Nitric Oxide in Plant Growth, Development and Stress Physiology

290 Pages·2007·3.706 MB·English

by  Werner M. Kaiser, Kapuganti J. Gupta (auth.), Lorenzo Lamattina, Joseph C. Polacco (eds.)

6
Plant Cell Monographs
SeriesEditor:DavidG.Robinson
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ThePlantEndoplasmicReticulum
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ThePollenTube
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Nitric Oxide in Plant Growth,
Development and Stress Physiology
Volume Editors: Lorenzo Lamattina,Joseph C. Polacco
With39Figuresand5Tables
123
VolumeEditors:
ProfessorDr.LorenzoLamattina ProfessorJosephC.Polacco
InstitutodeInvestigacionesBiol´ogicas DepartmentofBiochemistry
FacultaddeCienciasExactasyNaturales 112SchweitzerHall
UniversidadNacionaldeMardelPlata UniversityofMissouri-Columbia
CC1245,(7600)MardelPlata Columbia,MO65211
Argentina USA
SeriesEditor:
ProfessorDr.DavidG.Robinson
Ruprecht-Karls-UniversityofHeidelberg
HeidelbergerInstituteforPlantSciences(HIP)
DepartmentCellBiology
ImNeuenheimerFeld230
D-69120Heidelberg
Germany
LibraryofCongressControlNumber:2006932400
ISSN1861-1370
ISBN-103-540-45128-5SpringerBerlinHeidelbergNewYork
ISBN-13978-3-540-45128-0SpringerBerlinHeidelbergNewYork
DOI10.1007/11563280
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Editors
LorenzoLamattina was born in Argentina, wherehestudied agronomyand
biologyandobtainedhisPh.D.fromtheUniversityofMardelPlata.Hedid
postdoctoralresearchattheInstitutdeBiologieMoleculairedesPlantes(IBMP-
CNRS) atStrasbourg,France, where he and his co-workers discovered RNA
editinginplantmitochondria.In1991,hejoinedtheInstitutodeInvestigaciones
Biologicas(IIB),attheFacultyofExactandNaturalSciences,UniversityofMar
delPlata,asprofessorofmolecularbiology.HechairedtheIIBfrom2000to2004
andsince1999hasbeendirectoroftheMolecularandIntegrativePhysiologyLab.
Hehastaughtmolecularbiologyandplantmolecularbiologytoundergraduate
andgraduatestudents.Hisresearchfocusesonpathwaysandmoleculesinvolved
innitricoxide(NO)-mediatedprocessesinplants.Initiallyfocusedonthean-
tioxidantpropertiesofNOanditsprotectionagainstthedeleteriouseffectsof
reactiveoxygenspecies(ROS),hisresearchhasrecentlydealtwiththeNOregu-
lationofstomatalclosure,adventitiousandlateralrootformationaswellasroot
hairdevelopment.Morerecently,thestudiesrelatedtotheNOinvolvementin
plantironmetabolismandtransportisfindingapplicationinseveralareas.
LorenzoLamattinaisamemberofseverallearnedsocieties.HeisaGuggenheim
Fellow(2005–2006)andheobtainedthe2006awardfromtheBungeandBorn
FoundationforhisresearchregardingNOeffectsinplantbiology.
JoePolacco, anativeofBrooklynNY,obtainedhisB.S.atCornellUniversity
andPh.D.atDukeUniversity,bothinbiochemistrywithemphasesinchem-
istryandgenetics,respectively.Aftertwoyearsasanassistantprofessoratthe
UniversidaddelValleinCali,Colombia,heheldasix-monthpostdoctoralpo-
sitionatBrookhavenNationalLaboratories,whereheenteredthefieldofplant
scienceunderthetutelageofPeterCarlson.Subsequently hespentfiveyears
asastaffgeneticistattheConnecticutAgriculturalExperimentStation–the
oldestintheU.S.andinternationallysecondonlytothatatWageningen.Since
1979hehasbeenamemberoftheBiochemistryDepartmentoftheUniversityof
Missouri-Columbia.Hehastaughtundergraduatesandintheschoolofmedicine
andgraduateschool.Heintroducedbiotechoutreachcoursesfornon-science
majors,suchas“BiotechnologyinSociety.”Hisresearchhastouchedonmi-
tochondrialfunction,lipoxygenaseroles,Nimetabolismandplantinteractions
withmethylotrophiccommensalbacteria.Themainfocusofhisresearchisthe
assimilationoffixednitrogenintheformofureidesandonmobilizationofN
reserves.Hisinterestinnitrogenmetabolismleddirectlytostudiesonnitric
oxide(NO)productionandfunctioninplants.
