Transcriptional regulation in wood formation

Taku Demura 1and Hiroo Fukuda 2

1RIKEN Plant Science Center,Yokohama,Kanagawa 230-0045,Japan

Department of Biological Sciences,Graduate School of Science,The University of Tokyo,Tokyo 113-0033,Japan

Wood (i.e.xylem tissue)in trees is mainly composed of two types of cells,?bres and tracheary elements.Recent molecular studies of various trees,as well as the non-tree species Arabidopsis thaliana and Zinnia elegans ,have revealed coordinated gene expression during differentiation of these cells in wood and the presence of several transcription factors that might govern the complex networks of transcriptional regulation.This article reviews recent ?ndings concerning the regulation of genes by transcription factors involved in wood for-mation such as AUXIN RESPONSE FACTOR (ARF),CLASS III HOMEODOMAIN–LEUCINE ZIPPER (HD-ZIPIII),KANADI (KAN),MYB and NAM/ATAF/CUC (NAC).Process of wood formation

Wood represents one of the most important sources of energy on earth,and is an environmentally acceptable future alternative to fossil fuel resources.Moreover,developing wood is an important sink that absorbs excess atmospheric CO 2,one of the major causes of global warm-ing.Wood is mainly composed of two types of cells with secondary cell walls:(i)?bres,which mechanically sup-port the plant bodies,and (ii)tracheary elements com-posed of vessels (not found in gymnosperm wood)and tracheids (found in both angiosperm and gymnosperm woods;see Glossary),which transport water and solutes.In general,these cells are formed from procambial cells or daughter cells produced by cambial initials (Figure 1a).Four major steps are involved in the formation of these cells:cell expansion,deposition of secondary walls,lig-ni?cation and programmed cell death [1].Expansion of the procambial cells and the cambial daughter cells involves primary wall formation and modi?cation.The expansion is followed by secondary wall formation,which includes the biosynthesis of polysaccharides (cellulose,hemicelluloses)and cell wall proteins,and ligni?cation.Finally,programmed cell death occurs to form an empty tube with secondary walls.Recent advances in the mol-ecular study of these processes have revealed the highly regulated genetic control of wood formation (mainly at the transcriptional level),on which we will focus in this review.In addition,although we are well aware that such genetic control could easily be in?uenced by many devel-opmental and environmental factors,we will venture to draw a simpli?ed scenario of wood formation by the

control of various transcriptional regulators and signal molecules.

Transcriptional pro?ling during wood formation

Technologies for measuring gene expression in plants have improved during the past decade [2].The exhaustive sequencing of expressed sequence tags (ESTs)generated from large numbers of cDNA libraries isolated from specialized tissues and organs provides a useful tool for gene pro?ling.Production and analysis of ESTs from wood-forming tissues have increased our understanding of the gene regulation involved in wood formation in tree species including loblolly pine (Pinus taeda )[3–6],poplar (Populus species)[7,8],black locust (Robinia pseudoacacia )[9],Eucalyptus [10–12],and white spruce (Picea glauca )[13].The non-tree species Zinnia elegans (common zinnia)and Arabidopsis thaliana could also be used for transcrip-tional pro?ling of differentiating cells in xylem.In zinnia,mesophyll cells isolated from young leaves can be induced to transdifferentiate synchronously and at high frequency into tracheary elements in the presence of auxin and cytokinin [14].As a result,the zinnia xylogenic system is considered to be the best source for the identi?cation of signals,proteins and genes essential for xylem formation,including cell fate determination,cell–cell interaction,secondary wall formation and programmed cell death [14].A large number of ESTs have been produced from differentiating tracheary elements in the zinnia in vitro transdifferentiation system [15–17]

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Glossary

Abaxial :facing away from or on the opposite side of the axis.The abaxial leaf surface is most commonly the underside or side facing away from the stem.Adaxial :facing toward or on the same side of the axis.The adaxial leaf surface is most commonly the upper side or side facing the stem.

Cambium :meristematic tissue (a layer of actively dividing cells)from which secondary growth occurs in roots and stems.

