2014 annurev-arplant-Posttranslationally modified small-peptide signals in plants

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? Our comprehensive searchFurtherPosttranslationallyModi?edSmall-PeptideSignalsinPlantsYoshikatsuMatsubayashiNationalInstituteforBasicBiology,Okazaki444-8585,Japan;email:ymatsu@nibb.ac.jp

Annu. Rev. Plant Biol. 2014.65:385-413. Downloaded from http://wendang.chazidian.com

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Annu.Rev.PlantBiol.2014.65:385–http://wendang.chazidian.comThisarticle’sdoi:10.1146/annurev-arplant-050312-120122c2014byAnnualReviews.Copyright??AllrightsreservedKeywordsposttranslationalmodi?cation,secretedpeptide,proteolyticprocessing,cell-to-cellcommunication,planthormone,receptorkinaseAbstractCell-to-cellsignalingisessentialformanyprocessesinplantgrowthanddevelopment,includingcoordinationofcellularresponsestodevelopmentalandenvironmentalcues.Cumulativestudieshavedemonstratedthatpeptidesignalingplaysagreater-than-anticipatedroleinsuchintercellularcommu-nication.Somepeptidesactassignalsduringplantgrowthanddevelopment,

whereasothersareinvolvedindefenseresponsesorsymbiosis.Peptidesse-cretedassignalsoftenundergoposttranslationalmodi?cationandprote-olyticprocessingtogeneratesmallerpeptidescomposedofapproximately10aminoacidresidues.Suchposttranslationallymodi?edsmall-peptidesig-nalsconstituteoneofthelargestgroupsofsecretedpeptidesignalsinplants.Thelocationofthemodi?cationgroupincorporatedintothepeptidesbyspeci?cmodi?cationenzymesandthepeptidechainlengthde?nedbytheprocessingenzymesarecriticalforbiologicalfunctionandreceptorinterac-tion.Thisreviewcovers20yearsofresearchintoposttranslationallymodi?edsmall-peptidesignalsinplants.

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Contents

INTRODUCTION...............................................................ABRIEFHISTORYOFHOWPEPTIDESIGNALSWEREIDENTIFIED.......Bioassay-GuidedPuri?cation....................................................ClassicalGenetics..............................................................Bioinformatics..................................................................STRUCTURALCHARACTERISTICS...........................................POSTTRANSLATIONALMODIFICATIONS...................................TyrosineSulfation..............................................................ProlineHydroxylation..........................................................HydroxyprolineArabinosylation.................................................PROTEOLYTICPROCESSING.................................................STRUCTURESANDFUNCTIONSOFPOSTTRANSLATIONALLY

MODIFIEDSMALL-PEPTIDESIGNALS....................................PSK...........................................................................CLV3..........................................................................CLEFamilyPeptides...........................................................TDIF/CLE41/CLE44..........................................................CLE-RS.......................................................................CLE40.........................................................................CLE8..........................................................................CLE45.........................................................................HypSys........................................................................IDA............................................................................PSY............................................................................CEP...........................................................................RGF...........................................................................FUTUREDIRECTIONS.........................................................

386388388389390390391391391394395396396397399399400400401401401402403403404405

Annu. Rev. Plant Biol. 2014.65:385-413. Downloaded from http://wendang.chazidian.com Access provided by China Agricultural University on 01/17/15. For personal use only.

INTRODUCTION

Recentbiochemical,genetic,andbioinformaticanalyseshaverevealedthatsecretedpeptidesareimportantcell-to-cellsignalingcomponentsthatcoordinateandspecifycellularfunctionsinplants.Overthepastdecade,thetotalnumberoffunctionallycharacterizedpeptidesignalshasincreasedseveralfold(70,83,112)andnowexceedsthetotalnumberofclassicalplanthormones.Addition-ally,peptidesignalsinplantshaveproventobefunctionallyandstructurallymorediversethananticipated.Someofthesepeptidesactassignalsduringplantgrowthanddevelopment,whereasothersareinvolvedindefenseresponsesorsymbiosis.

Ingeneral,peptidescanbecategorizedintotwomajorclasses—secretedpeptidesandnon-secretedpeptides—accordingtothepropertiesoftheN-terminalleadersequences(Figure1).Cell-to-cellsignalingismediatedlargelybythesecretedsignals,butthereisalsoevidencethatnonsecretedpeptidesdirectlyreleasedfromthedamagedcellsactascell-to-cellsignalsindefenseresponsesinplants.Inrarecases,nonsecretedpeptidesencodedbyshortopenreadingframescontributetoplantdevelopmentinacell-autonomousmanner.

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Matsubayashi

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Annu. Rev. Plant Biol. 2014.65:385-413. Downloaded from http://wendang.chazidian.com Access provided by China Agricultural University on 01/17/15. For personal use only.