JoePolacco,twiceaFulbrightFellow,hasextensiveinternationalexperiencein
science.HiscollaborationwithLorenzoLamattinainvolvedafive-monthstay
inhislab,followedbyhostingDr.LamattinaasaGuggenheim Fellow.Heis
amemberofseveralscientificsocietiesandanaward-winningteacher.
Preface
Nitric oxide (NO) has definitively emerged as a ubiquitous molecule in life
anditsstudyhascontributedtoabetterknowledgeofmanymechanismsand
functions that were not well understood until very recently. NO is probably
the inorganic molecule with the best characterized influence on biological
processes. It has been proposed that at earlier stages of evolution, NO could
have acted as an antioxidant. As complexity evolved, new and specialized
antioxidant activities coevolved to detoxify reactive oxygen species (ROS).
Thus, NOwasacquiring newfunctionstocontributetothecurrentexquisite
network of cellular signaling. We now know that NO is involved in disease
resistance,abioticstress,growthanddevelopmentprocesses,celldivisionand
celldeath,nervoussystemresponses,immuneresponses,etc.
ThereareseveralsourcesofNO.However,itschemicalnatureandstructure
makeNOevenmorefascinating.NOisagas,afreeradicalwithanunpaired
electron,butwithoutcharge.ThesepropertiesenableNOtomovewithincells,
crossmembranesandberemovedefficientlybydifferentcellularcomponents.
Becauseofitsrapidmovement andremoval,thebehaviorofNOinsignaling
is optimal (Neil et al. 2003; Lamattina et al. 2003). NO is able to switch on
and switch off, in a precise manner, a number of cellular functions. NO can
also interact with other signaling molecules contributing to the generation
of amplified signaling cascades. NO behaves like a hormone. Its versatility
confers to this molecule the property of acting simultaneously in different
cellular compartments and in opposite directions. This ability is essential to
accomplishahousekeepingroleinhomeostaticcellprocessesandtoact,atthe
sametime,asasynchronizerofcellularmetabolism.
TheNOsourceinplantsconstitutesacomplexpanorama.NOcanbegener-
atedthroughenzymaticandnon-enzymaticpathways,eachofwhichisfinely
tunedandregulated(Yamasakietal.1999,Guoetal.2003,Corpasetal.2004,
Rockeletal.2002,Bethkeetal.2004).Thiscomplexitychallengesgeneticap-
proachestounravelplantNOfunctionality.InadditiontotheabilityofNOto
crosscellmembranesandhenceactat“adistance”,theintracellularlocaliza-
tionofthedifferentNOsourcesmightbelinkedtodifferenttargetsandtothe
regulationofdifferentphysiologicalprocesses.
NoDNAsequence hasbeenfoundtobindNOdirectly.However,microar-
rays,northernblotsandAFLPanalyseshaverevealedthatNOisimplicatedin
VIII Preface
theregulationofthelevelofnumeroustranscriptsinArabidopsis.Theresults
indicatethatNO-regulatedgenesareinvolvedineveryaspectofplantgrowth
anddevelopment,aswellasinstressresponses(Polverarietal.2003,Paraniet
al.2004,Heetal.2005).Inaddition,post-translationalmodificationsinduced
byNOthroughS-nitrosylationhaverevealedanimpressivenumberofproteins
aspotential NOtargets(Lindermayr et al. 2005). These proteins are thought
to be involved in primary and secondary cell metabolism. Furthermore, the
abilityofNOtobeoneofthecellularmessengersinvolvedintheregulationof
cytosolicCa2+concentrationwhile,nitricoxidesynthase(NOS)isitselfaCa2+-
dependent activity, make NO an excellent candidate as a signaling molecule
ineveryCa2+-modulatedcellresponse(Garcia-Mataetal.2003;Lamotteetal.
