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VOLUMESEVENTYSEVEN A DVANCES IN BOTANICAL RESEARCH Nitric Oxide and Signaling in Plants ADVANCES IN BOTANICAL RESEARCH Series Editors Jean-PierreJacquot Professor,MembredeL’InstitutUniversitairedeFrance,UnitéMixtedeRecherche INRA,UHP1136“InteractionArbresMicroorganismes”,UniversitédeLorraine, FacultédesSciences,Vandoeuvre,France PierreGadal HonoraryProfessor,UniversitéParis-SudXI,InstitutBiologiedesPlantes,Orsay,France VOLUME SEVENTY SEVEN A DVANCES IN BOTANICAL RESEARCH Nitric Oxide and Signaling in Plants Volume Editor DAVID WENDEHENNE University of Bourgogne Franche-Comté, UMR 1347 Agroécologie, Dijon, France AMSTERDAM(cid:129)BOSTON(cid:129)HEIDELBERG(cid:129)LONDON NEWYORK(cid:129)OXFORD(cid:129)PARIS(cid:129)SANDIEGO SANFRANCISCO(cid:129)SINGAPORE(cid:129)SYDNEY(cid:129)TOKYO AcademicPressisanimprintofElsevier AcademicPressisanimprintofElsevier 125LondonWall,LondonEC2Y5AS,UK TheBoulevard,LangfordLane,Kidlington,OxfordOX51GB,UK 50HampshireStreet,5thFloor,Cambridge,MA02139,USA 525BStreet,Suite1800,SanDiego,CA92101-4495,USA Firstedition2016 Copyright(cid:1)2016ElsevierLtd.Allrightsreserved. Nopartofthispublicationmaybereproducedortransmittedinanyformorbyanymeans, electronicormechanical,includingphotocopying,recording,oranyinformationstorageand retrievalsystem,withoutpermissioninwritingfromthepublisher.Detailsonhowtoseek permission,furtherinformationaboutthePublisher’spermissionspoliciesandour arrangementswithorganizationssuchastheCopyrightClearanceCenterandtheCopyright LicensingAgency,canbefoundatourwebsite:www.elsevier.com/permissions. Thisbookandtheindividualcontributionscontainedinitareprotectedundercopyrightby thePublisher(otherthanasmaybenotedherein). Notices Knowledgeandbestpracticeinthisfieldareconstantlychanging.Asnewresearchand experiencebroadenourunderstanding,changesinresearchmethods,professionalpractices, ormedicaltreatmentmaybecomenecessary. Practitionersandresearchersmustalwaysrelyontheirownexperienceandknowledgein evaluatingandusinganyinformation,methods,compounds,orexperimentsdescribed herein.Inusingsuchinformationormethodstheyshouldbemindfuloftheirownsafetyand thesafetyofothers,includingpartiesforwhomtheyhaveaprofessionalresponsibility. Tothefullestextentofthelaw,neitherthePublishernortheauthors,contributors,oreditors, assumeanyliabilityforanyinjuryand/ordamagetopersonsorpropertyasamatterof productsliability,negligenceorotherwise,orfromanyuseoroperationofanymethods, products,instructions,orideascontainedinthematerialherein. ISBN:978-0-12-801074-7 ISSN:0065-2296 ForinformationonallAcademicPresspublications visitourwebsiteathttp://store.elsevier.com CONTRIBUTORS AlexandraAgeeva HelmholtzZentrumMu€nchen–GermanResearchCenterforEnvironmentalHealth, InstituteofBiochemicalPlantPathology,Mu€nchen-Neuherberg,Germany MagdalenaArasimowicz-Jelonek DepartmentofPlantEcophysiology,FacultyofBiology,AdamMickiewiczUniversity, Poznan(cid:2),Poland JuanB.Barroso GroupofBiochemistryandCellSignalinginNitricOxide,DepartmentofBiochemistryand MolecularBiology,UniversityofJaén,Jaén,Spain JuanC.Begara-Morales GroupofBiochemistryandCellSignalinginNitricOxide,DepartmentofBiochemistryand MolecularBiology,UniversityofJaén,Jaén,Spain DianaBellin DipartimentodiBiotecnologie,Universit(cid:3)adegliStudidiVerona,Verona,Italy GeraldA.Berkowitz DepartmentofPlantScienceandLandscapeArchitecture,UniversityofConnecticut,Storrs, CT,USA AlexandreBoscari InstitutSophiaAgrobiotech(ISA),INRA,CNRS,UniversitéNiceSophiaAntipolis,Sophia Antipolis,France RenaudBrouquisse