Acts extracellularly

Figure1

Categorizationofthepeptidesignalsinplantsintermsofstructureandsiteofaction.Thisreviewcoversposttranslationallymodi?edsmallpeptides(bluebox),butcysteine-richpeptidesandnonsecretedpeptidesarealsoknowntoactassignals.Fordetailsonindividualpeptides,seethefollowingreferences:PSK(69),CLV3(26),CLE(16),HypSys(102),IDA(6),TDIF(45),PSY(3),CEP(95),CLE-RS(98),RGF(72),LAT52(84),SCR/SP11(116,137),RALF(103),TPD1(145),EA1(64),EPF(35),LURE(100),STOMAGEN(54a,133),EC1(126),SYSTEMIN(106),AtPep1(42),ENOD40(74),ROT4/DVL(86,141),andPOLARIS(12).

Fromastructuralpointofview,secretedpeptidesignalsarefurtherdividedintotwomajorclasses:posttranslationallymodi?edsmallpeptidesandcysteine-richpeptides(Figure2).Post-translationallymodi?edsmallpeptidesarecharacterizedbythesmallsizeofmaturepeptidesandthepresenceofposttranslationalmodi?cations(65,66).Bycontrast,cysteine-richpeptidesarecharacterizedbythepresenceofanevennumberofcysteineresiduesnecessaryfortheforma-tionofintramoleculardisul?debonds.Thisreviewfocusonposttranslationallymodi?edsmallpeptides,http://wendang.chazidian.comrma-tionregardingcysteine-richpeptidesanddefense-relatednonsecretedpeptideshasbeenreviewedelsewhere(38,63,83,111,119).

Posttranslationallymodi?edsmallpeptideshavethefollowingcharacteristics:(a)theyaregenerallylessthan20aminoacidresiduesinlength,withatypicallengthofapproximately10residues;(b)theyaregeneratedbyproteolyticprocessingfromlargerpolypeptideprecursorswithanN-terminalsecretionsignalsequence;and(c)theycontainatleastoneposttranslationalmodi?cation,suchastyrosinesulfation,prolinehydroxylation,orhydroxyprolinearabinosylation(Table1).Themolecularnatureandlocationofthemodi?cationgroupincorporatedbythemodi?cationenzymesandthepeptidechainlengthde?nedbytheprocessingenzymesarecriticalforbiologicalfunctionandreceptorinteraction.Becausecomputationallypredictingthemature,biologicallyfunctionalstructuresofthesepeptidesignalsisstilldif?cult,the

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Acts intracellularly

Secretionsignalsequence:ashort(?20-amino-acid)peptidepresentattheNterminusofanewlysynthesizedpeptidedestinedfortheextracellularspace

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PropeptideXXMature peptideCCCPosttranslationallymodified small peptideCysteine-rich peptideFigure2Structuralcategorizationofsecretedpeptidesignals.Peptidesthatundergocomplexposttranslationalmodi?cationsfollowedbyproteolyticprocessingarede?nedasposttranslationallymodi?edsmallpeptides;peptidesthatundergointramoleculardisul?debondformationarede?nedascysteine-richpeptides.AdaptedfromReference66,publishedinTheArabidopsisBook(http://wendang.chazidian.com);copyright??c2011bytheAmericanSocietyofPlantBiologists.searchfornovelpeptidesignalspresentsahighlyattractivechallengeinthepostgenomicera.ABRIEFHISTORYOFHOWPEPTIDESIGNALSWEREIDENTIFIEDBioassay-GuidedPuri?cationThe?rstpeptidesignalidenti?edinplantswasatomatosystemininvolvedinthedefenseresponse,whichwasreportedin1991(106).Althoughtomatosysteminisnotasecretedpeptideanddoesnotcontainposttranslationalmodi?cations,discoveryofthispeptideinspiredplantbiologiststoiden-tifyotherbiologicallyactivepeptidesignalsinplants.Thefactthattomatosysteminwasidenti?edthroughabioassay-guidedpuri?cationprocessalsoimpressedresearcherswiththeeffectivenessofusingabiochemicalapproachtodissectthemechanismofcell-to-cellcommunication.In1996,aclassicalpuri?cationstudyledtotheidenti?cationofphytosulfokine(PSK),whichisinvolved

primarilyincellproliferation(69).PSKisthe?rstexampleofaposttranslationallymodi?edsmallpeptidediscoveredinplants.

