R2R3-MYB
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LiandLuBMCGenomics2014,15:277
http://wendang.chazidian.com/1471-2164/15/277
Genome-widecharacterizationandcomparativeanalysisofR2R3-MYBtranscriptionfactorsshowsthecomplexityofMYB-associatedregulatorynetworksinSalviamiltiorrhiza
CailiLiandShanfaLu*
Background
Salviaischaracterizedwithonlytwostamensconnectedtoformalever.Itincludesabout900speciesandisthelargestgenusoftheLabiataefamily.Salvia,togetherwiththegeneraLepechinia,Melissa,Dorystaechas,Meriandra,Zhumeria,PerovskiaandRosmarinus,formsamonophy-lecticlineagewithintheLabiatae[1,2].S.miltiorrhizaBunge,knownasDansheninChinese,isaneconomicallyimportantmedicinalplantspeciesoftheSalviagenus.ItshowsclosephylogeneticrelationshipswithotherAsianandMediterraneanspeciesintheSalviagenus,suchasS.roborowskiiandS.glutinosa[2].S.miltiorrhizahasbeen
*Correspondence:sflu@http://wendang.chazidian.com
InstituteofMedicinalPlantDevelopment,ChineseAcademyofMedicalSciences&PekingUnionMedicalCollege,No.151,MalianwaNorthRoad,HaidianDistrict,Beijing100193,
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widelyandsuccessfullyusedintraditionalChinesemedi-cine(TCM)forhundredofyearstotreatnumerousdis-eases,suchascoronaryheartdiseases,dysmenorrheal,amenorrhoea,andinflammatorydiseases[3,4].ThemainbioactivecomponentsofS.miltiorrhizamaybedividedintotwogroups.Thefirstgroupisabietanetype-diterpenequin-inepigments,knownastanshinones,whicharelipophilicandconsistofmorethanthirtycompounds[5].Thesecondgroupishydrophilicphenolicacids,includingrosmarinicacid,salvianolicacidA,salvianolicacidB,lithospermicacid,andmanyotherchemicals[6].Biosynthesisofmainbio-activecomponentsinS.miltiorrhizarequiresthecoordin-ationofaseriesofkeyenzymes[7].Theexpressionofgenesencodingthesekeyenzymesisregulatedbyvarioustranscriptionfactors,ofwhichMYBsappeartoplaysignifi-cantroles[8,9].IdentificationandcharacterizationofMYB
©2014LiandLu;licenseeBioMedCentralLtd.ThisisanOpenAccessarticledistributedunderthetermsoftheCreativeCommonsAttributionLicense(http://wendang.chazidian.com/licenses/by/2.0),whichpermitsunrestricteduse,distribution,andreproductioninanymedium,providedtheoriginalworkisproperlycredited.
LiandLuBMCGenomics2014,15:277
http://wendang.chazidian.com/1471-2164/15/277
genesinS.miltiorrhizaisveryimportantinunderstandingtheregulatorymechanismofbioactivecomponentbiosyn-thesis.SinceMYBsarealsovitalregulatorsinplantdevel-opmentandplantresponsestovariousbioticandabioticstresses,elucidationofMYB-associatedregulatorynet-worksmaygreatlyhelpinimprovingthegrowthanddefenseabilitiesofS.miltiorrhizathroughgeneticengin-eeringapproaches.
MYBproteins,characterizedbytheMYBdomain,havebeenwidelyfoundinmanyorganisms,includinganimals,fungiandplants.TheMYBdomainofMYBproteinsisdeeplyconservedandcontainsuptofourimperfectrepeats(R)ofabout52aminoacids[10].ManyvertebratescontainthreeMYBgenes,knownasc-MYB,A-MYBandB-MYB[11].Therepeatsinc-MYBproteinsarereferredtoasR1,R2andR3.RepeatsfromotherproteinsarenamedbasedontheirsimilaritytoR1,R2orR3ofc-MYBproteins[10,12].Inplants,MYBisthelargesttranscriptionfactorfamilyandmaybeclassifiedintofoursubfamiliesbasedonthenumberofadjacentimperfectrepeats[10,13].ItincludesR1R2R3R1/2-MYBs(4R-MYBs),R1R2R3-MYBs(3R-MYBs),R2R3-MYBsandMYBswithasingleorpartialMYBrepeat(1R-MYBorMYB-related),ofwhichR2R3-MYBisthelar-gestsubfamilyofplantMYBs[10].ThenumberofR2R3-MYBgenesinArabidopsisthaliana,PopulustrichocarpaandOryzasativais137,198,and95,respectively[13].