InstitutSophiaAgrobiotech(ISA),INRA,CNRS,UniversitéNiceSophiaAntipolis,Sophia Antipolis,France ClaudeBruand LaboratoiredesInteractionsPlantes-Microorganismes(LIPM),INRA,CNRS, Castanet-Tolosan,France MouniraChaki GroupofBiochemistryandCellSignalinginNitricOxide,DepartmentofBiochemistryand MolecularBiology,UniversityofJaén,Jaén,Spain FranciscoJ.Corpas GroupofAntioxidants,FreeRadicalsandNitricOxideinBiotechnology,Foodand Agriculture,DepartmentofBiochemistry,CellandMolecularBiologyofPlants,Estacio(cid:2)n ExperimentaldelZaidín,CSIC,Granada,Spain NataliaCorrea-Aragunde InstitutodeInvestigacionesBiolo(cid:2)gicas,ConsejoNacionaldeInvestigacionesCientíficasy Técnicas(CONICET),UniversidadNacionaldeMardelPlata(UNMdP),MardelPlata, Argentina j xi xii Contributors LauraDeGara CentroIntegratodiRicerca,Universit(cid:3)aCampusBio-MedicodiRoma,Rome,Italy MariaConcettadePinto DipartimentodiBiologia,Universit(cid:3)adegliStudidiBari“AldoMoro”,Bari,Italy MassimoDelledonne DipartimentodiBiotecnologie,Universit(cid:3)adegliStudidiVerona,Verona,Italy ZuzanaDr(cid:2)abkov(cid:2)aTrojanov(cid:2)a DepartmentofBotany,FacultyofScience,PalackýUniversityinOlomouc,Olomouc, CzechRepublic JolantaFloryszak-Wieczorek DepartmentofPlantPhysiology,Poznan(cid:2)UniversityofLifeSciences,Poznan(cid:2),Poland NoeliaForesi InstitutodeInvestigacionesBiolo(cid:2)gicas,ConsejoNacionaldeInvestigacionesCientíficasy Técnicas(CONICET),UniversidadNacionaldeMardelPlata(UNMdP),MardelPlata, Argentina PierreFrendo InstitutSophiaAgrobiotech(ISA),INRA,CNRS,UniversitéNiceSophiaAntipolis,Sophia Antipolis,France LucasFrungillo DepartmentofPlantBiology,InstituteofBiology,UniversityofCampinas,Campinas/SP, Brazil AlokKumarGupta NationalInstituteofPlantGenomeResearch,NewDelhi,India KapugantiJ.Gupta NationalInstituteofPlantGenomeResearch,NewDelhi,India JohnT.Hancock FacultyofHealthandAppliedSciences,UniversityoftheWestofEngland,Bristol,UK Im(cid:3)eneHichri InstitutSophiaAgrobiotech(ISA),INRA,CNRS,UniversitéNiceSophiaAntipolis,Sophia Antipolis,France ZahraImanifard DipartimentodiBiotecnologie,Universit(cid:3)adegliStudidiVerona,Verona,Italy KarolinaIzbian(cid:2)ska DepartmentofPlantEcophysiology,FacultyofBiology,AdamMickiewiczUniversity, Poznan(cid:2),Poland AardraKachroo DepartmentofPlantPathology,UniversityofKentucky,Lexington,KY,USA Contributors xiii PradeepKachroo DepartmentofPlantPathology,UniversityofKentucky,Lexington,KY,USA Eva-EstherKo€nig HelmholtzZentrumMu€nchen–GermanResearchCenterforEnvironmentalHealth, InstituteofBiochemicalPlantPathology,Mu€nchen-Neuherberg,Germany IzabellaKovacs HelmholtzZentrumMu€nchen–GermanResearchCenterforEnvironmentalHealth, InstituteofBiochemicalPlantPathology,Mu€nchen-Neuherberg,Germany LucieKubienov(cid:2)a DepartmentofBiochemistry,FacultyofScience,PalackýUniversityinOlomouc,Olomouc, CzechRepublic AprajitaKumari NationalInstituteofPlantGenomeResearch,NewDelhi,India LorenzoLamattina InstitutodeInvestigacionesBiolo(cid:2)gicas,ConsejoNacionaldeInvestigacionesCientíficasy Técnicas(CONICET),UniversidadNacionaldeMardelPlata(UNMdP),MardelPlata, Argentina Ale(cid:4)sLebeda DepartmentofBotany,FacultyofScience,PalackýUniversityinOlomouc,Olomouc, CzechRepublic Gah-HyunLim DepartmentofPlantPathology,UniversityofKentucky,Lexington,KY,USA ChristianLindermayr HelmholtzZentrumMu€nchen–GermanResearchCenterforEnvironmentalHealth, InstituteofBiochemicalPlantPathology,Mu€nchen-Neuherberg,Germany TengfangLing DipartimentodiBiotecnologie,Universit(cid:3)adegliStudidiVerona,Verona,Italy RuitaoLiu DipartimentodiBiotecnologie,Universit(cid:3)adegliStudidiVerona,Verona,Italy VittoriaLocato