2004;Lanterietal.2006).
FigureAshowstheexponential growthinthenumber ofpapersthathave
appeared in a 10 years period (1995-2004) concerning NO action in plant
biology. In comparison to the number of papers on auxin over the same
period, it can be observed that NOis rapidly catching up thisin an exciting
eraofworldwideauxinresearch.FigureBshowsthattheratiobetweenauxin-
Preface IX
vsNO-relatedpublicationswas19infavorofauxinin1995,whereastheratio
droppedto1.4in2004.
Finally,theindustrialrevolutionanditssubsequentexponentialgrowthled
tobothenvironmentalpollutionandaparallelincreaseofNOlevels.Increased
NOlevelsinthetropospherebringaboutanaturalpressureonNO-regulated
processesinbiosphere.Wehavenoidea,atthemoment,abouttherealsignifi-
canceofthatpressureanditsevolutionaryside-effects.However,wewouldlike
tociteatleasttwoexamplesthattouchonthisquestion:(i)pharmacologistsat
theFreeUniversityofBerlinobtainedunexpected resultsinameasurements
oftheNO-regulatedguanylatecyclase(Friebeetal.1996)and(ii)treesinNew
York’sCentralParkshowedbettergrowththanthoseofneighboringruralar-
eas as aresult of NOx-mediated depletion ofurban growth-inhibiting ozone
(Gregg et al. 2003). Thus, at least these particular examples possibly corrob-
orate the popular saying “What doesn’t kill you, makes you stronger”. They
alsopointtotheneedforinteractivemolecularandecologicalapproachesto
understandtheadaptivechangesoccurringinaverydynamicequilibrium.
The revolution of genomics, proteomics and metabolomics has infused
afloodofdatainbiology.Nevertheless, basic ecological,biochemical,physi-
ologicalandcellularbiologicalapproachesarebeingrevisitedtovalidateand
integrate the voluminous bioinformatics and in silico data. This book com-
pileschapterseachofwhichprovidesabalancedtreatmentofnewresultsand
prospectsineveryfieldofNObiologyinplants,fromphysiological,biochemi-
calandmolecularpointsofview.Weintendthisbooktobeprovocative,butat
thesametime,avaluablesourceofinformationandatooltoinspirescientists
tothinkabouthowNOcouldbeavariableintheirownfieldsofplantresearch.
ConsideringthatthemajorityofthedatareportingNOactioninplantbiology
has appeared during the last 8 years, this book will be absolutely necessary
for teachers and students to update “standard” knowledge in plant biology
courses.Allthechaptersofthisvolumewerewrittenbyactivelyworkingplant
scientists. Theeditorswouldlike toexpress their gratitudefortheir valuable
contributionsandwehopethattheyspurfurtheradvancesbyyouthereader.
We are certainly embarking on a century that will bring us unexpected and
excitingdiscoveriesinvolvingNOactionsinplants.
MardelPlata,Argentina LorenzoLamattina
Columbia,MO,USA JosephC.Polacco
Finally, wewishtoremember withaffectionourdearcolleagueDr.Radomir
Konjevi´c(correspondingauthor,chapter6)whodiedonJuly22nd,2006.
X Preface
NoteaddedinProof
Durnerandcoworkers(Zemotjeletal.,2006)havecalledtoquestiontheactual
activityoftheproteinencodedbyAtNOS1.Theyhavenotbeenabletodetect
NOS activity in the recombinant protein using both an [3H]-arginine and
aGriessreagent-basedNOSassay.Crawfordandcolleagues,intheirresponseto
Durner’sletter(Crawfordetal.,2006),haveacceptedthatthenewexperiments
show no detectable citrulline in the analysis of the products produced from
[14C]-arginineinpresenceoftherecombinantAtNOS1.Moreover,theattempts
toreproducethereportedproductionofNOusingtheGriessreagenthavealso
failed.
That Atnos1 produces much less basal NO than wild type is indisputable
(Guo et al., 2003), hence the proposed renaming of the gene as NOA1 (NO-
Associated 1). However, since the molecular basis of the Atnoa1 phenotype
isunknown,itsuseasagenetictoolinmanipulatingendogenousNOisnow
strongly diminished. Science is a self-correcting mode of inquiry, and erro-
neousresultsmustbeaccepted, rapidlycommunicated tothescientific com-
munity, and then withdrawn.This new turnofevents willundoubtedly help
deterusfrommakingwrongturnsinthecontinuingquestforNOsourcesin
plants.