Companion cell :parenchymatous cell closely associated with the conducting sieve element in phloem.

Interfascicular fibre :fibre cell arising between vascular bundles in some conifers and dicots.

Metaxylem :primary xylem produced from procambium,developing after the protoxylem and before the secondary xylem.Metaxylem vessels usually have reticulate and pitted thickenings of secondary cell walls.

Procambium :meristematic tissue near the shoot or root apex from which primary vascular bundles develop.

Protoxylem :first-formed primary xylem produced from procambium.Proto-xylem vessels usually have annular and spiral secondary wall thickenings.Sieve element :conducting cell in phloem,closely associated with companion cells.

Tracheid :water-conducting xylem cell with lignified secondary cell wall usually containing bordered pits,but lacking perforation plates.

Corresponding author:Demura,T.(demura@riken.jp ).Available online 16January 2007.

https://www.360docs.net/doc/9710955654.html,

Arabidopsis undergoes secondary growth in roots,hypocotyls and stems.Routine removal of in?orescence stems induces secondary xylem at the root–hypocotyl junc-tion [18,19],which is used for generating ESTs [20].Ara-bidopsis plants grown under a combination of short-and long-day conditions can also produce extensive secondary xylem in hypocotyls and in?orescence stems [21–23].The secondary xylem tissues induced arti?cially in Arabidopsis hypocotyls and stems are remarkably similar to those of the poplar tree [18,19,21,23](Figure 1b,c).In addition,Arabidopsis in?orescence stems develop interfascicular ?bre cells with thick secondary walls when internodes of the stems cease to elongate.Recently,a new in vitro xylogenic system was established in which Arabidopsis suspension cells were induced to differentiate into tracheary elements by culturing in the presence of brassi-nolide [24,25](Figure 1d).

The cDNA clones that were sequenced for EST analysis were used for comprehensive transcriptional pro?ling by cDNA microarrays (or macroarrays)in loblolly pine [3,26],black locust [9,27],Eucalyptus [10,28],poplar [29–31]and zinnia [15,17].In addition to the cDNA microarray analysis,other methods such as serial analysis of gene expression [32],cDNA-ampli?ed fragment length polymorphism [16,33,34]and differential display [35],have been success-fully adopted for transcriptional pro?ling during wood for-mation.Genome-wide expression pro?ling using Affymetrix GeneChip array ATH1,which represents $23750Arabi-dopsis genes [36],was carried out with wood-forming Ara-bidopsis tissues and organs [22,23,37,38],as well as with differentiating tracheary elements in the in vitro xylogenic

culture [24].Moreover,laser microdissection [39,40]and ?uorescence-activated cell sorting analysis have proven,in combination with microarray analysis,to be useful tools for global gene expression pro?ling in speci?c cell types [41].These analyses have uncovered several genes whose expression was changed signi?cantly during wood formation (Table 1),including genes encoding cell wall structural proteins and various enzymes associated with the biosyn-thesis of secondary cell wall polysaccharides (e.g.cellulose),the degradation and modi?cation of primary cell walls,the biosynthesis of lignin precursors,the polymerization of lig-nin in secondary walls,and programmed cell death [14,42].Because the expression of these genes is highly coordinated,it is expected that speci?c transcription factors might regulate their expression in a coordinated fashion.Indeed,transcriptional pro?ling indicates that many genes encoding transcription factors are expressed preferentially during wood formation in various plant species (Table 1).Transcription factors regulating wood formation

The characterization of Arabidopsis mutants with defects in vascular development,and reverse genetic analysis of vascular tissue-related genes revealed by transcriptional pro?ling has furthered our knowledge of transcriptional regulation during wood formation [14,43–45].As a result,several classes of transcription factors involved in wood formation have come under the spotlight.

