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Microbiome Modulation—Toward a Better Understanding of Plant Microbiome Response to Microbial Inoculants

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Microbiome Modulation—Toward a Better Understanding of Plant Microbiome Response to Microbial Inoculants fmicb-12-650610 March 31, 2021 Time: 16:31 # 1 REVIEW published: 08 April 2021 doi: 10.3389/fmicb.2021.650610 Microbiome Modulation—Toward a Better Understanding of Plant Microbiome Response to Microbial Inoculants Gabriele Berg1, Peter Kusstatscher1*, Ahmed Abdelfattah1, Tomislav Cernava1 and Kornelia Smalla2 1 Institute of Environmental Biotechnology, Graz University of Technology, Graz, Austria, 2 Julius Kühn Institute (JKI) Federal Research Centre for Cultivated Plants, Institute for Epidemiology and Pathogen Diagnostics, Braunschweig, Germany Plant-associated microorganisms are involved in important functions related to growth, performance and health of their hosts. Understanding their modes of action is important for the design of promising microbial inoculants for sustainable agriculture. Plant- associated microorganisms are able to interact with their hosts and often exert specific functions toward potential pathogens; the underlying in vitro interactions are Edited by: well studied. In contrast, in situ effects of inoculants, and especially their impact on Yong Wang, the plant indigenous microbiome was mostly neglected so far. Recently, microbiome Guizhou University, China research has revolutionized our understanding of plants as coevolved holobionts but Reviewed by: Sara Borin, also of indigenous microbiome-inoculant interactions. Here we disentangle the effects University of Milan, Italy of microbial inoculants on the indigenous plant microbiome and point out the following Jay Prakash Verma, Banaras Hindu University, India types of plant microbiome modulations: (i) transient microbiome shifts, (ii) stabilization or *Correspondence: increase of microbial diversity, (iii) stabilization or increase of plant microbiome evenness, Peter Kusstatscher (iv) restoration of a dysbiosis/compensation or reduction of a pathogen-induced shift, (v) [email protected] targeted shifts toward plant beneficial members of the indigenous microbiota, and (vi) Specialty section: suppression of potential pathogens. Therefore, we suggest microbiome modulations as This article was submitted to novel and efficient mode of action for microbial inoculants that can also be mediated via Microbe and Virus Interactions with the plant. Plants, a section of the journal Keywords: holobiont, microbial diversity, healthy plant microbiome, mode of action, microbiome shift Frontiers in Microbiology Received: 07 January 2021 Accepted: 19 March 2021 INTRODUCTION Published: 08 April 2021 Citation: Plants are naturally associated with specific microorganisms, which fulfill important functions, Berg G, Kusstatscher P, e.g., nutrient, mineral and vitamin supply, and protection against biotic and abiotic stress Abdelfattah A, Cernava T and (Vandenkoornhuyse et al., 2015; Sánchez-Cañizares et al., 2017; Bakker et al., 2020). Microbiome Smalla K (2021) Microbiome research has revolutionized our understanding of plant microbiome functioning, and it Modulation—Toward a Better Understanding of Plant Microbiome simultaneously opened new possibilities for applications toward sustainable agriculture (Berg et al., Response to Microbial Inoculants. 2020). Advances in engineering of environmental microbiomes are predicted to replace toxic Front. Microbiol. 12:650610. chemicals and fertilizers in agriculture in the future, and stimulate a more sustainable use of doi: 10.3389/fmicb.2021.650610 environmental resources, as well as improve our food processing (Massart et al., 2015). Currently, Frontiers in Microbiology| www.frontiersin.org 1 April 2021| Volume 12| Article 650610 fmicb-12-650610 March 31, 2021 Time: 16:31 # 2 Berg et al. Mode of Action Microbiome Shift agricultural products based on microorganisms are one of the novel, so far mostly unexplored mode of action to be termed fastest growing sectors in agronomy with a Compound Annual “microbiome modulation.” Growth Rate (CAGR) of 15–18% and a predicted value of over $10 billion United States dollars by 2025 for the whole biocontrol sector (DunhamTrimmer, 2017). CURRENT KNOWLEDGE RELATED TO Understanding their modes of action is important for the PLANT MICROBIOME INTERACTIONS design of promising applications in the form of microbial inoculants for sustainable agriculture (Berg, 2009; Köhl Plant microbiomes are characteristic microbial communities et al., 2019). Microbial inoculants comprise bioprotectants, in habitats that are well-defined by distinct physio-chemical biopesticides, and biostimulants, as well as biofertilizers properties, e.g., in the rhizoplane (the surface of the root), (Lugtenberg and Kamilova, 2009; DunhamTrimmer, 2017). rhizosphere (the soil influenced by the