MM3transcription factors in plants JAwEu PAZ-‘W!s fjW.-)
Tbe cloning of lbejiht transcriptiottfactorJkmtj&zntg tbe Cl gene of maize, indkztted tbatphts use tranmiptiott faders tbat are strtutnr~ m&ted to of animals in their cmtml of gene exptvsstorr, bemuse Cl sbowed StgniJicant structural bmalogy to tbe miebmte celklarp c-MYLGSince 1987, tbe mtahgae of bW&elated traascriptkm factors bas iocreased comiderab~ in sire due, printarily, to tbe ever+aadittg number of MyBgenes ideat@ed in bigberplaats (Arabidopsb tbaliana is estintated to cuatain mom than a bundred MYttgeaes). In vertebrates, tbe MHkehted pmtomcogenes comprise a maIlfamily tmVba ctatral mleiacowtmllingceUular~ferationaadcmnmheMto developntettt Howeveq wbUe tbejhctiom of someplant MYBgenes are relatiueiy wetl tmksto& tbcyawat presen& quite disttn& front tbeir animal couaterpatts.
between the repeats, with R2 and R3 positioned towards the 3’ and 5’ parts of the core motif bound by all vertebrate MY8 proteins**. A probable consequence of this interaction is that it has unposed constraints on repeat co-evolution. In agreement with this, MYB chimaeras prepared by combinations of R2 and R3 repeats from different protein sources generally have reduced binding afinity when compared with their progenitors. The DNA-binding specificity of plant MY8 proteins differs considerably between themselves, as well as from that of the vertebrate MYl3 proteinsts-19. For instance, the maize P protein recognizes the motif lC/AlTCClT/AlACC similar to that bound by -305 from Anrirrhinum, and neither of these proteins appears to bind to the similar vertebrate MYEt consensus motif (TAACNG) (Refs 17, 18). PhMYB3 from Pefuniu binds to two sequences, MBSI (TAAClC/GlG’l% and MBSII (TAACTAAC) (Ref. 18). In the case of PhMY83, it has been shown that a substitution of a single residue in the R2 recognition helix, Let144 to Glu (for nomenclature of positions, see Pig. 11, switches the dual DNA-binding specificity to that of c-MYEt, and the reciprocal substitution in c-MYB, Glu43 to Leu, gives dual DNA-binding specificity similar to PhhWB3 (Ref. 13). In agreement with experimental data, molecular modelling predicts that the presence in PhMYB3 of Leu, instead of Glu, has two consequences: one direct, due to the change in base-contacting specificity of Leu versus Glu (Ref. 20); and one indirect due to the inability of Leu, in contrast to Glu, to interact electrostatically with a base-contacting residue (Lys40), thereby facilitating the interaction of Lys40 with either of two altemative positions in the target DNA. Mutations in residues that do not contact bases also affect sequence-specific binding and might account for some of the differences in DNA-binding specificity
POD Thesis, Univ. de Al&al, like c-MYB (Ref. 291, but redox control remains to be demonstrated in r&o sIn plants. NalWOfMYBpiottin spedes Members of the plant MYB famHomo sapien c-MYB (Ref. 52) HshUl3 ily contain several serine or thfeoHsMYBL2 EwB/MYlw (Ref. 53) especially in their nine residues, A-MYB/MYFlLl (Ref. 53) HsMYBLl C-terminal domains, which are hMYEiC1 zea mays Cl(Ref.7) possible substrates of kinases, sugZmMYBPl PI (Ref. 1n gesting that phosphorylation can ZIWYBl zml (Ref. 39) affect the activitv of some olant zm3R (Ref. 391 zmMy838 MYB proteins as lt does for c&B HvMYEGa Hordium m&are GAMYB (Ref. 26) (Refs 4. 22). Phosnhorvlation might Anlimbinum majus Am305 (Ref. 22) AmMyB305 influence DNA bmdmg or t&rbl340 (Ref. 22) -340 MKTA (Ref. 24) Afdw?Wx scriptional actnation potential. GLl <Ref. 42) AthWBGll Ambidopsis tbaltana However, experimental evidence AtMYBl(Ref.46) AtMYBl for such control in plant MYB proAtMYB2 AtMYEt2(Ref. 15) teins is presently lacking, except MYBPh3 (Ref. 18) Petunia bybrkia PMIyB3 for AmMYB340, a protein that AN2 (Ref. 40) PhhwBAn2 shows little DNA binding when DmMYB Drosophila nrskrnogaster synthesized in s&o, but that recovDicpusrelium discoides !iizsfi?) ers b&h-afhmity binding, equivalent CDCS &. 