R2R3-MYBproteinscontaintworepeatssimilartoR2andR3ofc-MYBproteinsandhavebeenproposedtobeevolvedfroma3R-MYBgeneancestorbythelossofR1[14].InadditiontotheMYBdomain,otherlessconservedmotifswerealsofoundinR2R3-MYBproteins.BasedonthesimilarityofthesemotifsorphylogeneticrelationshipsofMYBaminoacids,R2R3-MYBsmaybedividedintosubgroups.Forinstance,thelargeArabidopsisR2R3-MYBsubfamilyhasbeendividedinto25subgroupsaccordingtothemotifs[10,12].However,basedonphylogeneticre-lationships,thenumberofR2R3-MYBsubgroupsinAra-bidopsis,P.trichocarpa,soybeanandmaizeis40,42,48,and18,respectively[15-17].ItsuggeststhattheresultingnumberofR2R3-MYBsubgroupsinArabidopsissignifi-cantlyvariesbetweentwoapproachesusedandshowsthatsomesubgroupsarenotdeeplyconservedamongdifferentplantspecies.Proteinsinnon-conservedsubgroupsmighthavespecializedroles.
ThefunctionsofnumerousR2R3-MYBshavebeencharacterizedinArabidopsis.Theknownfunctionswerewell-summarizedintofourplant-specificprocesses,in-cludingprimaryandsecondarymetabolism,cellfateandidentity,developmentalprocessesandresponsestobioticandabioticstresses[10].ItclearlydemonstratesfunctionaldivergenceandsignificanceofArabidopsisR2R3-MYBs.ExtensivestudiesontheMYBgenefamilyhavebeencon-ductedinvariousplantspecies,suchasrice,maize,wheat,poplar,eucalyptusandgentian[18-23].Theresultsshowed
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thatthefunctionsofR2R3-MYBsbelongingtothesamesubgroupwereusuallyconservedamongdifferentplantspecies.Forinstance,subgroup7MYBs,includingArabi-dopsisAtMYB11,AtMYB12andAtMYB111[24],grapeVvMYBF1[25],tomatoSlMYB12[26],gentianGtMYBP3andGtMYBP4[27],andmanyothers,areinvolvedinthecontrolofflavonolbiosynthesis.Subgroup6MYBs,suchasArabidopsisAtMYB75/PAP1,AtMYB90/PAP2,AtMYB113andAtMYB114[28],cauliflowerBoMYB2[29],appleMYB110a[30],andpearPyMYB10[31],regulateanthocya-ninbiosynthesis.ItsuggeststhatthefunctionsofMYBsmaybepredictedbyphylogeneticanalysis.Sofar,littleisknownaboutMYBsinS.miltiorrhiza.
S.miltiorrhizaisemergingasamodelplantforTCMstudies,sinceitsrelativelysmallgenomesize(~600Mb),shortlifecycle,undemandinggrowthrequirements,andsignificantmedicinalvalue[7].Recently,thegenomeofS.miltiorrhizahasbeensequencedandaworkingdraftofthegenomehasbeenassembled(Chenetal.,unpublished).InordertoelucidatetheroleofMYBgenesinS.miltiorrhizadevelopment,defenseandbioactivecomponentbiosyn-thesis,weperformedagenome-wideanalysisoftheR2R3-MYBgenesubfamilyinS.miltiorrhiza.
Resultsanddiscussion
Identificationof110S.miltiorrhizaR2R3-MYBgenes
ThroughBLASTanalysisof125A.thalianaR2R3-MYBs[12]againstthecurrentassemblyoftheS.miltiorrhizagen-ome(Chenetal.,unpublished)andsubsequentgenepredic-tionoftheretrievedgenomicDNAsequences,atotalof110full-lengthornearfull-lengthmembersoftheS.miltiorrhizaR2R3-MYBgenesubfamilywerepredicted.Notably,itmaynotbeacompletesetofR2R3-MYBgenesinS.miltiorrhiza,sincethecurrentassemblyoftheS.miltiorrhizagenomeisjustaworkingdraftandwedoidentifiedfromthecurrentassemblysomepartialsequenceswithhighhomologytoknownR2R3-MYBsinotherplantspecies(datanotshown).Toverifytheresultsfromcomputationalprediction,primersweredesignedforPCR-amplificationoffull-lengthcodingsequences(CDSs)of110S.miltiorrhizaR2R3-MYBs.Atotalof109CDSswereobtained.SequencecomparisonshowedthattheclonedCDSsof102R2R3-MYBswereidenticaltothepredictedsequences.TheothersevenclonedCDSs,includingthoseofSmMYB1,SmMYB13,SmMYB16,SmMYB35,SmMYB62,SmMYB63andSmMYB79,differedfromthepredictedonesbyoneorafewbasesonly;How-ever,thededucedaminoacidswereidentical.TheresultsconfirmthecorrectnessofMYBgeneannotationandsug-gestthereliabilityofDNAsequencedata.WewerenotabletoclonetheCDSofSmMYB108.Itcouldbeduetolowexpressionlevelinthetissuesanalyzed.All109clonedCDSsandthepredictedSmMYB108havebeensubmittedtoGenBank.TheaccessionnumbersinGenBankareshowninAdditionalfile1:TableS1.
