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      The Arabidopsis leucine-rich repeat receptor kinase MIK2/LRR-KISS connects cell wall integrity sensing, root growth and response to abiotic and biotic stresses

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          Abstract

          Plants actively perceive and respond to perturbations in their cell walls which arise during growth, biotic and abiotic stresses. However, few components involved in plant cell wall integrity sensing have been described to date. Using a reverse-genetic approach, we identified the Arabidopsis thaliana leucine-rich repeat receptor kinase MIK2 as an important regulator of cell wall damage responses triggered upon cellulose biosynthesis inhibition. Indeed, loss-of-function mik2 alleles are strongly affected in immune marker gene expression, jasmonic acid production and lignin deposition. MIK2 has both overlapping and distinct functions with THE1, a malectin-like receptor kinase previously proposed as cell wall integrity sensor. In addition, mik2 mutant plants exhibit enhanced leftward root skewing when grown on vertical plates. Notably, natural variation in MIK2 (also named LRR-KISS) has been correlated recently to mild salt stress tolerance, which we could confirm using our insertional alleles. Strikingly, both the increased root skewing and salt stress sensitivity phenotypes observed in the mik2 mutant are dependent on THE1. Finally, we found that MIK2 is required for resistance to the fungal root pathogen Fusarium oxysporum. Together, our data identify MIK2 as a novel component in cell wall integrity sensing and suggest that MIK2 is a nexus linking cell wall integrity sensing to growth and environmental cues.

          Author summary

          Plants are constantly exposed to external stresses of biotic and abiotic nature, as well as internal stresses, resulting from growth and mechanical tension. Feedback information about the integrity of the cell wall can enable the plant to perceive such stresses, and respond adequately. Plants are known to perceive signals from their environment through receptor kinases at the plant cell surface. Here, we reveal that the Arabidopsis thaliana receptor kinase MIK2 regulates responses to cell wall perturbation. Moreover, we find that MIK2 controls root growth angle, modulates cell wall structure in the root tip, contributes to salt stress tolerance, and is required for resistance against a root-infecting pathogen. Our data suggest that MIK2 is involved in sensing cell wall perturbations in plants, whereby it allows the plant to cope with a diverse range of environmental stresses. These data provide an important step forward in our understanding of the mechanisms plants deploy to sense internal and external danger.

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          Comparative analysis of the receptor-like kinase family in Arabidopsis and rice.

          Receptor-like kinases (RLKs) belong to the large RLK/Pelle gene family, and it is known that the Arabidopsis thaliana genome contains >600 such members, which play important roles in plant growth, development, and defense responses. Surprisingly, we found that rice (Oryza sativa) has nearly twice as many RLK/Pelle members as Arabidopsis does, and it is not simply a consequence of a larger predicted gene number in rice. From the inferred phylogeny of all Arabidopsis and rice RLK/Pelle members, we estimated that the common ancestor of Arabidopsis and rice had >440 RLK/Pelles and that large-scale expansions of certain RLK/Pelle members and fusions of novel domains have occurred in both the Arabidopsis and rice lineages since their divergence. In addition, the extracellular domains have higher nonsynonymous substitution rates than the intracellular domains, consistent with the role of extracellular domains in sensing diverse signals. The lineage-specific expansions in Arabidopsis can be attributed to both tandem and large-scale duplications, whereas tandem duplication seems to be the major mechanism for recent expansions in rice. Interestingly, although the RLKs that are involved in development seem to have rarely been duplicated after the Arabidopsis-rice split, those that are involved in defense/disease resistance apparently have undergone many duplication events. These findings led us to hypothesize that most of the recent expansions of the RLK/Pelle family have involved defense/resistance-related genes.
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            Plant PRRs and the activation of innate immune signaling.

            Despite being sessile organisms constantly exposed to potential pathogens and pests, plants are surprisingly resilient to infections. Plants can detect invaders via the recognition of pathogen-associated molecular patterns (PAMPs) by pattern recognition receptors (PRRs). Plant PRRs are surface-localized receptor-like kinases, which comprise a ligand-binding ectodomain and an intracellular kinase domain, or receptor-like proteins, which do not exhibit any known intracellular signaling domain. In this review, we summarize recent discoveries that shed light on the molecular mechanisms underlying ligand perception and subsequent activation of plant PRRs. Notably, plant PRRs appear as central components of multiprotein complexes at the plasma membrane that contain additional transmembrane and cytosolic kinases required for the initiation and specificity of immune signaling. PRR complexes are under tight control by protein phosphatases, E3 ligases, and other regulatory proteins, illustrating the exquisite and complex regulation of these molecular machines whose proper activation underlines a crucial layer of plant immunity. Copyright © 2014 Elsevier Inc. All rights reserved.
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              Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases.