10) Scbimwccbammyces$mnbe SpMYF%CDS to that of the protein synthesized in PLBD <Ref. 11) AnMYBFD Aspagillus nidulam vitro, after treatment of extracts in this review we have used the original gene name when referringto MYBgenes with alkaline phosphataseza. for whichmutationsare known.WherehWBgeneshavebeen isolatedon the basii MYB proteins can potentially of sequencehomology,we have used a standardized nOtEefl&NIe giving firstthe compete for common target motifs. initials0fthespe~ics,thenthet~rmMYf3, andthenate~dcscribiigthepanicular Tbii type of interaction has been familymemberderivedfromthe originaldescriptions(see references).In the figures suggested to occur in mammalian ibtmting sequencesimilarities, we use thisstandardized nomenclature throughout cells where transcriptional actiso that MYEtoroteins from a sinale suecies can he readily identikd. vation by c-MYB (or its retroviral derivative, v-MYB) can be Inhibited between plant MYB proteinst3JO. Of the eight putative in some cells by the activity of MYBL2, which can bid to the same DNA sequence&sl. Such competition base-contacting residues ln MYE3 proteins, six are fully conserved in all plant MYB proteins, and the remaining might also occur in plant cells, because MYE? proteins with very similar DNA-binding domains can compete two are conserved ln at least SO% of these proteins. In particular, the P protein shams all the putative basefor a common target site; this has been shown for contacting residues with c-MYB or PhMYB3 (Fig. l), two flower-specific MYB proteins, AmMYE%305 and -340 from Antiwhinum. but shows a very diierent DNA-binding behaviour to The net activation of these two proteins. Therefore, protein context has a transcription of their target genes in any particular cell significant effect on the specificity properties of basewill be dependent on the relative amounts of the two contacting residues and the strength of their contacts proteins, their relative abilities to bind DNA and their and might also inlluence the DNA bending or distorting differing abilities to activate transcriptions. properties of the proteins*t. In summary, although plant MYB proteins also interact with other transcriptional MYB moteins share the homoloaous MYB domain. regulators. Such interactions are widespread for c-MYB, differences in their base-contactingâ€?residues and in the and some are believed to involve interactions with a overall context of their MYB domains produce distinct negative regulatory domam in the C-terminus of the DNA-binding specificities in cliierent members of the protein that contains a leucine zipper motif. No similar family. domain has yet been described in any plant MYB protein. However, the Cl protein of maize interacts, in an obligate fashion, with the R protein, or its homologues Gene activity can potentially be regulated at many (B, SN and LC), to promote anthocyanin biosynthesis diierent stages. Pretranslational control is evident from (see below). R, LC, SN and B contain a bHLH (basicmany diierences in the organ-specific and temporal helix-loop-helm) motif characteristic of MYC transcrippatterns of accumulation of RNA of different plant MIT3 tion factorss*. Experiments using the yeast two-hybrid genest5J2-*-25and In response to environmental stimuli, system have shown that the Cl protein interacts directly such as light, salt stress or the plant hormones, gibberelwith the B protein, an interaction requiring the Nlit acid and abscisic acid*5J6J7. terminal part of Cl (containing the MYB domain), and Post-translational control can operate through diierthe N-terminal domain of B (which does not contain the ent mechanisms, including cellular redox potentialâ€?, bHLH domain). B derivatives lacking the bHLH motif phosphorylation and protein-protein interactions. still retain their competence to induce anthocyanin Thus. the in DNA-bmclmn caoacitv of two slant biosynthesis and can still bind Cl, strongly suggesting MYB proteins, AmM~B305 aid l%M?B3, has been that the major role of B is via its interaction with the Cl found to be sensitive to oxidation lR. Solano (1995) proteids.
