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      A lysin motif effector subverts chitin‐triggered immunity to facilitate arbuscular mycorrhizal symbiosis

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          Summary

          • Arbuscular mycorrhizal (AM) fungi greatly improve mineral uptake by host plants in nutrient‐depleted soil and can intracellularly colonize root cortex cells in the vast majority of higher plants. However, AM fungi possess common fungal cell wall components such as chitin that can be recognized by plant chitin receptors to trigger immune responses, raising the question as to how AM fungi effectively evade chitin‐triggered immune responses during symbiosis.

          • In this study, we characterize a secreted lysin motif (LysM) effector identified from the model AM fungal species Rhizophagus irregularis, called RiSLM.

          • RiSLM is one of the highest expressed effector proteins in intraradical mycelium during the symbiosis. In vitro binding assays show that RiSLM binds chitin‐oligosaccharides and can protect fungal cell walls from chitinases. Moreover, RiSLM efficiently interferes with chitin‐triggered immune responses, such as defence gene induction and reactive oxygen species production in Medicago truncatula. Although RiSLM also binds to symbiotic (lipo)chitooligosaccharides it does not interfere significantly with symbiotic signalling in Medicago. Host‐induced gene silencing of RiSLM greatly reduces fungal colonization levels.

          • Taken together, our results reveal a key role for AM fungal LysM effectors to subvert chitin‐triggered immunity in symbiosis, pointing to a common role for LysM effectors in both symbiotic and pathogenic fungi.

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          CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis.

          Chitin is a major component of fungal cell walls and serves as a microbe-associated molecular pattern (MAMP) for the detection of various potential pathogens in innate immune systems of both plants and animals. We recently showed that chitin elicitor-binding protein (CEBiP), plasma membrane glycoprotein with LysM motifs, functions as a cell surface receptor for chitin elicitor in rice. The predicted structure of CEBiP does not contain any intracellular domains, suggesting that an additional component(s) is required for signaling through the plasma membrane into the cytoplasm. Here, we identified a receptor-like kinase, designated CERK1, which is essential for chitin elicitor signaling in Arabidopsis. The KO mutants for CERK1 completely lost the ability to respond to the chitin elicitor, including MAPK activation, reactive oxygen species generation, and gene expression. Disease resistance of the KO mutant against an incompatible fungus, Alternaria brassicicola, was partly impaired. Complementation with the WT CERK1 gene showed cerk1 mutations were responsible for the mutant phenotypes. CERK1 is a plasma membrane protein containing three LysM motifs in the extracellular domain and an intracellular Ser/Thr kinase domain with autophosphorylation/myelin basic protein kinase activity, suggesting that CERK1 plays a critical role in fungal MAMP perception in plants.
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            A golden gate modular cloning toolbox for plants.

            Plant Synthetic Biology requires robust and efficient methods for assembling multigene constructs. Golden Gate cloning provides a precision module-based cloning technique for facile assembly of multiple genes in one construct. We present here a versatile resource for plant biologists comprising a set of cloning vectors and 96 standardized parts to enable Golden Gate construction of multigene constructs for plant transformation. Parts include promoters, untranslated sequences, reporters, antigenic tags, localization signals, selectable markers, and terminators. The comparative performance of parts in the model plant Nicotiana benthamiana is discussed.
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              Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza.

              Arbuscular mycorrhiza (AM) is a root endosymbiosis between plants and glomeromycete fungi. It is the most widespread terrestrial plant symbiosis, improving plant uptake of water and mineral nutrients. Yet, despite its crucial role in land ecosystems, molecular mechanisms leading to its formation are just beginning to be unravelled. Recent evidence suggests that AM fungi produce diffusible symbiotic signals. Here we show that Glomus intraradices secretes symbiotic signals that are a mixture of sulphated and non-sulphated simple lipochitooligosaccharides (LCOs), which stimulate formation of AM in plant species of diverse families (Fabaceae, Asteraceae and Umbelliferae). In the legume Medicago truncatula these signals stimulate root growth and branching by the symbiotic DMI signalling pathway. These findings provide a better understanding of the evolution of signalling mechanisms involved in plant root endosymbioses and will greatly facilitate their molecular dissection. They also open the way to using these natural and very active molecules in agriculture.
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                Author and article information

                Contributors
                erik.limpens@wur.nl
                Journal
                New Phytol
                New Phytol
                10.1111/(ISSN)1469-8137
                NPH
                The New Phytologist
                John Wiley and Sons Inc. (Hoboken )
                0028-646X
                1469-8137
                23 November 2019
                January 2020
                : 225
                : 1 ( doiID: 10.1111/nph.v225.1 )
                : 448-460
                Affiliations
                [ 1 ] Laboratory of Molecular Biology Wageningen University & Research 6708 PB Wageningen the Netherlands
                [ 2 ] Department of Plant Sciences Laboratory of Phytopathology Wageningen University & Research 6708 PB Wageningen the Netherlands
                [ 3 ] Laboratory of Biochemistry Wageningen University & Research 6708 WE Wageningen the Netherlands
                [ 4 ] LIPM Université de Toulouse INRA CNRS Castanet‐Tolosan France
                [ 5 ] CNRS CERMAV University Grenoble Alpes UPR 5301 38041 Grenoble France
                Author notes
                [*] [* ] Author for correspondence:

                Erik Limpens

                Tel: +31 317 483264

                Email: erik.limpens@ 123456wur.nl

                [†]

                These authors contributed equally to this work.

                Author information
                https://orcid.org/0000-0002-0315-7658
                https://orcid.org/0000-0003-2385-8782
                https://orcid.org/0000-0002-6133-9900
                https://orcid.org/0000-0003-4125-4181
                https://orcid.org/0000-0002-9668-4085
                Article
                NPH16245 2019-30147
                10.1111/nph.16245
                6916333
                31596956
                eb813ed0-50e6-4e6b-9aa7-02209d331eb0
                © 2019 The Authors. New Phytologist © 2019 New Phytologist Trust

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 04 February 2019
                : 24 September 2019
                Page count
                Figures: 7, Tables: 0, Pages: 13, Words: 9763
                Funding
                Funded by: European Research Council , open-funder-registry 10.13039/100010663;
                Award ID: ERC‐2011‐AdG294790
                Categories
                Full Paper
                Research
                Full Papers
                Custom metadata
                2.0
                January 2020
                Converter:WILEY_ML3GV2_TO_JATSPMC version:5.7.3 mode:remove_FC converted:17.12.2019

                Plant science & Botany
                arbuscular mycorrhiza,chitin,effector,lysm,plant immunity,symbiosis
                Plant science & Botany
                arbuscular mycorrhiza, chitin, effector, lysm, plant immunity, symbiosis

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