              Plant receptor-like kinases (RLKs) are proteins with a predicted signal sequence, single transmembrane region, and cytoplasmic kinase domain. Receptor-like kinases belong to a large gene family with at least 610 members that represent nearly 2.5% of Arabidopsis protein coding genes. We have categorized members of this family into subfamilies based on both the identity of the extracellular domains and the phylogenetic relationships between the kinase domains of subfamily members. Surprisingly, this structurally defined group of genes is monophyletic with respect to kinase domains when compared with the other eukaryotic kinase families. In an extended analysis, animal receptor kinases, Raf kinases, plant RLKs, and animal receptor tyrosine kinases form a well supported group sharing a common origin within the superfamily of serine/threonine/tyrosine kinases. Among animal kinase sequences, Drosophila Pelle and related cytoplasmic kinases fall within the plant RLK clade, which we now define as the RLK/Pelle family. A survey of expressed sequence tag records for land plants reveals that mosses, ferns, conifers, and flowering plants have similar percentages of expressed sequence tags representing RLK/Pelle homologs, suggesting that the size of this gene family may have been close to the present-day level before the diversification of land plant lineages. The distribution pattern of four RLK subfamilies on Arabidopsis chromosomes indicates that the expansion of this gene family is partly a consequence of duplication and reshuffling of the Arabidopsis genome and of the generation of tandem repeats.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Genet
                PLoS Genet
                plos
                plosgen
                PLoS Genetics
                Public Library of Science (San Francisco, CA USA )
                1553-7390
                1553-7404
                12 June 2017
                June 2017
                : 13
                : 6
                : e1006832
                Affiliations
                [1 ]The Sainsbury Laboratory, Norwich Research Park, Norwich, United Kingdom
                [2 ]Department of Biology, Norwegian University of Science and Technology, Trondheim, Norway
                [3 ]Department of Life Sciences, Imperial College London, London, United Kingdom
                [4 ]Institut Jean-Pierre Bourgin, INRA, AgroParisTech, CNRS, Université Paris-Saclay, Versailles, France
                [5 ]Department of Plant Cell Biology, University of Amsterdam, Amsterdam, The Netherlands
                [6 ]Department of Phytopathology, University of Amsterdam, Amsterdam, The Netherlands
                [7 ]Centro de Biotecnología y Genómica de Plantas (UPM-INIA), Universidad Politécnica de Madrid (UPM)–Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA), Campus Montegancedo UPM, Pozuelo de Alarcón (Madrid), Spain
                [8 ]Department of Plant Molecular Biology, University of Lausanne, Biophore Building, Lausanne, Switzerland
                University of Massachusetts at Amherst, UNITED STATES
                Author notes

                The authors have declared that no competing interests exist.

                • Conceptualization: DVdD FB SV AM CT GM HH TH CZ.

                • Formal analysis: DVdD FB TE SV GM IK NT EM ASB.

                • Funding acquisition: CSH AM MRe CT HH TH CZ.

                • Investigation: DVdD FB TE JR JFM SV IK NT MV EM CS MRo ASB.

                • Project administration: TH CZ.

                • Resources: MRo.

                • Supervision: SV AM CT GM HH TH CZ.

                • Validation: DVdD FB TE JR.

                • Visualization: DVdD.

                • Writing – original draft: DVdD CZ.

                • Writing – review & editing: DVdD FB TE JR JFM SV IK NT MV EM CS MRo ASB CSH AM MRe CT GM HH TH CZ.

                [¤a]

                Current address: Department of Biological and Medical Sciences, Oxford Brookes University, Oxford, United Kingdom.

                [¤b]

                Current address: Department of Plant Science, Plant Genomics and Breeding Institute, and Research Institute of Agriculture and Life Sciences, Seoul National University, Seoul, Republic of Korea.

                [¤c]

                Current address: University of Copenhagen, Department of Biology, Copenhagen, Denmark.