TIG FEBRUARY1997 VOL. 13 No. 2
whatogllt MYB transmiptioll The three the vertebrate iWBL1
cellular members of IMYB family, c-MYB, MYBL2
similar target motifs and all are believed to play roles in cellular proliferation and are expressed in actively dividing cells before diier-
entiation, albeit in somewhat diierent tissue+~. In plants there is good evidence for diitinct functions for diierent MYB proteins; some controlling secondary metabolism, some regulating cellular morph& genesis and some serving in the signal transduction pathways responding to plant growth regulators. Within these groups there are sub groups of MYB proteins with overlapping functions as seen with the vertebrate hIYB proteins.
HsMYBLIKO~K-RVIELVQKP~.;SVIAMLKG. HsMYBLl tkMYEL2 WMYB DmMYB &nMYBFD SpMYBCD5 AmMYB305 AmMYBMx AtMYBl AtMYB2 AtMYBGll HvMYBGa PhMYB3 PhMYBAll2 ZlllMYBI ZmMY838 ZmMYBCl
HSMYBl.2 WMYB DrnMYB AnMYBFD SpMYECDS AmMYBSO5 AmMYBMx AtMYBl AtMYBP AtMYBGll HvMYBGa PhMYB3 PhMYBAn2 ZmMYR38 ZmMYBcl ZmMYBPl
RIGKSPE LIKGPWrKEEoPRVIELVQK.WSLI:AKHLKG. LVKG~KRELlQKVIELVKKYOTKQ.Wl'LIAKHLKG. LVKGAWTKDE,,DKVIELVKTYGPKK.WSDIALHLKG. LIKGPWTRDKDDNVIKLVRNFOPKK.IITLIARYLNG. iiRRGP+WPEEDQLLLQLVREQGPNNKWVRISQHNHY. LKILKAA"SKYGKNQ.WARISSLLVR. VRKG -ILINYIA.~SLARSAGLK VKKG ~KLLAYIEEIiGHGS.WRSLPLKAGLQ RVKGPWSKEEDDVLSELm .WSFIAP.SIPG. ~PWTEEEDAILVNFVSIHODAR.WNHIARSSGLK YKKGLwrVEmxi I~rn~.WNRIVP.KTGLIc LKKGPUPSAeDAILVDWKKHDE GN.WNA"QKNTGLF LKKGPWl'AAEDSIU4.EYVKKHGEGN.WNAVKRNSGLM VRKGAWPEEEOLLLRECIDKYGEGK.HHLVrmRAGLN~~PH LNRGSWTPQEpIRLIAYIQKXGHTN.WRALPKQAGLL ltmPD TNRG&4TKEEDEFUVAYIRGC.WRSLPKAAGLL RC-PD -SKEGK.WREVPQKAGLRRC~PN LKRGRWPAEEM)LLANYIARHGEGS.WRSLPKNAGLL It* v w *w VKKTSWTEIZDRIIYQA NP&EIARLLP.. STMRRR VKKSSviTE~DRIIY~ MWAEIAKLLP.. VKKSCWTElXDRIICE :zz NRWARIAKMLP.. IKKRAwsDlzEQIIFc@tAIHG NxWAEIAKFLP..-IKNmmSNKRv 1KKTAWTESEDEIIYQA"LEI.G XiWAKIAKRLP..-IKNSWNSTNKRK LNRDPISABXXAIERMVNEEG R~IARRLG..~D IKKTENSREEDEKLLHLAKLLP TwRTIApIApIV==A~LERypKLLDDL VRRGNITP~QLLINEL NRWSKIAKTLP..GRPDXEIPXfWRTRIQK IKRGPFSL(;eEQTIIQLLG ~SAIASHLP..FRTC+JEI-HLKKR LIRNSFTEbEDQAIIAAEAIHG Ni‘W3UIAKM.P. .Cd’KW%-SALR VRRGNITLIzQFMTLKLZ-ISLW.3 NRWSKIAQYLP..GRTDNEIF&43WRTRVQKQ VNKGNFTEQ3EDLIIRUtKLu; NRWSLIAKRVP..GKTL%QVKNY#NTHLSKK LKKGAFTPJZERLIIQL"SKNG tSwmaAmP..GR~I~IKRC LKKGAFTVEERRIIIEI -QLP..GRTS@E-KRR IKF.GDFSLIEVDLILRUiKLLG NRWSLIAGRLP..GRT-RKK LKRGNFTDEEEEAII'RLLG NKWSKIAACLP..--KKK LKRGNFTAIEDDLIVKLHSLLG NKWSLIAARLP..GRTDNRI~~ IRRGNISYIZEDLIIRLG NJ.WSLIAGRLP..GRTD1&IKNYWNSTLGRR VKRGNISKEEEDIIIKU,ATLG NRWSLIASHLP..GRTD8RIKNYXNSHLSRQ
