Regulation of cell wall biosynthesis
Regulation of cell wall biosynthesis Ruiqin Zhong and Zheng-Hua Ye
Plant cell walls differ in their amount and composition among various cell types and even in different microdomains of the wall of a given cell.Plants must have evolved regulatory mechanisms controlling biosynthesis,targeted secretion,and assembly of wall components to achieve the heterogeneity in cell walls.A number of factors,including hormones,the cytoskeleton,glycosylphosphatidylinositol-anchored proteins, phosphoinositides,and sugar nucleotide supply,have been implicated in the regulation of cell wall biosynthesis or deposition.In the past two years,there have been important discoveries in transcriptional regulation of secondary wall biosynthesis.Several transcription factors in the NAC and MYB families have been shown to be the key switches for activation of secondary wall biosynthesis.These studies suggest a transcriptional network comprised of a hierarchy of transcription factors is involved in regulating secondary wall biosynthesis.Further investigation and integration of the regulatory players participating in the making of cell walls will certainly lead to our understanding of how wall amounts and composition are controlled in a given cell type.This may eventually allow custom design of plant cell walls on the basis of our needs.
Address
Department of Plant Biology,University of Georgia,Athens,GA30602, USA
Corresponding author:Ye,Zheng-Hua(zhye@https://www.wendangku.net/doc/f27651732.html,)
Current Opinion in Plant Biology2007,10:564–572
This review comes from a themed issue on
Cell Biology
Edited by Ben Scheres and Volker Lipka
Available online22nd October2007
1369-5266/$–see front matter
#2007Elsevier Ltd.All rights reserved.
DOI10.1016/j.pbi.2007.09.001
Introduction
Plant cells are encased in rigid walls composed of cellu-lose,hemicellulose,pectin,proteins,and/or lignin,which vary in amount depending on cell types.The walls function as the plant‘exoskeleton’and de?ne the cell shape,and ultimately organ and whole plant morphology. They not only regulate cell growth and provide structural and mechanical support to plants,but also act as a physical barrier to biotic and abiotic stresses.Plant cell walls are important in human life,providing major dietary?bers and essential raw materials for textile,lumber,pulping, and potentially for biofuels.Therefore,understanding how plants make cell walls is imperative for basic plant biology and will have far-reaching impacts on biotechno-logical applications.
In the last decade,tremendous progress has been made toward identi?cation and functional characterization of genes involved in the biosynthesis of cell wall polysac-charides,including cellulose,glucomannan,xyloglucan, xylan,and pectin[1 ,2 ,3,4 ,5 ,6 ,7 ],as well as genes responsible for the biosynthesis of sugar nucleotide donors involved in polysaccharide biosynthesis[8].Mol-ecular and biochemical dissection of genes participating in the biosynthesis of individual cell wall components is the?rst critical step toward understanding cell wall bio-synthesis.Although plant cell walls are made of common components,their amount and composition differ among various cell types and even in different microdomains of the wall of a given cell[9].The walls can be modi?ed to meet the special needs of certain cell types,such as water-conducting tracheary elements,guard cells,and endoder-mis.In addition,the amount and composition of walls may change during cell growth[10]and in response to biotic and abiotic stresses[11].Therefore,plants must have evolved mechanisms to turn on different biosyn-thetic pathways of wall components in various cell types, synthesize the right amount of wall components,and assemble them in the right place to suit a wall?t to functions of speci?c cell types.
To understand how plants make different wall types,it is necessary to know the biosynthetic genes responsible for their synthesis and also the regulation of cell wall bio-synthesis and assembly.A number of factors,such as hormones[12–15],the cytoskeleton[16 ],glycosylpho-sphatidylinositol-anchored proteins[17–19],phosphoino-sitides[20–22],sugar nucleotide supply[23],and coordination of wall biosynthesis[24,25],have been implicated in the regulation of cell wall biosynthesis or deposition.Other factors might also be involved in the targeted secretion of wall materials,thereby regulating wall dynamics and heterogeneity[26].Owing to space limitation,this review only focuses on the recent advances in the transcriptional regulation of cell wall biosynthesis.