AUX/IAAs and auxin response factors

Mutation of the MONOPTEROS/AUXIN RESPONSE FACTOR 5(MP /ARF5)gene,which encodes a

transcription

Figure 1.Wood formation from procambium and vascular cambium.(a)Schematic model of xylem (wood)formation.Procambial cells and daughter cells produced by cambial initials differentiate into phloem cells and xylem (wood)cells.Xylem (wood)cells include tracheary elements and fibres.Tracheids and vessels are constituents of tracheary elements.Two types of vessels are observed in angiosperms:protoxylem vessels that commonly have annular and spiral secondary wall thickenings and metaxylem vessels that usually have reticulate and pitted thickenings.(b)Cross-section of a poplar stem.(c)Cross-section of an Arabidopsis hypocotyl.(d)Tracheary elements induced in the Arabidopsis xylogenic culture.(e)Vessel elements transdifferentiated from the cortex cells of Arabidopsis roots overexpressing the VND7protein.

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factor that belongs to a family of ARFs,disrupts the normal body organization along the apical–basal axis and results in discontinuous and reduced vascular formation[44]. Similar phenotypes have been shown by dominant muta-tions in BODENLOS/INDOLEACETIC ACID-INDUCED PROTEIN12(BDL/IAA12)and AUXIN-RESISTANT6/ ARABIDOPSIS CULLIN1(AXR6/AtCUL1),which encode, respectively,a protein that belongs to a family of auxin-inducible transcriptional regulators(AUX/IAAs)and a member of the CULLIN/CDC53family of proteins consist-ing of SCF(for SKP1,CULLIN/CDC53,F-box protein) ubiquitin ligase[44].Recent?ndings suggested that the function of MP/ARF5as a transcriptional activator was suppressed through its interaction with BDL/IAA12in the absence of an auxin signal[46].In the presence of auxin, TRANSPORT INHIBITOR RESPONSE1(TIR1)encoding an auxin receptor F-box protein,which is a member of the SCF complex known as SCF TIR,might bind to auxin and activate degradation of BDL/IAA12[46].As a result,MP/ ARF5can be released from the inhibitory interaction with BDL/IAA12and then be activated for the transcription of genes involved in vascular formation[46].

Class III homeodomain-leucine zippers and KANADIs Mutations with defects in the determination of plant adaxial–abaxial(central–peripheral)polarity also affect the determination of xylem–phloem identity[47].Two classes of genes are known to comprise a genetic system involved in tissue patterning and polarity.The?rst class consists of three genes encoding class III homeodomain-leucine zipper(HD-ZIPIII)transcription factors:REVO-LUTA/INTERFASCICULAR FIBRELESS1(REV/IFL1), PHABULOSA/ARABIDOPSIS THALIANA HOMEOBOX 14(PHB/ATHB14)and PHAVOLUTA/ATHB9(PHV/ ATHB9).The second class contains three KANADI (KAN)genes(KAN1–KAN3)encoding members of the GARP-type transcription factor family[48].Gain-of-func-tion mutations in these HD-ZIPIII genes resulted in the formation of adaxialized lateral organs and amphivasal (xylem surrounding phloem)vascular bundles[47,49–52]. Similarly,simultaneous loss-of-function mutation in all KAN genes resulted in amphivasal vascular bundles,whereas the phb phv rev triple loss-of-function mutant has radicalized cotyledons with amphicribral(phloem sur-rounding xylem)vascular bundles[47].Furthermore,a comprehensive genetic analysis of the HD-ZIPIII genes revealed that the defects in interfascicular?bre formation in the rev-6(one of the rev/i?1mutations)were partially suppressed in the rev-6corona/athb15(cna/athb15)athb8 triple mutant,suggesting that ATHB8and CNA/ATHB15 have functions antagonistic to the REV/IFL1function in vascular formation[53].Moreover,the comprehensive analysis showed that REV/IFL1,PHB/ATHB14and PHV/ATHB9positively regulate the size of vascular bun-dles in a partially redundant manner[53].

