XB-ART-55947
Plant Cell
2019 Jul 01;317:1539-1562. doi: 10.1105/tpc.19.00057.
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The Ca2+ Channel CNGC19 Regulates Arabidopsis Defense Against Spodoptera Herbivory.
Meena MK
,
Prajapati R
,
Krishna D
,
Divakaran K
,
Pandey Y
,
Reichelt M
,
Mathew MK
,
Boland W
,
Mithöfer A
,
Vadassery J
.
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Cellular calcium elevation is an important signal used by plants for recognition and signaling of environmental stress. Perception of the generalist insect, Spodoptera litura, by Arabidopsis (Arabidopsis thaliana) activates cytosolic Ca2+ elevation, which triggers downstream defense. However, not all the Ca2+ channels generating the signal have been identified, nor are their modes of action known. We report on a rapidly activated, leaf vasculature- and plasma membrane-localized, CYCLIC NUCLEOTIDE GATED CHANNEL19 (CNGC19), which activates herbivory-induced Ca2+ flux and plant defense. Loss of CNGC19 function results in decreased herbivory defense. The cngc19 mutant shows aberrant and attenuated intravascular Ca2+ fluxes. CNGC19 is a Ca2+-permeable channel, as hyperpolarization of CNGC19-expressing Xenopus oocytes in the presence of both cyclic adenosine monophosphate and Ca2+ results in Ca2+ influx. Breakdown of Ca2+-based defense in cngc19 mutants leads to a decrease in herbivory-induced jasmonoyl-l-isoleucine biosynthesis and expression of JA responsive genes. The cngc19 mutants are deficient in aliphatic glucosinolate accumulation and hyperaccumulate its precursor, methionine. CNGC19 modulates aliphatic glucosinolate biosynthesis in tandem with BRANCHED-CHAIN AMINO ACID TRANSAMINASE4, which is involved in the chain elongation pathway of Met-derived glucosinolates. Furthermore, CNGC19 interacts with herbivory-induced CALMODULIN2 in planta. Together, our work reveals a key mechanistic role for the Ca2+ channel CNGC19 in the recognition of herbivory and the activation of defense signaling.
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References [+] :
Albert,
Peptides as triggers of plant defence.
2013, Pubmed
Albert, Peptides as triggers of plant defence. 2013, Pubmed
Alonso, Genome-wide insertional mutagenesis of Arabidopsis thaliana. 2003, Pubmed
Andersen, Integration of biosynthesis and long-distance transport establish organ-specific glucosinolate profiles in vegetative Arabidopsis. 2013, Pubmed , Xenbase
Angelovici, Genome-wide analysis of branched-chain amino acid levels in Arabidopsis seeds. 2013, Pubmed
Balagué, HLM1, an essential signaling component in the hypersensitive response, is a member of the cyclic nucleotide-gated channel ion channel family. 2003, Pubmed , Xenbase
Bartels, The family of Peps and their precursors in Arabidopsis: differential expression and localization but similar induction of pattern-triggered immune responses. 2013, Pubmed
Boller, A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. 2009, Pubmed
Brown, Variation of glucosinolate accumulation among different organs and developmental stages of Arabidopsis thaliana. 2003, Pubmed
Burow, The Glucosinolate Biosynthetic Gene AOP2 Mediates Feed-back Regulation of Jasmonic Acid Signaling in Arabidopsis. 2015, Pubmed
Burow, Altered glucosinolate hydrolysis in genetically engineered Arabidopsis thaliana and its influence on the larval development of Spodoptera littoralis. 2006, Pubmed
Cheng, Genomic adaptation to polyphagy and insecticides in a major East Asian noctuid pest. 2017, Pubmed
Chiasson, A quantitative hypermorphic CNGC allele confers ectopic calcium flux and impairs cellular development. 2017, Pubmed , Xenbase
Clough, Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. 1998, Pubmed
Clough, The Arabidopsis dnd1 "defense, no death" gene encodes a mutated cyclic nucleotide-gated ion channel. 2000, Pubmed
Crocoll, Optimization of Engineered Production of the Glucoraphanin Precursor Dihomomethionine in Nicotiana benthamiana. 2016, Pubmed
DeFalco, Multiple Calmodulin-Binding Sites Positively and Negatively Regulate Arabidopsis CYCLIC NUCLEOTIDE-GATED CHANNEL12. 2016, Pubmed
Demidchik, Calcium transport across plant membranes: mechanisms and functions. 2018, Pubmed
