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      Mode of Action of Microbial Biological Control Agents Against Plant Diseases: Relevance Beyond Efficacy

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          Abstract

          Microbial biological control agents (MBCAs) are applied to crops for biological control of plant pathogens where they act via a range of modes of action. Some MBCAs interact with plants by inducing resistance or priming plants without any direct interaction with the targeted pathogen. Other MBCAs act via nutrient competition or other mechanisms modulating the growth conditions for the pathogen. Antagonists acting through hyperparasitism and antibiosis are directly interfering with the pathogen. Such interactions are highly regulated cascades of metabolic events, often combining different modes of action. Compounds involved such as signaling compounds, enzymes and other interfering metabolites are produced in situ at low concentrations during interaction. The potential of microorganisms to produce such a compound in vitro does not necessarily correlate with their in situ antagonism. Understanding the mode of action of MBCAs is essential to achieve optimum disease control. Also understanding the mode of action is important to be able to characterize possible risks for humans or the environment and risks for resistance development against the MBCA. Preferences for certain modes of action for an envisaged application of a MBCA also have impact on the screening methods used to select new microbials. Screening of MBCAs in bioassays on plants or plant tissues has the advantage that MBCAs with multiple modes of action and their combinations potentially can be detected whereas simplified assays on nutrient media strongly bias the selection toward in vitro production of antimicrobial metabolites which may not be responsible for in situ antagonism. Risks assessments for MBCAs are relevant if they contain antimicrobial metabolites at effective concentration in the product. However, in most cases antimicrobial metabolites are produced by antagonists directly on the spot where the targeted organism is harmful. Such ubiquitous metabolites involved in natural, complex, highly regulated interactions between microbial cells and/or plants are not relevant for risk assessments. Currently, risks of microbial metabolites involved in antagonistic modes of action are often assessed similar to assessments of single molecule fungicides. The nature of the mode of action of antagonists requires a rethinking of data requirements for the registration of MBCAs.

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          Most cited references83

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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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            Bacillus lipopeptides: versatile weapons for plant disease biocontrol.

            In the context of biocontrol of plant diseases, the three families of Bacillus lipopeptides - surfactins, iturins and fengycins were at first mostly studied for their antagonistic activity for a wide range of potential phytopathogens, including bacteria, fungi and oomycetes. Recent investigations have shed light on the fact that these lipopeptides can also influence the ecological fitness of the producing strain in terms of root colonization (and thereby persistence in the rhizosphere) and also have a key role in the beneficial interaction of Bacillus species with plants by stimulating host defence mechanisms. The different structural traits and physico-chemical properties of these effective surface- and membrane-active amphiphilic biomolecules explain their involvement in most of the mechanisms developed by bacteria for the biocontrol of different plant pathogens.
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              Pathogen population genetics, evolutionary potential, and durable resistance.

              We hypothesize that the evolutionary potential of a pathogen population is reflected in its population genetic structure. Pathogen populations with a high evolutionary potential are more likely to overcome genetic resistance than pathogen populations with a low evolutionary potential. We propose a flexible framework to predict the evolutionary potential of pathogen populations based on analysis of their genetic structure. According to this framework, pathogens that pose the greatest risk of breaking down resistance genes have a mixed reproduction system, a high potential for genotype flow, large effective population sizes, and high mutation rates. The lowest risk pathogens are those with strict asexual reproduction, low potential for gene flow, small effective population sizes, and low mutation rates. We present examples of high-risk and low-risk pathogens. We propose general guidelines for a rational approach to breed durable resistance according to the evolutionary potential of the pathogen.
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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
                19 July 2019
                2019
                : 10
                : 845
                Affiliations
                [1] 1Wageningen Plant Research, Wageningen University & Research , Wageningen, Netherlands
                [2] 2Linge Agroconsultancy B.V. , Oosterhout, Netherlands
                [3] 3Koppert Biological Systems , Berkel en Rodenrijs, Netherlands
                Author notes

                Edited by: Jesús Mercado-Blanco, Instituto de Agricultura Sostenible (IAS), Spain

                Reviewed by: Linda Thomashow, Agricultural Research Service (USDA), United States; Gianfranco Romanazzi, Marche Polytechnic University, Italy; Clara Pliego Prieto, Andalusian Institute for Research and Training in Agriculture, Fisheries, Food and Ecological Production (IFAPA), Spain

                *Correspondence: Jürgen Köhl, jurgen.kohl@ 123456wur.nl

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

                Article
                10.3389/fpls.2019.00845
                6658832
                31379891
                4e3dbb10-d93c-44ee-b545-a428e19b9727
                Copyright © 2019 Köhl, Kolnaar and Ravensberg.

                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
                : 18 February 2019
                : 12 June 2019
                Page count
                Figures: 1, Tables: 2, Equations: 0, References: 101, Pages: 19, Words: 0
                Categories
                Plant Science
                Review

                Plant science & Botany
                biological control,plant diseases,mode of action,antagonist,risk assessment,screening

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