FIGLIW1. The DNA-binding domain of plant MYB proteins:sequenceand structure.(a) Sequencealignment of the R2 and R3 repeatsof representativeMYB proteins from plants, Iimgi and animals using the CLUSTALV programs’. To unify nomenclatureall MYB proteins have been renamed to add a two letter prefix as a speciesidentifier (Box 1). Residuesconservedin all plant hWB proreins arehighlighted in white letters. The three regularlyspaced nyptophan residuespresentin each repeat of animal MYB prnteinsand known to be imponant in mainraining the hydrophobic core of the DNA-binding domain are labelled with asterisks.The positions correspondingto base-contactingresiduesof the murine homologue of HsMYB aremarked with arrowheads(K39, E43, N47, N90, r(93, iV94,N97 and S98; where position 1 is the first residueof the RZ repeat) and the size reflectsthe strengthof the contact. The three helicesin each repeaW* are shown in the lower part of the figure. The filled box correspondstc~the recognition helix. 6) Suucture of the MYB-DNA complex. Ribbon plot of the minimal DNA-binding domain of the murine homologue of HsMYB containing the R2 and R3 repeats, binding to its target DNA. The structure represented corresponds to the avenge of 25 NMR solutions”. Molecular mcdelling~j predictssimilar suucturesfor the different plant MYB proteins representedin Fig. l(a). The region in the recognition helix repeat correspondingto ba&contacting residuesis highlighted in red.
Phanylatanine +â€™ Cinnamate +* pCoumarat0 +3 pCwmaroyl-CoA-
(PhMYEt3?) + 4 Chakxne
(P) Phlobaphene -
+5 11 Flavanone +6 12 Dihydroflavonot-L
Flavonol (AmMYB905, AmMYB340?)
Leucoanthocyanidin 19 Anthocyanidin +9,10 Anthocyanin (Cl PLANP)
F2. Summaryof current understandingof the mks c MYB-relatedtranscriptionfactors in controlling phenylpropanoid
metabolism from phenyl alanine. MY&elated proteins known fo control expression of the subsets of genes encoding enzymes involved in these steps are shown at the end of each patkay. Nameswith question marks refer to proteinswhox role has been demonstrated only biochemically. The functions of MY6 proteins without question marks have been demonstrated genetically. P has been shown to control steps 4,5 and 7, and Cl m conrrol steps4,7,8,9 and a glutatbione-S-transferee (which is involved in transponation of ambocyanins to the vacuole). AN2 controls steps 7.8 and 10. AmMYB305and AmMYB340have been shown to activatesteps 1,5 and 6, PhhUB3 has been shown to activate one gene encodingCHS (step 4) in Petlrnia KHSJX and ZmMYLU has txen shown to activatestep 7.