CentroIntegratodiRicerca,Universit(cid:3)aCampusBio-MedicodiRoma,Rome,Italy LenkaLuhov(cid:2)a DepartmentofBiochemistry,FacultyofScience,PalackýUniversityinOlomouc,Olomouc, CzechRepublic YiMa DepartmentofPlantScienceandLandscapeArchitecture,UniversityofConnecticut,Storrs, CT,USA ElianeMeilhoc LaboratoiredesInteractionsPlantes-Microorganismes(LIPM),INRA,CNRS, Castanet-Tolosan,France xiv Contributors SonalMishra NationalInstituteofPlantGenomeResearch,NewDelhi,India AnnalisaParadiso DipartimentodiBiologia,Universit(cid:3)adegliStudidiBari“AldoMoro”,Bari,Italy MarekPet(cid:4)rivalský DepartmentofBiochemistry,FacultyofScience,PalackýUniversityinOlomouc,Olomouc, CzechRepublic MaríaC.Romero-Puertas DepartmentofBiochemistryandCellularandMolecularBiologyofPlants,Estacio(cid:2)n ExperimentaldelZaidín(CSIC),Granada,Spain WilmaSabetta Spin-offSINAGRIsrl,Universit(cid:3)adegliStudidiBari“AldoMoro”,Bari,Italy IoneSalgado DepartmentofPlantBiology,InstituteofBiology,UniversityofCampinas,Campinas/SP, Brazil BeatrizS(cid:2)anchez-Calvo GroupofBiochemistryandCellSignalinginNitricOxide,DepartmentofBiochemistryand MolecularBiology,UniversityofJaén,Jaén,Spain LuisaM.Sandalio DepartmentofBiochemistryandCellularandMolecularBiologyofPlants,Estacio(cid:2)n ExperimentaldelZaidín(CSIC),Granada,Spain MichaelaSedl(cid:2)a(cid:4)rov(cid:2)a DepartmentofBotany,FacultyofScience,PalackýUniversityinOlomouc,Olomouc, CzechRepublic StevenH.Spoel InstituteofMolecularPlantSciences,SchoolofBiologicalSciences,Universityof Edinburgh,Edinburgh,UK RaquelValderrama GroupofBiochemistryandCellSignalinginNitricOxide,DepartmentofBiochemistryand MolecularBiology,UniversityofJaén,Jaén,Spain ElodieVandelle DipartimentodiBiotecnologie,Universit(cid:3)adegliStudidiVerona,Verona,Italy AakankshaWany NationalInstituteofPlantGenomeResearch,NewDelhi,India MatthewWhiteman UniversityofExeterMedicalSchool,UniversityofExeter,Exeter,UK PREFACE Living cells possess intricate signaling systems which play crucial roles for sensing and interacting with their environment. The complexity of these systemsisexemplifiedinhighereukaryotesinwhichphysiologicalfunctions requirecoordinatedcommunicationsbetweenorgansatthewholeorganism level. Understanding these systems is a formidable task and of fundamental importance. Deciphering cell signaling processes requires identification of the actors and resolution of their spatial and temporal dynamics of mutual and coordinated interactions. Although the elucidation of cell signaling mechanisms seems an unresolvable problem as ever more data come to hand, the discovery that nitric oxide (NO) displays signaling function in many, if not all, living organisms is considered as a major breakthrough. Nitricoxideisareactivediatomicgas.Accordingtosomeauthors,itmay have played an early role during evolution in primitive organisms by neu- tralizingozoneandbyservingasadefencemechanismagainstreactiveoxy- genspecies.Furthermore,thepossibilitythatthereleaseandsensingofNO could represent an intra- and extracellular mechanism before specialized receptors evolved has been proposed. Paradoxically, its involvement as a physiological mediator in mammals was not recognized until the mid- 1980s. Nevertheless, over the past 30years, our understanding of the role of NO in animals has been enriched by fascinating discoveries. First identi- fied as an antimicrobial effector molecule, numerous studies have high- lighted that NO is also a unique biological messenger involved in major processes including neuronal signal transmission, blood vessel dilatation