Functional Diversification within the Family of
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FunctionalDiversificationwithintheFamilyof
B-GATATranscriptionFactorsthroughthe
Leucine-Leucine-MethionineDomain1[C][W][OPEN]
CarinaBehringer,EmmanouilBastakis,QuirinL.Ranftl,KlausF.X.Mayer,andClausSchwechheimer*
PlantSystemsBiology,TechnischeUniversitätMünchen,85354Freising,Germany(C.B.,E.B.,Q.L.R.,C.S.);and
MunichInformationCentreforProteinSequences,InstituteforBioinformaticsandSystemsBiology,Helmholtz
ZentrumMünchen,GermanResearchCenterforEnvironmentalHealth,85764Neuherberg,Germany(K.F.X.M.)
ThetranscriptionoftheArabidopsis(Arabidopsisthaliana)GATAtranscriptionfactorsGATA,NITRATE-INDUCIBLE,CARBON
METABOLISM-INVOLVED(GNC)andGNC-LIKE(GNL)/CYTOKININ-RESPONSIVEGATAFACTOR1iscontrolledby
severalgrowthregulatorysignalsincludinglightandthephytohormonesauxin,cytokinin,andgibberellin.Todate,GNCandGNL
havebeenattributedfunctionsinthecontrolofgermination,greening,floweringtime,floraldevelopment,senescence,andfloralorgan
abscission.GNCandGNLbelongtothe11-memberfamilyofB-classGATAtranscriptionfactorsthatarecharacterizedtodatesolely
bytheirhighsequenceconservationwithintheGATADNA-bindingdomain.Thedegreeoffunctionalconservationamongthevarious
B-classGATAfamilymembersisnotunderstood.Here,weidentifyandexamineB-classGATAsfromArabidopsis,tomato(Solanum
lycopersicon),Brachypodium(Brachypodiumdistachyon),andbarley(Hordeumvulgare).WefindthatB-classGATAsfromthesefour
speciescanbesubdividedbasedontheirshortorlongNterminiandthepresenceofthe13-aminoacidC-terminalleucine-leucine-
methionine(LLM)domainwiththeconservedmotifLLM.Throughoverexpressionanalysesandbycomplementationofagncgnl
doublemutant,weprovideevidencethatthelengthoftheNterminusmaynotallowdistinguishingbetweenthedifferentB-class
GATAsatthefunctionallevel.Inturn,wefindthatthepresenceandabsenceoftheLLMdomainintheoverexpressorshasdifferential
effectsonhypocotylelongation,leafshape,andpetiolelength,aswellasongeneexpression.Thus,ouranalysesidentifytheLLM
domainasanevolutionarilyconserveddomainthatdeterminesB-classGATAfactoridentityandprovidesafurthersubclassification
criterionforthistranscriptionfactorfamily.
GATAfactorsareevolutionarilyconservedtran-
scriptionalregulatorswithatypeIVzincfingerdomain
(C-X2-C-X17-20-C-X2-C)thatbindstotheconsensusDNA
sequenceWGATAR(whereWisTorAandRisGorA;
Reyesetal.,2004).WhereasGATAfactorsfromnonplant
speciesoftencontainmultipleGATAdomainswithloops
ofvariablelength,all30previouslyclassifiedGATA-like
zincfingerproteinsfromArabidopsis(Arabidopsisthaliana)
containonlyonezincfinger(http://www.arabidopsis.org;
Reyesetal.,2004).GATAfactorsfromArabidopsisand
rice(Oryzasativa)weresubdividedintofourclassesbased
ontheirsequencesimilarity,thepresenceorabsenceof
additionalrecognizableproteindomains,andtheirexon-
intronstructure(Reyesetal.,2004).ThisclassificationalsoincludesB-GATAsthatsharehighsequencesimilarities
betweentheindividualfamilymembersbutaredevoid
ofanyasyetidentifieddistinguishingsequencefeatures
outsideoftheGATADNA-bindingdomain.
Todate,fourofthe11membersoftheArabi-
dopsisB-GATAshavebeenexaminedinsomedetail:
thefunctionallyredundantGATA,NITRATE-INDUCIBLE,
CARBONMETABOLISM-INVOLVED(GNC;AtGATA21),
CYTOKININ-RESPONSIVEGATAFACTOR1/GNC-LIKE
(CGA1/GNL;AtGATA22;hithertoGNL),HANABA
TARANU(HAN;AtGATA18),andGATA23(AtGATA23).
GNCwasoriginallyidentifiedasanitrate-induciblegene
withanapparentroleinthecontrolofgreening(Bietal.,
2005;Hudsonetal.,2011;Chiangetal.,2012).TheGNC
paralogGNLwasalsodesignatedCGA1basedonits
transcriptionalregulationbycytokinin(Naitoetal.,
2007).FurtheranalysesshowedthatGNCandGNLare
functionallyredundanttranscriptionfactorswhoseex-
pressionisalsocontrolledbytheDELLAregulatorsofthe
GAsignalingpathway,thelight-labilePHYTOCHROME
INTERACTINGFACTORS,theAUXINRESPONSE
FACTORSARF2andARF7oftheauxinsignalingpath-
way,andthefloweringregulatorSUPPRESSOR-OF-
constans1(Richteretal.,2010,2013a,2013b).Moreover,
GNCandGNLwereproposedtobedirectlyrepressed
bythefloraldevelopmentregulatorsAPETALA3and
PISTILLATA,anditwassuggestedthatthisrepression
servestopreventgreeninginArabidopsispetals
(Mara1ThisworkwassupportedbygrantsfromtheDeutscheFor-
schungsgemeinschaft(nos.SCHW751/9–1andSCHW751/10–1in
theSPP1530toC.S.andno.SFB924toK.F.X.M.).
*Addresscorrespondencetoclaus.schwechheimer@wzw.tum.de.
Theauthorresponsiblefordistributionofmaterialsintegraltothe
findingspresentedinthisarticleinaccordancewiththepolicyde-
scribedintheInstructionsforAuthors(www.plantphysiol.org)is:
ClausSchwechheimer(claus.schwechheimer@wzw.tum.de).
[C]Somefiguresinthisarticlearedisplayedincoloronlinebutin
blackandwhiteintheprintedition.
[W]TheonlineversionofthisarticlecontainsWeb-onlydata.
[OPEN]Articlescanbeviewedonlinewithoutasubscription.
www.plantphysiol.org/cgi/doi/10.1104/pp.114.246660