MYEi proteins are known to play an important role in the control of phenylpropanoid metabolism. The Cl protein activates transcription of genes encoding enzymes involved in the biosynthesis of the anthocyanin pigments in the outer layer of cells of the maize seed endosperm (the aleuroneY.37.M. Activation has been demonstrated for five genes in the pathway to anthocyanin (Fig. 21, although Cl probably activates expression of all the genes required specifically for anthocyanin biosynthesis in the aleurone. Activation by Cl Involves a partner transcriptional activator in aleurone encoded by the R genes*. While Cl is active in aleurone, a very similar MYEt protein, PL, is functional in controlliig anthocyanin biosynthesis in the maize plant Cmcluclmg leaves, stems, and So on) where it interacts with other members of the R-protein family to activate anthocyanln biosynthetic gene expression23. In maize, another MYB protein, ZmMYE51 can activate one of the structural genes required for anthocyanin biosynthesis, but not the entire pathway39, while yet another, ZmMyB38, inhibits Cl-mediated activation
Cell shape The second well-established role for plant MYB genes is in the control of cell shape where the MLXi?A gene of Antirrbinum and the orthologous PhMyBl gene from Petunia have been shown to be essential for developing the conical form of petal epidermal cells (Fig. 3) and the CL1 gene of Arabidopsis has been shown to be essential for the differentiation of hair cells
TIG FEBRUARY 1997 VOL. 13 No. 2
(trichomes) in some parts of the leaf and in the stem24.42 IL. Mur W95) PhD Thesis, Vrije Univ. of Amsterdaml. These two roles might be mechanistically similar because overexpression of MIXTA in transgenic tobacco results in t&home formation on petals, suggesting that conical petal cells might be ‘trichoblasts’ arrested at an early stage in trichome formation (B. Glover and C. Mattin, unpublished). GLl is required for an initial expansion in the size of the cell that develops Into the trichome, and it acts upstream of a number of other genes43, mutation of which gives rise to cellular outgrowths that do not develop into full, branched trichomes. One, GQ, encodes a homeodomain protein that is probably a transcriptional activator of subsequent stages in trichome developmen@. It is, therefore, possible that GLl is a direct activator of the GZZ gene. Supporting this idea, the CL2 gene promoter contains motifs very similar to the binding sites of P and AmMYB305 transcription factors, and these lie in a region shown to affect CL2 function quantitatively, presumably through affecting the level of CL.2 expression44. The conical cells produced by the action of the MlXl% gene of Antirrbinum resemble the limited outgrowths produced in Arabidapsis g12 mutants where uichome formation is aborted. Perhaps the initial stages of trichome formation regulated by GLl are similar to those regulated by MIXTA. The developmental programme giving rise to conical cells in petals might terminate before the onset of that part of the programme regulated by GL2 in trichome development. In its speciRcation of trichome formation, GLl is either controlled by or interacts with the product of the 7TG gene, which is required for ttichome formation and anthocyanin production. Overexpression of the maize Rgene complements the rtg mutation leading to the suggestion that the 7TG gene product ia also a R-related protein that interacts with GLl in a manner analogous to the interaction of Cl and R in maize4s. Two MYB proteins from fungi, the CDCSgene product from Schirosaccbaromyces pornbe’ and the FLBD gene product from Aqwgilhs nidulans*~ can also control aspects of cell shape. The FLBD gene product is required for early conidiophore production in Aspetgilhs colonies. ‘Ihe initial branching of the hmgal mycelium might have mechanistic similarities to trichome formation, and FLBD is thought to activate a cascade of transcription factors for conidiophore production. Clearly, assessment of these similarities in the cellular mode of action of such diverse MYB proteins requires understanding of the specific biochemical processes they activate. Response to hormones A more-recently defined role for plant MYB proteins responses during seed development and germination. A barley MYB protein (GAhtYB) whose expression is induced by gibberellic acid (GA) has been is in hormonal
shown to activateexpressionof a gene encoding a high p1 a-amylase that is synthesized in barley aleurone upon germination for the mobilization of starch in the endosperm*s. Expression of GAMYB is induced by treatment of aleurone layers with GA and expression of the a-amylase gene is induced subsequently. There is a suggestion that other GA-inducible genes can also
Ftauas 3. Plant phenotypesdue to hfYBgene mutations. (a) Phenotypeof unstableallele of the Cl locus of maize.A tmnsposableelementinactivatesthe gene so the production of anthncyaninpigment in the aleurone layer of the kernel is suppressed.Somaticexcisiongivestise to pigmentedrevertant sectors.Photographcourtesyof Brian Scheftler.6) Phenntypeof locus of Anfiwbitwf~f t~tajta.Pigmented unstableallele of MLk’XA petal cellsarc viewed under the microscope.The tranqxxable elementsuppresseshKiTAexpression to give paler cellsand somaticreversiongivessectorsof full colour. The effect of MlXXA works not throughcontrol of pigmentproduction. hourever,but through the mndiication of the optical propertiesof the petal epidennal cells.(c)The effectof MNTAon cell shape.The MIxTI1gene controlsthe fortnationof conicalccll~ on the petal. Tntnspnsoninsenion givesrise to flat celb with sectorsof revertantconical cells due tn somaticexcisionas revealedby scanningelectronmicroscopy.The conical cellsappear mnre darkly pigmentedthan the flat cellsdue to their optimized reflectionand refractionprop&es.
respond to activation by hWB pmteins during seed germination because MYB-like motifs from other GAresponsive gene promoters have been shown to direa reporter gene expression in response to GA (Ref. 25). There is, as yet, no strong evidence for MYB protein involvement in other GA-induced processes in other pans of the plant although some MEI genes ate
TIG FEBRUARY 1997 VOL. 13 No. 2
animal counterparts. There is certainly a subckrss of MYB proteins (includiig AtM%Bl from Arabidopsis, Fig. 4) that bear greater structural similarity to vertebrate MYB proteins than to the other plant MYB proteins, and this structural similarity could reflect homologous cellular functions.
