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      Extracellular ATP acts as a damage-associated molecular pattern (DAMP) signal in plants

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          Abstract

          As sessile organisms, plants have evolved effective mechanisms to protect themselves from environmental stresses. Damaged (i.e., wounded) plants recognize a variety of endogenous molecules as danger signals, referred to as damage-associated molecular patterns (DAMPs). ATP is among the molecules that are released by cell damage, and recent evidence suggests that ATP can serve as a DAMP. Although little studied in plants, extracellular ATP is well known for its signaling roles in animals, including acting as a DAMP during the inflammatory response and wound healing. If ATP acts outside the cell, then it is reasonable to expect that it is recognized by a plasma membrane-localized receptor. Recently, DORN1, a lectin receptor kinase, was shown to recognize extracellular ATP in Arabidopsis. DORN1 is the founding member of a new purinoceptor subfamily, P2K (P2 receptor kinase), which is plant-specific. P2K1 (DORN1) is required for ATP-induced cellular responses (e.g., cytosolic Ca 2+ elevation, MAPK phosphorylation, and gene expression). Genetic analysis of loss-of-function mutants and overexpression lines showed that P2K1 participates in the plant wound response, consistent with the role of ATP as a DAMP. In this review, we summarize past research on the roles and mechanisms of extracellular ATP signaling in plants, and discuss the direction of future research on extracellular ATP as a DAMP signal.

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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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            Cross talk in defense signaling.

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              An endogenous peptide signal in Arabidopsis activates components of the innate immune response.

              Innate immunity is initiated in animals and plants through the recognition of a variety of pathogen-associated molecules that in animals are called pathogen-associated molecular patterns and in plants are called elicitors. Some plant pathogen-derived elicitors have been identified as peptides, but peptide elicitors derived from the plant itself that activate defensive genes against pathogens have not been previously identified. Here, we report the isolation and characterization of a 23-aa peptide from Arabidopsis, called AtPep1, which activates transcription of the defensive gene defensin (PDF1.2) and activates the synthesis of H(2)O(2), both being components of the innate immune response. The peptide is derived from a 92-aa precursor encoded within a small gene that is inducible by wounding, methyl jasmonate, and ethylene. Constitutive expression of the AtPep1 precursor gene PROPEP1 in transgenic Arabidopsis plants causes a constitutive transcription of PDF1.2. When grown in soil, the transgenic plants exhibited an increased root development compared with WT plants and an enhanced resistance toward the root pathogen Pythium irregulare. Six paralogs of PROPEP1 are present in Arabidopsis, and orthologs have been identified in species of several agriculturally important plant families, where they are of interest for their possible use in crop improvement.
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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
                23 July 2014
                03 September 2014
                2014
                : 5
                : 446
                Affiliations
                [1] 1Department of Plant Pathology, Washington State University Pullman, WA, USA
                [2] 2Division of Plant Sciences and Biochemistry, Christopher S. Bond Life Sciences Center, University of Missouri Columbia, MO, USA
                Author notes

                Edited by: Martin Heil, Centro de Investigación y de Estudios Avanzados del Instituto Población Nacional – Unidad Irapuato, Mexico

                Reviewed by: Stanley Roux, The University of Texas at Austin, USA; Stephen Chivasa, Durham University, UK

                *Correspondence: Kiwamu Tanaka, Department of Plant Pathology, Washington State University, P.O. BOX 646430, Pullman, WA 99164, USA e-mail: kiwamu.tanaka@ 123456wsu.edu

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

                Article
                10.3389/fpls.2014.00446
                4153020
                25232361
                16dc42f9-e196-46ac-a090-26e129bf8c17
                Copyright © 2014 Tanaka, Choi, Cao and Stacey.

                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) or licensor 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
                : 11 July 2014
                : 19 August 2014
                Page count
                Figures: 2, Tables: 2, Equations: 0, References: 90, Pages: 9, Words: 0
                Categories
                Plant Science
                Review Article

                Plant science & Botany
                extracellular atp,damps,immune defense,wound healing,symbiosis and immunity
                Plant science & Botany
                extracellular atp, damps, immune defense, wound healing, symbiosis and immunity

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