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      Climate change impacts on plant pathogens, food security and paths forward

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          Abstract

          Plant disease outbreaks pose significant risks to global food security and environmental sustainability worldwide, and result in the loss of primary productivity and biodiversity that negatively impact the environmental and socio-economic conditions of affected regions. Climate change further increases outbreak risks by altering pathogen evolution and host–pathogen interactions and facilitating the emergence of new pathogenic strains. Pathogen range can shift, increasing the spread of plant diseases in new areas. In this Review, we examine how plant disease pressures are likely to change under future climate scenarios and how these changes will relate to plant productivity in natural and agricultural ecosystems. We explore current and future impacts of climate change on pathogen biogeography, disease incidence and severity, and their effects on natural ecosystems, agriculture and food production. We propose that amendment of the current conceptual framework and incorporation of eco-evolutionary theories into research could improve our mechanistic understanding and prediction of pathogen spread in future climates, to mitigate the future risk of disease outbreaks. We highlight the need for a science–policy interface that works closely with relevant intergovernmental organizations to provide effective monitoring and management of plant disease under future climate scenarios, to ensure long-term food and nutrient security and sustainability of natural ecosystems.

          Abstract

          In this Review, Singh et al. explore the impact of future climate scenarios on plant pathogen burden and biogeography, their interaction with the plant microbiome and the consequences on plant disease and productivity in different ecosystems. They propose different approaches to ensure long-term global food security.

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          Most cited references185

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          Plant–microbiome interactions: from community assembly to plant health

          Healthy plants host diverse but taxonomically structured communities of microorganisms, the plant microbiota, that colonize every accessible plant tissue. Plant-associated microbiomes confer fitness advantages to the plant host, including growth promotion, nutrient uptake, stress tolerance and resistance to pathogens. In this Review, we explore how plant microbiome research has unravelled the complex network of genetic, biochemical, physical and metabolic interactions among the plant, the associated microbial communities and the environment. We also discuss how those interactions shape the assembly of plant-associated microbiomes and modulate their beneficial traits, such as nutrient acquisition and plant health, in addition to highlighting knowledge gaps and future directions.
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            Deciphering the rhizosphere microbiome for disease-suppressive bacteria.

            Disease-suppressive soils are exceptional ecosystems in which crop plants suffer less from specific soil-borne pathogens than expected owing to the activities of other soil microorganisms. For most disease-suppressive soils, the microbes and mechanisms involved in pathogen control are unknown. By coupling PhyloChip-based metagenomics of the rhizosphere microbiome with culture-dependent functional analyses, we identified key bacterial taxa and genes involved in suppression of a fungal root pathogen. More than 33,000 bacterial and archaeal species were detected, with Proteobacteria, Firmicutes, and Actinobacteria consistently associated with disease suppression. Members of the γ-Proteobacteria were shown to have disease-suppressive activity governed by nonribosomal peptide synthetases. Our data indicate that upon attack by a fungal root pathogen, plants can exploit microbial consortia from soil for protection against infections.
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              Pathogen-induced activation of disease-suppressive functions in the endophytic root microbiome

              Microorganisms living inside plants can promote plant growth and health, but their genomic and functional diversity remain largely elusive. Here, metagenomics and network inference show that fungal infection of plant roots enriched for Chitinophagaceae and Flavobacteriaceae in the root endosphere and for chitinase genes and various unknown biosynthetic gene clusters encoding the production of nonribosomal peptide synthetases (NRPSs) and polyketide synthases (PKSs). After strain-level genome reconstruction, a consortium of Chitinophaga and Flavobacterium was designed that consistently suppressed fungal root disease. Site-directed mutagenesis then revealed that a previously unidentified NRPS-PKS gene cluster from Flavobacterium was essential for disease suppression by the endophytic consortium. Our results highlight that endophytic root microbiomes harbor a wealth of as yet unknown functional traits that, in concert, can protect the plant inside out.
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                Author and article information

                Contributors
                b.singh@westernsydney.edu.au
                Journal
                Nat Rev Microbiol
                Nat Rev Microbiol
                Nature Reviews. Microbiology
                Nature Publishing Group UK (London )
                1740-1526
                1740-1534
                2 May 2023
                : 1-17
                Affiliations
                [1 ]GRID grid.1029.a, ISNI 0000 0000 9939 5719, Hawkesbury Institute for the Environment, , Western Sydney University, ; Penrith, New South Wales Australia
                [2 ]GRID grid.1029.a, ISNI 0000 0000 9939 5719, Global Centre for Land-Based Innovation, , Western Sydney University, ; Penrith, New South Wales Australia
                [3 ]GRID grid.466818.5, ISNI 0000 0001 2158 9975, Laboratorio de Biodiversidad y Funcionamiento Ecosistémico, Instituto de Recursos Naturales y Agrobiología de Sevilla (IRNAS), CSIC, ; Sevilla, Spain
                [4 ]GRID grid.15449.3d, ISNI 0000 0001 2200 2355, Unidad Asociada CSIC-UPO (BioFun), , Universidad Pablo de Olavide, ; Sevilla, Spain
                [5 ]GRID grid.5268.9, ISNI 0000 0001 2168 1800, Multidisciplinary Institute for Environment Studies ‘Ramon Margalef’, , University of Alicante, ; Alicante, Spain
                [6 ]GRID grid.47894.36, ISNI 0000 0004 1936 8083, Microbiome Newtork and Department of Agricultural Biology, , Colorado State University, ; Fort Collins, CO USA
                Author information
                http://orcid.org/0000-0003-4413-4185
                http://orcid.org/0000-0002-1211-2355
                http://orcid.org/0000-0001-5348-7391
                http://orcid.org/0000-0001-7252-4397
                http://orcid.org/0000-0002-8200-8801
                http://orcid.org/0000-0003-0173-2804
                Article
                900
                10.1038/s41579-023-00900-7
                10153038
                37131070
                a1b97de7-b3de-4a76-9b7c-60519b7a028c
                © Springer Nature Limited 2023, Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

                This article is made available via the PMC Open Access Subset for unrestricted research re-use and secondary analysis in any form or by any means with acknowledgement of the original source. These permissions are granted for the duration of the World Health Organization (WHO) declaration of COVID-19 as a global pandemic.

                History
                : 11 April 2023
                Categories
                Review Article

                pathogens,microbiome,climate change,plant sciences
                pathogens, microbiome, climate change, plant sciences

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