Heterogeneity of cell walls
Before the discussion of regulation of cell wall biosyn-thesis,it is important to brie?y review the diversity of cell walls in plants.Although cell walls are generally com-posed of cellulose,hemicellulose,pectin,proteins,and/or lignin,the amount and composition of individual wall components and the shapes of walls vary considerably
among cell types (Figure 1a).Plant cell walls are generally categorized into two types,primary and secondary walls.Primary walls are born during cytokinesis and further modi?ed during cell expansion,and secondary walls are laid down after cessation of cell expansion in some specialized cells.On the basis of the wall characteristics,plant cells are classi?ed into three basic types,that is,parenchyma,collenchyma,and sclerenchyma.Paren-chyma and collenchyma cells have only primary walls and sclerenchyma cells contain both primary and second-ary walls.Walls in parenchyma are typically thin and uniform,but their composition may differ dramatically among different parenchyma cells.For example,the storage parenchyma cells of some plant seeds,such as Coffea ,Diospyros ,and Phoenix spp.,have thick walls rich in hemicelluloses as storage polysaccharides [27].Collen-chyma cells have additional thickening of pectin-rich wall materials unevenly distributed around the cells (Figure 1b),which provide the needed mechanical strength without losing the plasticity of the elongating tissues [27].Sclerenchyma can be further divided into sclereids,?bers,and tracheary elements (Figure 1c and d).Sclereids and ?bers generally have uniformly thickened secondary walls,except for pits where second-ary wall thickening is locally prevented.However,the secondary wall thickening in tracheary elements has certain patterns,namely,annular,helical,reticulated,
scalariform,and pitted wall thickening [27].It is clear that plants have evolved sophisticated mechanisms to make various cell types with different walls,and these cells are organized to form a functional plant.
Transcriptional switches of secondary wall biosynthesis
As described above,the amount and composition of cell walls vary among cell types.Therefore,it is conceivable that genes involved in the biosynthesis of various wall components are coordinately expressed in a cell type speci?c manner.Little is known of molecular mechan-isms underlying the coordinated expression of genes involved in the biosynthesis of cellulose,hemicellulose,and pectin during primary wall formation.However,there have been recent breakthrough ?ndings in the regulation of secondary wall formation.
In some specialized cell types the secondary walls are required for mechanical strength,such as in tracheary elements,?bers,and sclereids.Secondary walls perform particular functions in certain cell types,such as endo-thecium,guard cells,endodermis,and trichomes.Sec-ondary walls are typically composed of cellulose,xylan,and/or lignin.To make secondary walls,genes participat-ing in the biosynthesis of cellulose,xylan,and lignin need to be coordinately expressed.One intriguing unknown is
Regulation of cell wall biosynthesis Zhong and Ye 565
Figure
1
Heterogeneity of walls in different cell types.(a)Cross section of a Smilax root showing the ordered arrangement of various cell types with diverse wall architectures.Note the uneven deposition of lignified secondary walls (stained red)in the endodermis.(b)Cross section of a
Sambucus stem showing lamellar collenchyma with additional wall thickening (stained green;arrows)unevenly placed around the cells.(c)Cross section of a flax stem showing phloem fibers (stained green)with extremely thick walls lacking lignin.Note the red lignin staining in the walls of xylem cells.(d)Cross section of a piece of wood from Quercus showing xylary fibers and vessels.Sections were stained with safranin and fast green.Lignified walls were stained red.ep,epidermis;co,cortex;en,endodermis;lc,lamellar collenchyma;mx,metaxylem;pf,phloem fiber;px,protoxylem;rp,ray parenchyma;sc,sclerenchyma;ve,vessel;xf,xylary fiber;xy,xylem.
the identity of the switch that turns on the developmental program of secondary wall biosynthesis.Recent studies on the development of?bers,vessels,and endothecium have found that several members of the NAC and MYB transcription factors are key switches in regulating sec-ondary wall biosynthesis(Table1).
The endothecium cells in anthers deposit band-like secondary wall thickening,which is required to release pollen through the stomium after anther maturation. Defects in secondary wall thickening in the endothecium produce an indehiscent anther phenotype[28].A study on two Arabidopsis NAC transcription factors,NAC SEC-ONDARY WALL THICKENING PROMOTING FACTOR1(NST1)and NST2,revealed that they func-tion redundantly in regulating secondary wall thickening in the endothecium of anthers[29 ].Simultaneous T-DNA knockout of the NST1and NST2genes results in a complete loss of secondary wall thickening in the endo-thecium,leading to a typical indehiscent anther pheno-type.Overexpression of either NST1or NST2induces ectopic deposition of secondary walls in parenchyma cells and upregulates the expression of genes involved in the biosynthesis of major secondary wall components.Thus, NST1and NST2are important in activation of the developmental pathway of secondary wall biosynthesis in the endothecium of anthers.