LiandLuBMCGenomics2014,15:277
http://wendang.chazidian.com/1471-2164/15/277
Page3of12
PhylogeneticanalysisofR2R3-MYBproteinsfromS.miltiorrhizaandArabidopsis
ConservationanddivergenceofMYBdomain
InordertoknowtherelationshipofR2R3-MYBsinS.mil-tiorrhizaandArabidopsis,aneighbor-joining(NJ)phylo-genetictreewasconstructedusingMEGA4.0(Figure1).TheresultsshowedthatmanyS.miltiorrhizaMYBswerehighlysimilartotheircounterpartsinArabidopsis.BasedonthephylogenetictreeandpreviousresultsfromArabi-dopsis[10],R2R3-MYBsinS.miltiorrhizaandArabidopsismightbeclassifiedinto37subgroups(namedS1–S37),ofwhichS1–S25werenamedaspreviouslydescribed[10];whiletheotherswerenovel.Thirtyoneof34subgroupsincludedproteinsfromS.miltiorrhizaandArabidopsis,whereastheothersixwerespecifictoS.miltiorrhiza(S29andS36)orArabidopsis(S10,S12,S35andS37).Species-specificsubgroupsofR2R3-MYBshavealsobeenfoundinotherplantspecies,suchasrice[16],maize[17]andwheat[32].SinceMYBsinasubgroupusuallyplaysimilarrolesorfunctioninametabolicpathway[10],ourresultsindi-catethatsomeMYBsplaydeeplyconservedrolesinS.miltiorrhizaandArabidopsis,whiletheothersmayexhibitspecies-specializedfunctions.
TheMYBdomainofMYBproteinsishighlyconservedinplants.Itcontainsuptofourimperfectrepeats(R)ofabout52aminoacids[10].R2R3-MYBsarecharacterizedwithtworepeats,knownasR2andR3.Consistently,theMYBdomainofS.miltiorrhizaandArabidopsisR2R3-MYBscontain107residues,ofwhich54formR2,whiletheother53constituteR3(Figure2).InordertoelucidatesequencefeaturesofMYBdomainandthedegreeofcon-servationofeachresidue,multiplesequencealignmentwasperformedandsequencelogoswerecreatedforR2andR3ofR2R3-MYBsfromS.miltiorrhizaandArabidop-sis(Figure2).TheresultsshowedthatthedistributionofresiduesinR2andR3ofS.miltiorrhizaR2R3-MYBswasquitesimilartoArabidopsis(Figure2BandFigure2D).R2ofbothS.miltiorrhizaandArabidopsisR2R3-MYBscon-tainsthreehighlyconservedtryptophanresidues(W)atpositions5,26and46(Figure2AandFigure2B),whichmayformatryptophanclusterinthe3-dimensionalHTHstructureandplaysignificantrolesinMYB-DNAinter-action[15,17].Similarly,threeregularlyspacedandhighlyconservedresidues,includingaphenylalanine(F)and
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LiandLuBMCGenomics2014,15:277
http://wendang.chazidian.com/1471-2164/15/277Page4of12
tryptophanresidues,existatpositions5,24and43ofR3
(Figure2CandFigure2D).Thehighlyconservedtrypto-
phanresidueswerealsofoundinR2R3-MYBsfromother
plantspecies,suchasPopulustrichocarpa[15]andsoy-
bean[16].Althoughthephenylalanineatposition5ofR3
isconservedinR2R3-MYBsfromS.miltiorrhiza,Arabi-
dopsis,andotherplantspecies,suchasP.trichocarpa[15]
andsoybean[16],thedegreeofconservationisapparently
lesscomparedwiththetryptophanresiduesatpositions
24and43(Figure2CandFigure2D).Thefunctionalsignificanceofphenylalanineatposition5ofR3remainstobeelucidated.TheotherconservedresiduesinR2andR3weremainlydistributedbetweenthesecondandthethirdresiduesofthreeconservedresiduesdescribedabove(Figure2).TheresiduesbetweenthefirstandthesecondconservedtryptophaninR2andthosebetweenthecon-servedphenylalanineandthefirstconservedtryptophaninR3,particularlytheresiduesformingthefirsthelixineachrepeat,areapparentlylessconserved(Figure2).The3’regionofR2inbothS.miltiorrhizaand
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LiandLuBMCGenomics2014,15:277
http://wendang.chazidian.com/1471-2164/15/277
Page5of12
R2R3-MYBscontainsahighlyconservedLRPDmotif(LRPD),whichwasalsoobservedinP.trichocarpa[15],soybean[16]andmaize[17].Theresultssuggestthecon-servationofaminoaciddistributionintheMYBdomainofplantR2R3-MYBs.Ontheotherhand,thepatternsatpositions15,22–25,28and36ofR2and26,29,30and52ofR3aredifferentbetweenS.miltiorrhizaandArabidopsis(Figure2),showingdivergenceoftheMYBdomain.