The pervasiveness of AfIB-related genes in aU major groups of eukaryotic organisms suggests that proteins with MYB-like DNA-binding domains developed early to regulate gene expression. Diierent types of MYB protein might then have evolved as a result of duplication or triplication of the basic repeat unit. It has been proposed that evolution has occurred mostly through modification of regulation of common structural genes, and the separation between different groups of eukaryotes might be accompanied by the differential use of the transcriptional factor classes. Thii does not, in itself, explain why plants have made such extensive use of MYB proteins, and it might well be that MYB genes have been duplicated and their functions expanded in conjunction with the development of novel functions in higher plants. Although fungi and bryophytes contain MYBs with two repeats, suggesting that R2R3-type proteins were early fonns of MYB available for controlling gene expression, it is the size of the R2R3-type MYI3 gene family in higher plants that is particularly remarkable. In one lower plant, the moss Physcmytmlla paiens, the MIT3 protein family has, in fact, been estimated to be small, with only two to three gene membersso. YYB gene function might have diversified in parallel to increasing complexity in developmental and metabolic pathways as, for example in phenylpropanoid metabolism and also in transcriptional responses to hormones, such as gibberellic acid and abscisic acid, which are, themselves, specialized plant signalling molecules generated from secondary metabohtes. So, plants appear to have used R2R3-type MYB transcription factors selectively to control their specialized physiological functions, while in contrast, vertebrates have developed only one small group of MYB proteins to control cellular proliferation and differentiation. However, only about 10% of the plant MYB genes have some attributed function, so the full extent of the participation of this transcription factor gene family in plant growth and development is only just becoming realized, as new and diverse functions are defined for its members.
spMYl3C!x Ftauna 4. Dendrogram of relationships among MYBproteins
derivedfrom the matrix of sequencesimilarities calculatedwith the CLUSTALVprogam5t. NomenciaNrefor MYB proteins as
in Fig. 1. expressed in response to GA treatment of Pefunia petals IL. Mur (1995) PhD Thesis. Vrije Univ. of Amsterdam]. Treatment with another plant hormone, abscisic acid (ABA), induces expression of ArMYE in Arabidapsis, a MYi gene that is also induced in response to dehydration or salt stree&. In maize, expression of the Cl gene is ABA-responsive, where it is involved in the formation of anthocyanin in the developing kemekY. AtMYB2 might be responsible for activating expression of some drought-responsive genes because binding by AtMYB2 to the promoier region of a drought- or saltstress-induced gene, rd22, has been demonstrated. The rd22 gene promoter also contains MYC-recognition sequences suggesting that AtMYB2 can interact with a bHLH protein to induce gene transcription in response to dehydration or salt stress*â€˜. Cellularpmli&ralion None of the known functions of MYB proteins in plants bear much similarity to the biological roles of the c-MYB family in vertebrates. Pan of the role of c-MYB in promoting cellular proliferation concerns the control of progression of the cell cycle from Gl to S phase through the regulation of CDC2 kinase. c-MYB has been shown to activate transcription from the CDC2 kinase gene promoter in animal cells and so to control the GI-S phase transition, a role that might go part of the way to explain its promotional effects on cellular proliferation@. No such role has yet been demonstrated for a plant MYE gene product although the CLX% gene from Arabidopsis has been shown to contain MYB recognition motifs withii its promoter. These sequences lie in regions dtar enhance the level of expression driven by the promoter as demonstrated by reporter gene fusion@. Perhaps there are MYB genes in plants with functions more closely analogous to their
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TIG FEBRUARY1997 VOL. 13 No. 2
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TIG FEBRUARY 1997 VOL. 13 No. 2