often in conjunction with morphological development. Recent advances in molecular biology, bioinformatics and comparative genomics have revealed that the genes encoding specific fungal secondary metabolites are clustered and often located near telomeres. In this review, we address some important questions, including which evolutionary pressures led to gene clustering, why closely related species produce different profiles of secondary metabolites, and whether fungal genomics will accelerate the discovery of new pharmacologically active natural products.
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              Fungal small RNAs suppress plant immunity by hijacking host RNA interference pathways.

              Botrytis cinerea, the causative agent of gray mold disease, is an aggressive fungal pathogen that infects more than 200 plant species. Here, we show that some B. cinerea small RNAs (Bc-sRNAs) can silence Arabidopsis and tomato genes involved in immunity. These Bc-sRNAs hijack the host RNA interference (RNAi) machinery by binding to Arabidopsis Argonaute 1 (AGO1) and selectively silencing host immunity genes. The Arabidopsis ago1 mutant exhibits reduced susceptibility to B. cinerea, and the B. cinerea dcl1 dcl2 double mutant that can no longer produce these Bc-sRNAs displays reduced pathogenicity on Arabidopsis and tomato. Thus, this fungal pathogen transfers "virulent" sRNA effectors into host plant cells to suppress host immunity and achieve infection, which demonstrates a naturally occurring cross-kingdom RNAi as an advanced virulence mechanism.
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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
                08 January 2020
                2019
                : 10
                : 1626
                Affiliations
                [1] 1 Agriculture Victoria Research, AgriBio, Centre for AgriBioscience , Bundoora, VIC, Australia
                [2] 2 AgroBioSciences Program, Mohammed VI Polytechnic University (UM6P) , Ben Guerir, Morocco
                [3] 3 CNRS/Université Claude Bernard Lyon 1/Institut National des Sciences Appliquées/Bayer CropScience Joint Laboratory (UMR 5240), Bayer CropScience , Lyon, France
                Author notes

                Edited by: Vincenzo Lionetti, Sapienza University of Rome, Italy

                Reviewed by: Raffaella Balestrini, Italian National Research Council (IPSP-CNR), Italy; Manuel Benedetti, University of L’Aquila, Italy

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

                Article
                10.3389/fpls.2019.01626
                6960344
                33281860
                2501f0da-9b2c-45ff-a360-786c70aebc0e
                Copyright © 2020 Vincent, Rafiqi and Job

                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
                : 29 July 2019
                : 19 November 2019
                Page count
                Figures: 1, Tables: 1, Equations: 0, References: 194, Pages: 19, Words: 9858
                Categories
                Plant Science
                Review

                Plant science & Botany
                agriculture,apoplast,extracellular vesicles,fungal effectors,plant–fungi interactions,root exudates,whole and integrated secretomics

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