AnalysisofconservedmotifsotherthantheMYBdomainArabidopsisR2R3-MYBsbelongingtoasubgroup.ThemajorityofmotifswerefoundinmorethanonesubgroupofR2R3-MYBs,exceptmotifs8and29existinginS1andmotif18inS18.Forinstance,motifs21and26widelyexistinR2R3-MYBsbelongingto16and15subgroups,respect-ively(Additionalfile2:FigureS1).Takentogether,there-sultssuggestthatthesemotifsareevolutionarilyconservedandfunctionallyimportant;however,itiscurrentlyun-knownfortheunderlyingmechanismofmotifstobeunderselectionandconservedamongdivergentspecies.
ExpressionprofilingofS.miltiorrhizaR2R3-MYBgenes
IthasbeenshownthattheC-terminalregionnexttotheMYBdomainofR2R3-MYBsusuallycontainsfunction-allyimportantmotifs,althoughthesemotifsarelesscon-servedcomparedwiththeMYBdomain[10,http://wendang.chazidian.comingtheMEMEsuite,atotalof40motifswereidentifiedinthedownstreamofMYBdomainofS.miltiorrhizaandArabidopsisR2R3-MYBs(Figure3andAdditionalfile2:FigureS1).Thelengthofmotifsvariesfrom8to107aminoacidsandthenumberofmotifsineachMYBvar-iesbetween0and6.Nomotifswerepredictedfor14SmMYBsand10AtMYBs.Althoughthemajorityof40motifsexistinbothS.miltiorrhizaandArabidopsisR2R3-MYBs,five(motifs11,22,23,36and38)areAtMYB-specific(Figure4).NoSmMYB-specificmotifswereidentified.Among40motifs,motif1isthemostcommonmotif,whichwasfoundin25AtMYBsand23SmMYBs.Thenextcommonmotifsaremotifs26and32presentin17AtMYBs/14SmMYBsand18AtMYBs/12SmMYBs,respectively.ManyS.miltiorrhizaR2R3-MYBsinasubgroupshareatleastamotif.Consistently,manyArabidoopsisR2R3-MYBsinasubgroupcontainsamemotif(s)astheirS.miltiorrhizaorthologuesinthesubgroup(Additionalfile2:FigureS1)[10,12].Itsug-geststheconservationofmotifsinS.miltiorrhizaand
InordertoelucidatepossiblerolesofR2R3-MYBsinthegrowthanddevelopmentofS.miltiorrhiza,weinvestigatedtherelativeexpressionlevelof110SmMYBsinroots,stems,leavesandflowersoftwo-year-old,fieldnursery-grownS.miltiorrhizaplantsusingthequantitativereal-timeRT-PCRmethod.Transcriptsweredetectedfor109of110SmMYBs(Figure4andAdditionalfile3:FigureS2).TheexpressionofSmMYB108wasundetected,whichisconsistentwiththeresultfromCDScloning.ItindicatesthatSmMYB108maybepseudogenesorexpressedatspe-cificdevelopmentalstagesorunderspecialconditions.Ofthe109detectableSmMYBs,31(28%)showedpredominantexpressioninleaves,17(15.5%)inflowers,12(11%)instems,and10(9%)inroots.Theother39(35.5%)werehighlyexpressedinatleasttwotissuesanalyzed(Figure5).DifferentialexpressionofSmMYBsisconsistentwiththefactthateachMYBisusuallyinvolvedinalimitednumberofcellularprocesses.
FurtherexaminationoftheexpressionofSmMYBsineachsubgroupshowedthatsomeMYBgenesinasub-groupsharedsimilarexpressionprofilesandtheprofileswereconsistentwithknownfunctionsoftheir
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