All the gain-of-function mutations in the HD-ZIPIII genes map to the microRNA165/166(miR165/166)target sequence,which is located in a region encoding the pre-dicted sterol/lipid-binding START domains[47,49–52]. These mutations disrupt the miR165or miR166target sequence,with or without alteration of the amino acid sequences in the START domains,and result in the elev-ated stability of the transcripts[47,51],suggesting that the stability of HD-ZIPIII transcripts is under the control of miRNA regulation[55].The expression of a maize REV homologue,rolled leaf1,in the xylem is de?ned by the accumulation of maize miR166in the phloem[50].In addition,overexpression of a MIR166a gene that targets CNA/ATHB15results in the overproduction of xylem cells with a severe reduction in the transcript level of CNA/ ATHB15[54].

In addition to mutant analyses in Arabidopsis,the functions of HD-ZIPIII genes in wood formation have been demonstrated by using reverse genetic approaches in other plant species[56–61].The expression of the Populus tremula?Populus alba(Pta)PtaHB1gene,which encodes a HD-ZIPIII protein that is most similar to REV/IFL1,has been shown to be closely associated with wood formation. Consistent with the results obtained in Arabidopsis,its expression was conversely correlated with the level of Pta-miR166[61].Four HD-ZIPIII genes have been identi?ed in Z.elegans(ZeHB10,ZeHB11and ZeHB12,and ZeHB13, corresponding to ATHB8,REV/IFL1and CNA/ATHB15, respectively),which are all differentially expressed in

Table1.Transcription factors identi?ed by transcriptional pro?lings

Species Source Number of differentially regulated

genes Number of upregulated

TFs

Class Refs

Populus sp.Developing wood5395HD-ZIPIII,MYB[29] Tension wood44416Zinc?nger,WRKY,LIM[30] Loblolly pine Xylem113919DNA/RNA-binding,Hap5a[5] Eucalyptus sp.Xylem1827HD,bZIP,Zinc?nger[10]

Arabidopsis thaliana Hypocotyl xylem31933HD-ZIPIII,NAC,MYB,bHLH,

WRKY

[37]

Bolting stem>3000191AP2/EREBP,MYB,bZIP,HD,

C3H

[38]

Wood forming stem and

mature stem

70039MYB,AP2/ERF,WRKY,NAC,

HD,AUX/IAA,ARF

[22]

Developing stem56776Zinc?nger,HD,AP2,MYC,NAC,

MYB

[23]

Differentiating vessel170520NAC,MYB,bHLH,HD,Zinc

?nger

[24]

Zinnia elegans Differentiating vessel6524ARF,HD-ZIPIII,AUX/IAA,NAC[16] Differentiating vessel5233NAC,ARF,HD-ZIPIII[15] Abbreviations:AP2,APETALA2;ARF,auxin response factor;bHLH,basic helix–loop–helix;bZIP,basic-leucine zipper;EREBP,ethylene-responsive element binding protein; ERF,ethylene response factor;HD,homeodomain;HD-ZIPIII,class III homeodomain-leucine zipper;LIM,LIN11/ISL-1/MEC-3;NAC,NAM/ATAF/CUC;TFs,transcription factors. 66Review TRENDS in Plant Science Vol.12No.2

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vascular tissues:the expression of ZeHB13is restricted to the procambium;ZeHB10is expressed preferentially in immature xylem;and the expression of ZeHB11and ZeHB12is observed in the procambium,immature xylem and xylem parenchyma cells[59].This expression pattern is compatible with the function of the Arabidopsis ortho-logues described above.Overexpression of a miR165-or miR166-resistant ZeHB12induces the overproduction of xylem parenchyma cells,but not that of tracheary elements[58],which suggests that a different HD-ZIPIII gene plays a role in the induction of a distinctive type of xylem cells.

MYBs and LIMs

A detailed promoter analysis of genes encoding enzymes implicated in lignin biosynthesis revealed that the AC elements,also known as H-boxes,are necessary for xylem-localized gene expression[62].The promoters of two Eucalyptus gunnii genes,EgCCR and EgCAD2,encod-ing the terminal enzymes of lignin biosynthesis cinnamoyl-CoA reductase(CCR)and cinnamyl alcohol dehydrogenase (CAD),respectively,direct the preferential expression of those genes in xylem tissues undergoing active ligni?ca-tion[62,63].Recently,EgMYB2,a member of a new sub-group of the R2R3-MY