root), phyllosphere (stem However, these classifications, which are mostly based on to and leaves) and the endosphere (inner plant parts) (Philippot the underlying modes of action, are currently under discussion. et al., 2013; Hardoim et al., 2015; Remus-Emsermann and Moreover, there are various country-specific as well as continent- Schlechter, 2018). The plant and its associated microbiome specific definitions (ibma-global.org). From the scientific can also be regarded as a meta-organism the so-called point of view, most of microbial inoculants influence the host “holobiont” (Vandenkoornhuyse et al., 2015). Plant microbiome plant by stimulating plant defense response, plant hormone assembly starts with seeds, which are an important reservoir production and nutrient uptake (Windisch et al., 2017). Thus, of microorganisms (Berg and Raaijmakers, 2018). The current the categories listed above might be important for regulation model of plant microbiome assembly indicates that both the purposes but are still poorly defined, because inoculants that seed and soil microbiome are able to colonize the plant seedling, improve plant growth might also enhance plant resistance which allows to maintain microbial diversity and function but toward pathogens. Here, we use the term microbial inoculant also facilitates adaptation to the local environment (Bergna without further categorizing it. Many of the currently available et al., 2018). The phyllosphere microbiome is also recruited from inoculants are able to establish interactions by relying on airborne dust or irrigation water (Vorholt, 2012). Moreover, several modes of action, and their interactions depend on recent experimental evidences on the seed’s role in vertical environmental conditions (Köhl et al., 2019). Despite this fact, transmission across plant generations showed high spatial interaction with the indigenous plant microbiome are often not partitioning of the fungal and bacterial community, within both considered at all. seed and seedling, indicating inheritance, niche differentiation, In vitro plant-microbe as well as pathogen-microbe and divergent transmission routes for the establishment of root interactions are well studied (reviewed by Whipps et al., and phyllosphere communities (Rezki et al., 2016; Wassermann 1988; Weller et al., 2002; Berg, 2009; Köhl et al., 2019), while et al., 2019; Abdelfattah et al., 2021). Distinct microbes from the interactions with microbial inoculants in situ are not yet fully surrounding environment can colonize the plants surface and understood. Here, three-way interactions with the plant, with tissues, especially in the rhizosphere, which is the soil influenced pathogens and with the indigenous microbiome are possible to by the plant root and as such the interface to the soil. Here, induce beneficial effects. In general, the competence of microbial the plant species, its specific rhizo-deposits and exudate blend inoculants to colonize plant habitats is essential for successful constitute the main factors shaping the microbiome assembled interactions (Lugtenberg and Kamilova, 2009). Distinct steps in the vicinity of the roots (Neumann et al., 2014; Schreiter during the initiation of such interplay include recognition, et al., 2014a). However, the plant growth developmental stage, soil adherence, invasion (only endophytes and pathogens), properties and diverse agricultural management practices also colonization and growth, and several specific strategies to strongly shape the rhizosphere microbiome and can influence establish interactions (Hardoim et al., 2015). Direct interactions plant microbiome assembly (Paul Chowdhury et al., 2019; Smalla of microbial inoculants with host plants include (i) provision pers. communication). of nutrients and minerals, (ii) balancing the hormonal status of The plant-associated indigenous microbiome contributes with plants, and (iii) priming and induction of resistance (Schenk multiple functions to the holobiont, including (i) germination et al., 2010; Pieterse et al., 2014). Moreover, the ability to suppress and growth, (ii) nutrient supply, (iii) resistance against biotic and pathogens can be an important feature (Weller et al., 2002). abiotic stress factors, (iv) production of bioactive metabolites, Pathogen suppression can be based on (i) antibiosis: inhibition (v) plant development and flowering, and (vi) attraction of of microbial growth by bioactive substances, (ii) competition pollinators and of predators and parasites of herbivores (Pieterse (e.g., for iron) and modification of microenvironments, (iii) et al., 2014; Wagner et al., 2014; Berg et al., 2016; Etemadi et al., interference with pathogenicity, and (iv) parasitism and lysis 2018). To fulfill these functions, plant-associated microorganisms (Lugtenberg et al., 2002; Linares et al., 2006). Furthermore, a are embedded in complex networks with microorganisms of meta-analysis
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