In addition,a member of the MYB transcription factor family,MYB26,can regulate secondary wall biosynthesis in the endothecium of anthers[30 ].Mutation of the MYB26gene in the Arabidopsis male sterile35mutant caused a loss of secondary wall thickening in the endo-thecium and concomitantly an indehiscent anther phe-notype[28].Overexpression of MYB26can induce the expression of secondary wall biosynthetic genes,leading to ectopic deposition of secondary walls[30 ].Since the expression of NST1and NST2is downregulated by MYB26mutation and upregulated by its overexpression, they were proposed as downstream targets of MYB26 although it is unknown whether MYB26directly activates NST1and NST2expression.These studies indicate that NST1,NST2,and MYB26are key regulators of second-ary wall biosynthesis in the endothecium.
Secondary walls are most abundantly deposited in ?bers and tracheary elements of wood.Recently,two research groups independently discovered important roles of two Arabidopsis NAC proteins,SECONDARY WALL ASSOCIATED NAC DOMAIN PROTEIN1
566Cell Biology
Table1
Transcription factors involved in regulation of secondary wall biosynthesis in Arabidopsis thaliana and other plants
Gene AGI code Tissue/cell type level
expression pattern
Dominant repression or
loss-of-function phenotype
Overexpression
phenotype
Reference
NST1At2g46770Anther;xylem;interfascicular
?ber;other organs Repression of secondary wall
thickening in endothecium
Ectopic deposition of
secondary walls
[29 ]
NST2At3g61910Anther;other organs Repression of secondary wall
thickening in endothecium;
NST1and NST2function
redundantly in the activation
of secondary wall thickening
in endothecium Ectopic deposition of secondary walls
[29 ]
SND1/NST3At1g32770Interfascicular?ber;xylary
?ber Repression of secondary wall
thickening in?bers;SND1/NST3
and NST1function redundantly
in the activation of secondary
wall thickening in?bers
Ectopic deposition of
secondary walls
[31 ,32 ,33 ]
VND6At5g62380Metaxylem in primary roots Repression of secondary wall
thickening in metaxylem Ectopic deposition of secondary walls
[36 ]
VND7At1g71930Protoxylem in primary roots Repression of secondary wall
thickening in protoxylem Ectopic deposition of secondary walls
[36 ]
MYB26At3g13890Anther Loss of secondary wall thickening
in endothecium Ectopic deposition of secondary walls
[28,30 ]
MYB46At5g12870Interfascicular?ber;xylary
?ber;vessel Repression of secondary wall
thickening in?bers and vessels
Ectopic deposition of
secondary walls
[35 ]
Pine PtMYB4–Secondary xylem Not determined Ectopic deposition of
lignin
[46] Eucalyptus EgMYB2–Secondary xylem Not determined Alteration of lignin
pro?le and increased
secondary wall
thickening in?bers
and vessels
[49 ]
Tobacco NtLIM1–Predominant expression
in stems Reduction in lignin content in
stem xylem
Not determined[53]
(SND1;also named NST3)and NST1,in the regulation of secondary wall biosynthesis in ?bers [31 ,32 ,33 ].The SND1gene is speci?cally expressed in interfascicular ?bers and xylary ?bers but not in the vessels of in?ores-cence stems.Inhibiting SND1functions by dominant repression results in a drastic reduction in secondary wall thickening in ?bers.Overexpression of SND1activates the expression of genes involved in the biosynthesis of cellulose,xylan,and lignin and leads to ectopic deposition of secondary walls (Figure 2b).SND1together with NST1,which was previously found to be important in secondary wall thickening of endothecium,acts redun-dantly in the regulation of secondary wall thickening in ?bers [32 ,33 ].Single knockout of either SND1or NST1has no effect on secondary wall thickening;how-ever,simultaneous RNAi inhibition or T-DNA knockout of both SND1and NST1results in a complete loss of secondary wall thickening in ?bers but does not affect vessels (Figure 2c and d).Effects of SND1overexpres-sion on secondary wall biosynthesis have also been reported [34].In addition,a MYB transcription factor,MYB46,has been found to be a direct target of SND1and to be important in the transcriptional regulation of sec-
ondary wall biosynthesis [35 ].It is clear that SND1,NST1,and MYB46are key switches regulating the devel-opmental program of secondary wall biosynthesis in ?bers.