B family of transcription factors,has been mapped to a quantitative trait locus for lignin con-tent.The transcription factor it encodes has the ability to bind to the promoters of the EgCCR and EgCAD2genes (which contain the A

C elements)and regulates their tran-scription[63].The thickness of the secondary cell wall of transgenic tobacco plants overexpressing EgMYB2 dramatically increases and the lignin pro?le is altered, which suggests that EgMYB2is a positive regulator for both lignin biosynthesis and secondary wall formation in the xylem[63].Other R2R3-MYB-encoding genes have also been shown to bind to AC elements and/or regulate ligni-?cation in Antirrhinum majus(AmMYB308and AmMYB330),Arabidopsis(AtMYBPAP1)and loblolly pine (PtMYB1and PtMYB4)[62].Furthermore,a member of the LIM(LIN11/ISL-1/MEC-3)family of transcriptional regu-lators has been shown to bind to AC elements and regulate the expression of some lignin biosynthetic genes[64]. Therefore,?ne-tuning the expression of lignin-associated genes with AC elements in their promoters can be con-trolled by multiple transcription factors.

Functional analysis of the Arabidopsis ALTERED PHLOEM DEVELOPMENT(APL)gene,which encodes a nuclear-localized MYB transcription factor,revealed that the APL protein is involved in the promotion of phloem and the repression of xylem development[65].Given that HD-ZIPIII and KAN genes control xylem and phloem development antagonistically,it will be interesting to investigate how APL genetically interacts with HD-ZIPIII and/or KAN genes.

NAM/ATAF/CUC

Many NAM/ATAF/CUC(NAC)family genes are expressed preferentially in developing wood and differen-tiating tracheary elements(Table1).Functional analysis of some of these NAC genes resulted in the discovery of new pivotal regulators for wood formation[24,66].Transcriptional pro?ling in an Arabidopsis xylogenic culture revealed that all seven VASCULAR-RELATED NAC-DOMAIN(VND)genes were expressed preferentially in developing vascular tissues[24].Of these,VND6and VND7showed speci?c expression in immature vessels of the metaxylem and protoxylem,respectively.Strikingly, the ectopic expression of VND6and VND7can induce transdifferentiation into metaxylem-and protoxylem-like vessel cells,respectively,from cell types as diverse as guard cells in leaves,epidermis cells in hypocotyls and cortex cells in roots(Figure1e).Conversely,the ectopic expressions of chimeric repressor genes derived from VND6and VND7inhibit the formation of metaxylem and protoxylem vessels,respectively[24].

NAC SECONDARY WALL THICKENING PROMOTING FACTOR1(NST1)and NST2,which belong to a subfamily closely related to the VND subfamily,have been subjected to functional analysis[66].Ectopic expres-sion of NST1and NST2induced transdifferentiation of various cells into cells with thickened secondary walls[66]. Overexpression of another member of this family,NST3/ SND1,also induced ectopic secondary wall thickening in various cells,and simultaneous loss-of-function of NST3/ SND1and NST1resulted in the suppression of?bre cell formation[67,68].Taken together,these NST genes seem to have pivotal functions in transcriptional regulation that directs?bre cell differentiation.

Conclusions and future perspectives

As described above,in recent years,advances have been made in understanding transcriptional regulation during wood formation at the tissue and cellular levels.In addition,recent studies using zinnia and Arabidopsis have uncovered signalling molecules governing wood formation such as cytokinins[69,70],brassinosteroids(BRs)[71,72], proteoglycans(xylogens)[73]and tracheary element differ-entiation inhibitory factors(TDIFs)that are dodecapep-tides encoded by CLE(CLV3/ESR-related)family genes [74].The interrelationship between these factors is illus-trated in Figure2.