Dodd, The language of calcium signaling. 2010, Pubmed
Earley, Gateway-compatible vectors for plant functional genomics and proteomics. 2006, Pubmed
Fand, Temperature Impacts the Development and Survival of Common Cutworm (Spodoptera litura): Simulation and Visualization of Potential Population Growth in India under Warmer Temperatures through Life Cycle Modelling and Spatial Mapping. 2015, Pubmed
Fischer, An IQ domain mediates the interaction with calmodulin in a plant cyclic nucleotide-gated channel. 2013, Pubmed
Fischer, Calmodulin as a Ca2+-Sensing Subunit of Arabidopsis Cyclic Nucleotide-Gated Channel Complexes. 2017, Pubmed
Gao, Cyclic nucleotide-gated channel 18 is an essential Ca2+ channel in pollen tube tips for pollen tube guidance to ovules in Arabidopsis. 2016, Pubmed
Genger, Signaling pathways that regulate the enhanced disease resistance of Arabidopsis "defense, no death" mutants. 2008, Pubmed
Gfeller, Jasmonate controls polypeptide patterning in undamaged tissue in wounded Arabidopsis leaves. 2011, Pubmed
Grefen, The determination of protein-protein interactions by the mating-based split-ubiquitin system (mbSUS). 2009, Pubmed
Huffaker, Endogenous peptide defense signals in Arabidopsis differentially amplify signaling for the innate immune response. 2007, Pubmed
Jurkowski, Arabidopsis DND2, a second cyclic nucleotide-gated ion channel gene for which mutation causes the "defense, no death" phenotype. 2004, Pubmed
Kaplan, Cyclic nucleotide-gated channels in plants. 2007, Pubmed
Kiep, Systemic cytosolic Ca(2+) elevation is activated upon wounding and herbivory in Arabidopsis. 2015, Pubmed
Klauser, The Arabidopsis Pep-PEPR system is induced by herbivore feeding and contributes to JA-mediated plant defence against herbivory. 2015, Pubmed
Kliebenstein, Genetic control of natural variation in Arabidopsis glucosinolate accumulation. 2001, Pubmed
Knight, Calcium signalling in Arabidopsis thaliana responding to drought and salinity. 1997, Pubmed
Krol, Perception of the Arabidopsis danger signal peptide 1 involves the pattern recognition receptor AtPEPR1 and its close homologue AtPEPR2. 2010, Pubmed
Kugler, Salt-dependent regulation of a CNG channel subfamily in Arabidopsis. 2009, Pubmed
Laluk, The calmodulin-binding transcription factor SIGNAL RESPONSIVE1 is a novel regulator of glucosinolate metabolism and herbivory tolerance in Arabidopsis. 2012, Pubmed
Lan, DELLA proteins modulate Arabidopsis defences induced in response to caterpillar herbivory. 2014, Pubmed
Landoni, A loss-of-function mutation in Calmodulin2 gene affects pollen germination in Arabidopsis thaliana. 2010, Pubmed
Lee, Genome-wide identification of touch- and darkness-regulated Arabidopsis genes: a focus on calmodulin-like and XTH genes. 2005, Pubmed
Levy, Arabidopsis IQD1, a novel calmodulin-binding nuclear protein, stimulates glucosinolate accumulation and plant defense. 2005, Pubmed
Liu, Internal aluminum block of plant inward K(+) channels. 2001, Pubmed , Xenbase
Lu, AtCNGC2 is involved in jasmonic acid-induced calcium mobilization. 2016, Pubmed
Lächler, The cytosolic branched-chain aminotransferases of Arabidopsis thaliana influence methionine supply, salvage and glucosinolate metabolism. 2015, Pubmed
Ma, Linking ligand perception by PEPR pattern recognition receptors to cytosolic Ca2+ elevation and downstream immune signaling in plants. 2012, Pubmed
Maffei, Effects of feeding Spodoptera littoralis on lima bean leaves. I. Membrane potentials, intracellular calcium variations, oral secretions, and regurgitate components. 2004, Pubmed
Martin, Transient expression in Nicotiana benthamiana fluorescent marker lines provides enhanced definition of protein localization, movement and interactions in planta. 2009, Pubmed
McCormack, Handling calcium signaling: Arabidopsis CaMs and CMLs. 2005, Pubmed
McCormack, Calmodulins and related potential calcium sensors of Arabidopsis. 2003, Pubmed
Mithöfer, Plant defense against herbivores: chemical aspects. 2012, Pubmed
Mousavi, GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signalling. 2013, Pubmed
Mäser, Phylogenetic relationships within cation transporter families of Arabidopsis. 2001, Pubmed
Müller, Differential effects of indole and aliphatic glucosinolates on lepidopteran herbivores. 2010, Pubmed