andbothinnateandadaptiveimmunity.Thediscoveryoftheenzymenitric oxide synthase (NOS) catalysing its synthesis, as well as those of key mech- anisms controlling the expression of NOS and mediating NO effects has greatlyexpandedourunderstandingofitsrole.ThesearchforNOfunctions remains an active area of investigation in mammals with applications in medicine. From the end of the 1990s, NO was also revealed to be a surprisingly ubiquitoussignaling moleculein plants.Indeed,NO possessesan unusually repertoire of physiological functions in plants. It is involved in all major physiological processes such as seed dormancy and germination, root growth,stomatalclosure,flowering,ironhomoeostasis,hormonalsignaling, senescence and contributes to immunity as well as to the adaptive response to abiotic stresses. Therefore, it is not surprising that this gas has become a j xv xvi Preface dominant part of physiological, cellular and molecular biology research. Accordingly, five Plant Nitric Oxide International Meetings have been heldsince2006,andthesixthwillbeorganizedin2016inGranadainSpain. Interestingly,anessentialpartofthedatageneratedtodateindicatesthatNO isamajorcomponentofplantcellsignalingand,comparedtoanimals,there isaremarkabledegreeofsimilarityinthemolecularmechanismsunderlying itseffects.ThefieldofNOresearchinplantsisstillinitsinfancyandnumer- ous questions remain as yet unanswered or poorly answered, notably those relating to its synthesis and its basis for specificity. ThisfocussectionofAdvancesinBotanicalResearchpresentsaseriesof 14 chapters highlighting recent insights into NO in plants. We learn from these contributions that NO cooperates with other signaling compounds includinghydrogensulphideandreactiveoxygenspecies,notablythesuper- oxide anion and hydrogen peroxide. As mentioned by J. Hancock and M. Whiteman (Chapter 1), these interactions might be viewed as an inter- active and complex web of reactive species determining cellular responses. Other authors illustrate the importance of such interplay in root growth and developmental processes (N. Correa-Aragunde et al., Chapter 3), in programmed cell death (V. Locato et al., Chapter 9), in the establishment of symbiosis (I. Hichri et al. Chapter 10) and in immunity (E. Vandelle et al., Chapter 11; P. Kachroo et al., Chapter 12). In addition to the reactive species, crosstalk also operates between NO and hormones, lipids and the second messengers Ca2+ and cyclic GMP. Examples of the occurrence of such crosstalk in auxin signaling and plant immunity are provided by N. Correa-Aragunde et al. (Chapter 3), P. Kachroo et al. (Chapter 12) and Y. Ma and G. Berkowitz (Chapter 14). Anothermainissuediscussedinthesechaptersconcernsthespecificityof NOaction.ItappearsthatthespecificityofNOsignalingispartlygoverned byitsabilitytomodulatetheactivityoftargetproteinsthroughposttransla- tional modification (PTM) including S-nitrosylation and tyrosine nitration. These NO-dependent PTMs play a fundamental role in the regulation of gene expression (I. Kovacs et al., Chapter 2), auxin signaling (N. Correa- Aragunde et al., Chapter 3), nitrogen assimilation (L. Frungillo et al., Chapter4),responsestoabioticstresses(F.Corpasetal.,Chapter5)includ- ingcadmiumexposure(M.Arasimowicz-Jeloneketal.,Chapter6),metab- olism (M. C. Romero-Puertas and L. Sandalio, Chapter 7; A. K. Gupta etal.,Chapter8),programmedcelldeath(V.Locatoetal.,Chapter9),sym- biosisandimmunity(I.Hichrietal.Chapter10;E.Vandelleetal.,Chapter 11; Y. Ma and G. Berkowitz, Chapter 14). Importantly, NO-dependent

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