MP/ARF5is expressed in the procambium,suggesting that auxin is a key factor controlling procambium main-tenance and/or development[44].A functional cytokinin receptor,WOODEN LEG/CYTOKININ RESPONSE1/ ARABIDOPSIS HISTIDINE KINASE4(WOL/CRE1/ AtHK4),is also expressed in procambium;its recessive Arabidopsis mutant wol shows a reduced number of pro-cambial cells in embryos and in root vascular system developing into protoxylem vessels[69].Therefore,cross-talk between auxin and cytokinin should occur in the procambium or vascular cambium,enhancing early vas-cular development.Genes of the HD-ZIPIII and KAN families,which positively or negatively regulate wood formation,have a complex pattern of overlapping and antagonistic functions.miR165and miR166control the levels of HD-ZIPIII transcripts;furthermore,the KAN genes-mediated negative regulation of HD-ZIPIII expres-sion might occur via miR165or miR166[75].BRs promote xylem formation from the procambium,probably through the up-regulation of HD-ZIPIII genes[14];conversely,BRs repress phloem formation[71].APL,which is expressed

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speci?cally in the phloem,is primarily required for the differentiation of sieve elements and companion cells,as well as for the inhibition of xylem formation [65].Class I HD-ZIP genes such as ZeHB3might also function in phloem formation [76].

Speci?cation into distinctive vascular cells seems to be controlled by NAC-type master genes:VND7,VND6and NST1,and NST3/SND1are involved in the differen-tiation of three types of wood cells,proto-and meta-xylem vessels,and ?bres,respectively [24,66–68].Cytokinins can negatively control protoxylem vessel differentiation and ARABIDOPSIS HISTIDINE PHOSPHOTRANSFER PROTEIN 6(AHP6),an inhibitory pseudophosphotrans-fer protein,counteracts cytokinin signalling and speci?es cell types of vessel cells [70].The speci?c expression pattern of APL gene in differentiating sieve elements and companion cells indicates that APL is required prim-arily for the differentiation of phloem cells [65].

Further efforts should be invested into demonstrating the aforementioned hierarchical network of transcrip-tional regulation.One promising approach is the identi-?cation of target genes of pivotal transcription factors.Indeed,a systematic analysis using GeneChip arrays in combination with the dexamethasone (DEX)-indu-cible system revealed possible target genes of ZeHB12,the zinnia homologue of REV/IFL1[58].Moreover,the expression of constitutive promoter-driven transcription factors fused to the glucocorticoid receptor (GR)in the

presence of a protein synthesis inhibitor (cycloheximide)has been successfully used in plants to identify their direct target genes [77,78].The identi?cation of the direct target genes of the transcription factors using inducible systems should expand our knowledge of the transcriptional net-work during wood cell formation.Finally,the elucidation of the modes of interaction between signalling molecules and transcription factors,as well as the exploitation of different types of data relating to post-transcriptional,translational and post-translational genetic control will be essential in improving our understanding of wood formation.

Acknowledgements

We thank Zheng-Hua Ye for critical reading of the manuscript.We thank Nobuyuki Nishikubo and Masatoshi Yamaguchi for providing the photographs in Figure 1.Our work cited here was supported in part by Grants-in-Aid from the Ministry of Education,Science,Sports and Culture of Japan (14036205),and the Japan Society for the Promotion of Science (15770043,17207004).

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Plant Science Conferences in2007

Fourth International Symposium on Dynamics of Physiological Processes in Roots of Woody Plants

16–19September2007

Bangor,UK

http://www.joensuu.fi/metsatdk/gsforest/documents/Roots_Bangor.pdf

16th Biennial Australasian Plant Pathology Society Conference

24–27September2007

Adelaide,Australia

https://www.360docs.net/doc/9710955654.html,.au/apps2007

21st Asian Pacific Weed Science Society Conference

2–6October2007

Colombo,Sri Lanka

http://www.apwss21.lk/

XVI International Plant Protection Congress

15–18October2007

Glasgow,UK

https://www.360docs.net/doc/9710955654.html,/iapps2007/

9th Meeting of International Society For Plant Anaerobiosis

19–23November2007

Sendai,Japan

ASCB47th Annual Meeting

1–5December2007,Washington,DC,USA

https://www.360docs.net/doc/9710955654.html,/meetings/

70Review TRENDS in Plant Science Vol.12No.2

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