Nelson, A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. 2007, Pubmed
Nguyen, Identification of cell populations necessary for leaf-to-leaf electrical signaling in a wounded plant. 2018, Pubmed
Nguyen, Emerging Jasmonate Transporters. 2017, Pubmed
Qi, Ca2+ signaling by plant Arabidopsis thaliana Pep peptides depends on AtPepR1, a receptor with guanylyl cyclase activity, and cGMP-activated Ca2+ channels. 2010, Pubmed
Rao, An improvement of the 2ˆ(-delta delta CT) method for quantitative real-time polymerase chain reaction data analysis. 2013, Pubmed
Rentel, Oxidative stress-induced calcium signaling in Arabidopsis. 2004, Pubmed
Scholz, Mutation of the Arabidopsis calmodulin-like protein CML37 deregulates the jasmonate pathway and enhances susceptibility to herbivory. 2014, Pubmed
Scholz, Evidence for GABA-Induced Systemic GABA Accumulation in Arabidopsis upon Wounding. 2017, Pubmed
Schuster, Branched-chain aminotransferase4 is part of the chain elongation pathway in the biosynthesis of methionine-derived glucosinolates in Arabidopsis. 2006, Pubmed
Seybold, Ca2+ signalling in plant immune response: from pattern recognition receptors to Ca2+ decoding mechanisms. 2014, Pubmed
Sheard, Jasmonate perception by inositol-phosphate-potentiated COI1-JAZ co-receptor. 2010, Pubmed
Shroff, Nonuniform distribution of glucosinolates in Arabidopsis thaliana leaves has important consequences for plant defense. 2008, Pubmed
Swarbreck, Plant calcium-permeable channels. 2013, Pubmed
Tan, Increased phloem transport of S-methylmethionine positively affects sulfur and nitrogen metabolism and seed development in pea plants. 2010, Pubmed
Toyota, Glutamate triggers long-distance, calcium-based plant defense signaling. 2018, Pubmed
Urquhart, The chimeric cyclic nucleotide-gated ion channel ATCNGC11/12 constitutively induces programmed cell death in a Ca2+ dependent manner. 2007, Pubmed
Vadassery, CML42-mediated calcium signaling coordinates responses to Spodoptera herbivory and abiotic stresses in Arabidopsis. 2012, Pubmed
Vadassery, Neomycin inhibition of (+)-7-iso-jasmonoyl-L-isoleucine accumulation and signaling. 2014, Pubmed
Van Poecke, Arabidopsis-insect interactions. 2007, Pubmed
Vincent, Interplay of Plasma Membrane and Vacuolar Ion Channels, Together with BAK1, Elicits Rapid Cytosolic Calcium Elevations in Arabidopsis during Aphid Feeding. 2017, Pubmed
Walter, Structural requirements of jasmonates and synthetic analogues as inducers of Ca2+ signals in the nucleus and the cytosol of plant cells. 2007, Pubmed
Wasternack, Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany. 2013, Pubmed
Wudick, CORNICHON sorting and regulation of GLR channels underlie pollen tube Ca2+ homeostasis. 2018, Pubmed
Xie, COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility. 1998, Pubmed
Yamaguchi, PEPR2 is a second receptor for the Pep1 and Pep2 peptides and contributes to defense responses in Arabidopsis. 2010, Pubmed
Yamaguchi, The cell surface leucine-rich repeat receptor for AtPep1, an endogenous peptide elicitor in Arabidopsis, is functional in transgenic tobacco cells. 2006, Pubmed
Yan, Injury Activates Ca2+/Calmodulin-Dependent Phosphorylation of JAV1-JAZ8-WRKY51 Complex for Jasmonate Biosynthesis. 2018, Pubmed
Yoshioka, Environmentally sensitive, SA-dependent defense responses in the cpr22 mutant of Arabidopsis. 2001, Pubmed
Zebelo, Role of early signalling events in plant-insect interactions. 2015, Pubmed
Zhang, N-terminal S-acylation facilitates tonoplast targeting of the calcium sensor CBL6. 2017, Pubmed
Zhang, Molecular and genetic evidence for the key role of AtCaM3 in heat-shock signal transduction in Arabidopsis. 2009, Pubmed
Zhang, Arabidopsis CNGC14 Mediates Calcium Influx Required for Tip Growth in Root Hairs. 2017, Pubmed
Zhou, A calcium-dependent protein kinase interacts with and activates a calcium channel to regulate pollen tube growth. 2014, Pubmed , Xenbase
Zimmermann, Herbivore-Triggered Electrophysiological Reactions: Candidates for Systemic Signals in Higher Plants and the Challenge of Their Identification. 2016, Pubmed
Zimmermann, System potentials, a novel electrical long-distance apoplastic signal in plants, induced by wounding. 2009, Pubmed