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Calcium Signalling in Plant Biotic Interactions

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Calcium Signalling in Plant Biotic Interactions International Journal of Molecular Sciences Review Calcium Signalling in Plant Biotic Interactions Didier Aldon, Malick Mbengue ID , Christian Mazars and Jean-Philippe Galaud * Laboratoire de Recherche en Sciences Vegetales, Universite de Toulouse, CNRS, UPS, 24, Chemin de Borde-Rouge, Auzeville, BP 42617, 31326 Castanet-Tolosan, France; [email protected] (D.A.); [email protected] (M.M.); [email protected] (C.M.) * Correspondence: [email protected]; Tel.: +33-534-323-828; Fax: +33-534-323-802 Received: 26 January 2018; Accepted: 22 February 2018; Published: 27 February 2018 Abstract: Calcium (Ca2+) is a universal second messenger involved in various cellular processes, leading to plant development and to biotic and abiotic stress responses. Intracellular variation in free Ca2+ concentration is among the earliest events following the plant perception of environmental change. These Ca2+ variations differ in their spatio-temporal properties according to the nature, strength and duration of the stimulus. However, their conversion into biological responses requires Ca2+ sensors for decoding and relaying. The occurrence in plants of calmodulin (CaM) but also of other sets of plant-specific Ca2+ sensors such as calmodulin-like proteins (CMLs), Ca2+-dependent protein kinases (CDPKs) and calcineurin B-like proteins (CBLs) indicate that plants possess specific tools and machineries to convert Ca2+ signals into appropriate responses. Here, we focus on recent progress made in monitoring the generation of Ca2+ signals at the whole plant or cell level and their long distance propagation during biotic interactions. The contribution of CaM/CMLs and CDPKs in plant immune responses mounted against bacteria, fungi, viruses and insects are also presented. Keywords: biotic stress responses; calcium; calcium signature; calmodulin; CMLs; CDPKs; plant immunity; symbiosis 1. Introduction Like all living organisms, plants face environmental challenges that can be either of a biotic nature such as interactions with pathogens (e.g., bacteria, fungi, oomycetes, viruses, insects) or of an abiotic nature such as drought, soil salinity, air pollution, extreme temperatures and mechanical injury [1]. These adverse conditions often limit growth and productivity of crops worldwide. The expected global temperature elevation in the coming years and associated climate modifications are creating ever-greater challenges for agriculture [2,3]. To adapt to adverse growth conditions, plants must be able to detect the nature and strength of environmental stimuli, interpret them and activate appropriate physiological responses [3]. Among signalling elements that are involved in plant stress responses and particularly during immune responses to pathogens, reactive oxygen species (ROS) and Ca2+ ions are among the earliest actors that coordinate plant adaptive responses [4–7]. The oxidative burst was first described in 1983 following Potato infection by the oomycete Phytophtora infestans [8], whereas the importance of Ca2+ signalling in plant immunity was reported in tobacco following Pseudomonas syringae inoculation in 1990 [9]. A close connection was then established between ROS and Ca2+ signalling pathways in plant immunity [10]. In this review, we will focus on the importance of Ca2+, a ubiquitous and versatile second messenger [11], in plant biotic interactions. To become informative, the Ca2+ message needs to be decoded and relayed in order to activate the appropriate cell response and this is carried out by Ca2+-binding proteins termed Ca2+ sensors [12]. The complex spatiotemporal patterns of Ca2+ changes at cellular and tissue levels (frequency, amplitude, and distribution within the cell) are proposed to carry information and are denoted as the Ca2+ signature [13,14] (Figure1). The Ca 2+ signature encodes Int. J. Mol. Sci. 2018, 19, 665; doi:10.3390/ijms19030665 www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2018, 19, 665 2 of 19 a first layer of specificity and will be considered first, with a particular emphasis on how methods to monitor Ca2+ signatures have evolved and brought new information. Ca2+-binding proteins Int. J. Mol. Sci. 2018, 19, x FOR PEER REVIEW 2 of 19 and their downstream targets provide a second layer of specificity. Most Ca2+-binding proteins 2+ are characterizeda first layerby of specificity the presence and will in be their considered sequence first, ofwith the a particular canonical emphasis Ca -binding on how methods motif calledto the EF-hand [monitor15]. For Ca example,2+ signatures the have plant evolved model andArabidopsis brought new thaliana information.encodes Ca2+-binding at least 250proteins EF-hand-containing and their proteins [downstream16]. This number targets isprovide much a higher second than layer in of mammals specificity. and Most notably, Ca2+-binding the majority proteins of are plant Ca2+ characterized by the presence in their sequence of the canonical Ca2+-binding motif called the EF- sensors do not have homologs in others organisms [17,18]. However, only about half of them have hand [15]. For example, the plant model Arabidopsis thaliana encodes at least 250 EF-hand-containing 2+ 2+ been consideredproteins [16]. as Ca This numbersensors is [much17]. These higher plantthan in Ca mammalssensors and arenotably, classified the majority into of four plant major Ca2+ groups: 2+ the calcineurinsensors B-like do not (CBL),have homologs the Ca in-dependent others organisms protein [17,18]. kinases However, (CDPK), only about the calmodulin half of them (CaM)have group and its closelybeen considered related group, as Ca2+ thesensors Calmodulin-like [17]. These plant protein Ca2+ sensors (CML) are classified family [ 17into,19 four]. Calmodulin major groups: (CaM) is one of thethe most calcineurin studied B-like eukaryotic (CBL), the proteins Ca2+-dependent and has protein been kinases shown (CDPK), to interact the calmodulin with and modulate(CaM) the group and its closely related group, the Calmodulin-like protein (CML) family [17,19]. Calmodulin activity of numerous target proteins [20]. Plants also possess a remarkable repertoire of CaM-related (CaM) is one of the most studied eukaryotic proteins and has been shown to interact with and proteins termedmodulate CMLs the activity (7 CaM of numerous and 50 CMLstarget proteins genes in[20].Arabidopsis Plants also )possess that are a remarkable not present repertoire in animals, of as is also the caseCaM-related for CBLs proteins and termed CDPKs CMLs (ten (7 and CaM 34 and genes 50 CMLs in Arabidopsis, genes in Arabidopsis respectively)) that are not [21 present,22]. To date, the roles ofin animals, most of as these is also Ca the2+ casesensors for CBLs remain and CDPKs unknown (ten butand recent34 genes studies in Arabidopsis, have pointed respectively) out the roles 2+ for some of[21,22]. them To in date, physiological the roles of processes most of these associated Ca sensors with remain development, unknown but abiotic recent plant studies stress have responses pointed out the roles for some of them in physiological processes associated with development, and plantabiotic immunity plant stress [23–25 responses]. Here, and we plant present immunity recent [23–25]. and relevant Here, we datapresent about recent CaM, and relevant CMLs data and CDPKs and theirabout involvement CaM, CMLs in and plant CDPKs responses and their to involvement various biotic in plant stresses. responses to various biotic stresses. Figure 1.FigureKey steps 1. Key insteps Ca in2+ Casignaling2+ signaling pathways pathways during during plant plant biotic biotic interactions. interactions. Plants are Plants exposed are to exposed to diversediverse microorganisms, microorganisms, pests pests or or other other aggressorsaggressors leading leading to beneficial to beneficial or detrimental or detrimental interactions. interactions. Plant cells possess a large repertoire of sensors that allow to perceive, discriminate and transduce Plant cellsdifferent possess signals a large during repertoire plant immunity of sensors (PAM thatPs allow [Pathogen-Associated to perceive, discriminate Molecular Patterns], and transduce different signalseffectors, duringtoxins, DAMPs plant immunity[Damage-Associated (Pathogen-Associated Molecular Patterns] Molecular or HAMPs Patterns [Herbivory-Associated (PAMPs) , effectors, toxins, Damage-AssociatedMolecular Patterns]) or Molecular during the interaction Patterns (DAMPs)with mutualistic or Herbivory-Associated organisms (Nod and Myc Molecular Factors). In Patterns (HAMPs))response or during to different the interaction stimuli, the with earliest mutualistic steps rely on organisms specific cytosolic (Nod Ca2+ and Mycrises termed Factors). calcium In response to differentsignatures stimuli, occurring the earliest in the stepscytosol rely and in on organell specifices, cytosolicincluding nucleus Ca2+ rises (Section termed 2.1). These calcium calcium signatures signatures differ by their spatio-temporal properties and encode a first layer of specificity. A second occurring in the cytosol and in organelles, including nucleus (Section 2.1). These calcium signatures layer of specificity, relies on the decoding of these calcium transients (Section 3). Ca2+ binds to a differ byplethora their spatio-temporal of sensors such as calmodulin properties (CaM), and encodeCaM-like aproteins first layer (CML), of calcium-dependent specificity. A second protein layer of specificity,kinases relies (CDPK) on the that decoding activate target of these proteins calcium either
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