Asearchforsystemin-likepeptidesinotherplantspeciesusingbioassay-guidedpuri?cationmethodsledtothe2001identi?cationofthehydroxyproline-richsystemin(HypSys)glycopeptidefamilyintobacco(102).Incontrasttotomatosystemin,HypSysisatypicalposttranslationallymodi?edsmallsecretedpeptide.In2006,furtherbioassay-guidedstudyidenti?edtrachearyel-ementdifferentiationinhibitoryfactor(TDIF),a12-amino-acidpeptidethatregulatesvascularstemcellfate(45).TheTDIFsequenceshowshighsimilaritytotheshortconserveddomainwithintheCLAVATA3(CLV3)/embryosurroundingregion(CLE)familypeptides.This?nd-ing,togetherwithelucidationofthestructureofmatureCLV3(describedbelow)(56,96),isareminderofhowimportantthepeptidechainlengthdeterminedbyproteolyticprocessingisforthefunctionofthistypeofpeptidesignal.

388MatsubayashiAnnu. Rev. Plant Biol. 2014.65:385-413. Downloaded from http://wendang.chazidian.com

Table1Structurallyand/orphysiologicallycharacterizedposttranslationallymodi?edsmall-peptidesignalsPeptidePSKCLV3

MaturepeptidestructureTyr(SO3H)-Ile-Tyr(SO3H)-Thr-GlnArg-Thr-Val-Hyp-Ser-Gly-[Ara3]Hyp-Asp-Pro-Leu-His-His-His

His-Glu-Val-Hyp-Ser-Gly-Hyp-Asn-Pro-Ile-Ser-Asn

Arg-Leu-Ser-Hyp-Gly-Gly-[Ara3]Hyp-Asp-Pro-Gln-His-Asn-Asn

CLEdomainoligopeptide(putative)CLEdomainoligopeptide(putative)CLEdomainoligopeptide(putative)Arg-Leu-Ser-Hyp-Gly-Gly-[Ara3]Hyp-Asp-Pro-Gln-His-HisArg-Leu-Val-Hyp-Ser-Gly-Hyp-Asn-Pro-Leu-His-Asn+Ara3,Ara4,orAra6

Arg-Gly-Ala-Asn-Leu-Pro-Hyp-Hyp-Ser-Hyp-Ala-Ser-Ser-Hyp-Hyp-Ser-Lys-Glu+Pentose9

EPIPdomainoligopeptide(putative)Asp-Tyr(SO3H)-Gly-Asp-Pro-Ser-Ala-Asn-Pro-Lys-His-Asp-Pro-Gly-Val-[Ara3]Hyp-Hyp-Ser

Asp-Phe-Arg-Hyp-Thr-Asn-Pro-Gly-Asn-Ser-Hyp-Gly-Val-Gly-HisAsp-Tyr(SO3H)-Ser-Asn-Pro-Gly-His-His-Pro-Hyp-Arg-His-Asn

Representativefunction(s)Cellularproliferationandexpansion

Regulationofthestemcellpopulationintheshootapicalmeristem

RegulationofthevascularstemcellpopulationAutoregulationofnodulationinleguminousplantsControllingstemcellfateintherootmeristemEmbryoandendospermdevelopmentPollentubegrowthUnknownUnknown

Receptor(s)PSKR1,PSKR2CLV1,CLV2,CRN/SOL2,RPK2TDR/PXYHAR1

Reference

6996

TDIF/CLE41/CLE44CLE-RS2

4599

Annu. Rev. Plant Biol. 2014.65:385-413. Downloaded from http://wendang.chazidian.com Access provided by China Agricultural University on 01/17/15. For personal use only.

CLE40CLE8CLE45CLE2CLE9

ACR4,CLV1UnknownSKM1,SKM2BindsCLV1BindsBAM1

41252096122

NtHypSysI

DefenseresponseinSolanaceaeplantsFloralorganabscissionandlateralrootemergenceCellularproliferationandexpansion

Lateralrootdevelopment?Rootstemcellnichemaintenanceand

transit-amplifyingcellproliferation

Unknown102

IDAPSY1

HAE,HSL2At1g72300?

63

CEP1RGF1

UnknownUnknown

9572

SulfatedtyrosineresiduesareindicatedasTyr(SO3H),hydroxyprolineresiduesareindicatedasHyp,andhydroxyprolineresiduesmodi?edwiththreeresiduesofarabinoseareindicatedas[Ara3]Hyp.

ClassicalGenetics

Peptidesignalshavealsobeenidenti?edusingclassicalgeneticsapproaches,althoughthishasbeenlimitedtofunctionallynonredundantpeptidegenes.CLV3,whichisinvolvedinstemcellmaintenanceintheshootapicalmeristem,wasidenti?edin1999(26),andINFLORESCENCEDEFICIENTINABSCISSION(IDA),whichregulatesorganabscission,wasidenti?edin2003(6).Themature,functionalstructureofCLV3waslaterelucidatedthroughbiochemicalanalyses(56,96),butthatofIDAremainstobedetermined.However,noadditionalpeptidesignalshavebeenidenti?edthroughclassicalgeneticssince2003,indicatingthatallnonredundantpeptidegenesthatproduceadiscerniblephenotypewhendisruptedbymutationhavebeenfullycharacterized.

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