References
BethkePC,BadgerMR,JonesRL(2004)Apoplasticsynthesisofnitricoxidebyplanttissues.
PlantCell16:332–341
Crawford NM, Galli M, Tischner R, Heimer YM, Okamoto M, Mack A (2006) Response
toZemojteletal.:Plantnitricoxidesynthase:backtosquareone.TrendsinplantSci
(Novemberissue)
CorpasFJ,BarrosoJB,delR´ıoLA(2004c)Enzymaticsourcesofnitricoxideinplantcells–
beyondoneprotein-onefunction.NewPhytologist162:246–248
FriebeA,MalkewitzJ, SchultzG,KoeslingD(1996) Positiveeffects ofpollution?Nature
382:120
Garcia-MataC, Gay R, SokolovskiS, HillsA, LamattinaL, BlattMR (2003) Nitricoxide
regulatesK+ andCl–channelsinguardcellsthroughasubsetofabscisicacid-evoked
signalingpathways.ProcNatlAcadSciUSA100:11116–11121
GreggJW,JonesCG,DawsonTE(2003)Urbanizationeffectsontreegrowthinthevicinity
ofNewYorkCity.Nature424:183–187
GuoFQ,OkamotoM,CrawfordNM(2003)Identificationofaplantnitricoxidesynthase
geneinvolvedinhormonalsignaling.Science302:100–103
He J-M, Xu H, She X-P, Song X-G, ZhaoW-M (2005) Theroleand theinterrelationship
ofhydrogenperoxideandnitricoxideintheUV-B-inducedstomatalclosureinbroad
bean.FunctionPlantBiol32:237–247
LamattinaL,Garcia-MataC,GrazianoM,PagnussatG(2003)Nitricoxide:Theversatility
ofanextensivesignalmolecule.AnnRevPlantBiol54:109–136
LamotteO,GouldK,LecourieuxD,Sequeira-LegrandA,Lebrun-GarciaA,DurnerJ,Pu-
ginA,WendehenneD(2004)Analysisofnitricoxidesignalingfunctionsintobaccocells
challengedbytheelicitorcryptogein.PlantPhysiol135:516–529
Preface XI
Lanteri ML, PagnussatGC, LamattinaL(2006) Calciumand calcium-dependent protein
kinasesareinvolvedinnitricoxide-andauxin-inducedadventitiousrootformationin
cucumber.JExpBot57:1341–1351
LindermayrC,SaalbachG,DurnerJ(2005)ProteomicidentificationofS-nitrosylatedpro-
teinsinArabidopsis.PlantPhysiol137:921–930
NeillSJ,DesikanR,HancockJT(2003)Nitricoxidesignalinginplants.NewPhytol159:11–35
ParaniM,RudrabhatlaS,MyersR,WeirichH,SmithB,LeamanDW,GoldmanSL(2004)Mi-
croarrayanalysisofnitricoxideresponsivetranscriptsinArabidopsis.PlantBiotechnolJ
2:359–366
PolverariA,MolesiniB,PezzottiM,BuonaurioR,MarteM,DelledonneM(2003) Nitric
oxide-mediated transcriptional changes in Arabidopsis thaliana. Mol Plant Microbe
Interact16:1094–1105
Rockel P, Strube F, Rockel A, Wildt J, Kaiser W (2002) Regulation of nitric oxide (NO)
productionbyplantnitratereductaseinvivoandinvitro.JExpBot53:103–110
YamasakiH,SakihamaY,TakahashiS(1999)Alternativepathwayfornitricoxideproduction
inplants:newfeaturesofanoldenzyme.TrendsPlantSci4:12
Zemojtel T, Frohlich A, Palmieri MC, Kolanczyk M, Mikula I, Wyrwicz LS, Wanker EE,
MundlosS,VingronM,MartasekP,DurnerJ(2006)Plantnitricoxidesynthase:anever-
endingstory?TrendsinPlantSci(Novemberissue)