                Author information
                http://orcid.org/0000-0002-2169-0536
                http://orcid.org/0000-0002-3953-1648
                http://orcid.org/0000-0003-4838-6048
                http://orcid.org/0000-0002-8973-5518
                http://orcid.org/0000-0002-1993-4802
                http://orcid.org/0000-0002-5593-3620
                http://orcid.org/0000-0003-3608-6283
                http://orcid.org/0000-0001-6738-115X
                http://orcid.org/0000-0002-5493-754X
                http://orcid.org/0000-0003-4935-8583
                Article
                PGENETICS-D-16-01740
                10.1371/journal.pgen.1006832
                5484538
                28604776
                037247d9-91cc-4f30-985f-c3b0c7c6a312
                © 2017 Van der Does et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 4 August 2016
                : 22 May 2017
                Page count
                Figures: 5, Tables: 0, Pages: 27
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100000268, Biotechnology and Biological Sciences Research Council;
                Award ID: BB/G024936/1
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100000268, Biotechnology and Biological Sciences Research Council;
                Award ID: BB/G024944/1
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100004410, European Molecular Biology Organization;
                Award ID: ALTF 657-2013
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100001659, Deutsche Forschungsgemeinschaft;
                Award ID: EN 1071/1-1
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100000268, Biotechnology and Biological Sciences Research Council;
                Award ID: n/a
                Award Recipient :
                Funded by: Norwegian University of Science and Technology
                Award ID: n/a
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100001665, Agence Nationale de la Recherche;
                Award ID: Pectosign
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100003339, Consejo Superior de Investigaciones Científicas;
                Award ID: BIO2012-32910
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100001665, Agence Nationale de la Recherche;
                Award ID: ANR-10-LABX-0040-SPS
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100000268, Biotechnology and Biological Sciences Research Council;
                Award ID: BB/K01269X/1
                Award Recipient :
                This research was supported by the Gatsby Charitable Foundation, by the Biotechnology and Biological Sciences Research Council (BBSRC) (grants BB/G024936/1 ‘ERA-PG PRR CROP’ and BB/G024944/1 ‘Pathonet’) (CZ), a long-term post-doctoral fellowship from the European Molecular Biology Organization (ALTF 657-2013) (to DVdD), a Deutsche Forschungsgemeinschaft post-doctoral fellowship (EN 1071/1-1) (to TE), a BBSRC industrial CASE PhD studentship (to JR), a BBSRC PhD studentship (to JFM), an NTNU post-doctoral fellowship (to MV), an ANR Grant « Pectosign » (to SV, GM and HH), a post-doctoral fellowship from MINECO (BIO2012-32910) (to EM), and a Netherlands Organization for Scientific Research (NWO) ALW Graduate Program grant 831.15.004 (to IK and CT). MRo was part of the John Innes Centre/The Sainsbury Laboratory PhD rotation program. The IJPB benefits from the support of the Labex Saclay Plant Sciences-SPS (ANR-10-LABX-0040-SPS). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Cell Biology
                Cellular Structures and Organelles
                Cell Walls
                Plant Cell Walls
                Biology and Life Sciences
                Cell Biology
                Cellular Types
                Plant Cells
                Plant Cell Walls
                Biology and Life Sciences
                Cell Biology
                Plant Cell Biology
                Plant Cells
                Plant Cell Walls
                Biology and Life Sciences
                Plant Science
                Plant Cell Biology
                Plant Cells
                Plant Cell Walls
                Physical Sciences
                Chemistry
                Chemical Compounds
                Organic Compounds
                Cellulose
                Physical Sciences
                Chemistry
                Organic Chemistry
                Organic Compounds
                Cellulose
                Research and Analysis Methods
                Experimental Organism Systems
                Model Organisms
                Arabidopsis Thaliana
                Research and Analysis Methods
                Model Organisms
                Arabidopsis Thaliana
                Biology and Life Sciences
                Organisms
                Plants
                Brassica
                Arabidopsis Thaliana
                Research and Analysis Methods
                Experimental Organism Systems
                Plant and Algal Models
                Arabidopsis Thaliana
                Biology and Life Sciences
                Organisms
                Plants
                Seedlings
                Biology and Life Sciences
                Biochemistry
                Biosynthesis
                Biology and Life Sciences
                Developmental Biology
                Plant Growth and Development
                Root Growth
                Biology and Life Sciences
                Plant Science
                Plant Growth and Development
                Root Growth
                Biology and Life Sciences
                Genetics
                Gene Expression
                Biology and Life Sciences
                Molecular Biology
                Molecular Biology Techniques
                Marker Genes
                Research and Analysis Methods
                Molecular Biology Techniques
                Marker Genes
                Custom metadata
                vor-update-to-uncorrected-proof
                2017-06-26
                All relevant data are within the paper and its Supporting Information files.

                Genetics
                Genetics

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