Since SND1speci?cally turns on the developmental program of secondary wall thickening in ?ber cells,this suggests that other SND1-like NAC transcription factors might be involved in the activation of secondary wall biosynthesis in vessels.Strong candidates are the VAS-CULAR-RELATED NAC-DOMAIN (VND )genes,which are closely related to SND1(Figure 2a).Two VND genes have been implicated as key regulators in protoxylem and metaxylem development.Protoxylem is developed during organ elongation and has vessels with annular and helical secondary wall thickenings that provide necessary mechanical strength for water-conducting vessels and also allow organ elongation.Metaxylem develops after cessation of organ elongation and has vessels with scalariform,reticulated,and pitted secondary wall thickenings.Such wall patterns provide maximum mechanical strength to the vessels.While studying genes upregulated during in vitro tracheary element differen-
Regulation of cell wall biosynthesis Zhong and Ye 567
Figure
2
NAC genes are key switches for activation of secondary wall biosynthesis.(a)Phylogenetic relationship of secondary wall associated NACs compared with a few other known NACs.Note that NST1/2,SND1,and VND1-7are closely related.The NAC protein sequences were aligned using the ClustalW program (https://www.wendangku.net/doc/f27651732.html,/clustalw/),and the resulting alignment parameters were used to generate the phylogenetic tree.(b)Ectopic deposition of helical secondary walls in leaf mesophyll cells (arrow)induced by overexpression of SND1.Note the normal
vascular strand with helical secondary wall thickening (ve).(c)Cross section of a wild-type Arabidopsis inflorescence stem showing the lignified secondary walls (stained red)of interfascicular fibers,vessels,and xylary fibers.(d)Cross section of a stem of the snd1/nst1double knockout line showing a complete loss of secondary wall thickening in interfascicular fibers and xylary fibers but no change in vessel walls.Lignified walls were stained red with phloroglucinol–HCl.if,interfascicular fiber;pf,phloem fiber;ve,vessel;xf,xylary fiber.
tiation in cultured Arabidopsis cells,Kubo et al.[36 ]found that the expression of seven NAC domain tran-scription factors,VND1–7,was closely associated with tracheary element development.VND6and VND7were speci?cally expressed in the metaxylem and protoxylem,respectively,of Arabidopsis primary roots,and inhibition of their functions by dominant repression caused a loss of development of metaxylem and protoxylem,respect-ively.Interestingly,overexpression of VND6and VND7resulted in ectopic deposition of secondary walls with patterns similar to metaxylem and protoxylem,respectively.The authors concluded that VND6and VND7are respective master switches of metaxylem and protoxylem development.
It is interesting that ectopic secondary wall thickenings caused by overexpression of SND1or NST1/2,which are involved in secondary wall biosynthesis in ?bers or endo-thecium,also exhibit both protoxylem and metaxylem-like secondary wall patterns depending on the cell types involved [31 ,32 ].This suggests that secondary wall patterns are dictated by the intrinsic microtubule organ-ization in different cell types.In addition,Mitsuda et al.[32 ]reported that expression of VND6or VND7,driven by the SND1/NST3promoter,compensated for the secondary wall defective phenotypes caused by simul-taneous loss of SND1and NST1.Since VND6and VND7are closely related to SND1and NST1/2(Figure 2a),they may have similar functions in the regulation of secondary wall thickening,albeit in different cell types.
Transcriptional network regulating secondary wall biosynthesis
Studies on the transcriptional regulation of secondary wall biosynthesis have revealed several important points.First,the NAC proteins NST1/2,SND1,and VND6/7are key switches regulating secondary wall biosynthesis.Since these NACs phylogenetically belong to the same subgroup,they most probably activate the same group of downstream targets,albeit in different cell types (Figure 3).Second,MYB26and MYB46are another set of transcription factors involved in the regulation of secondary wall biosynthesis.Third,these NAC and MYB genes have cell type speci?c expression patterns and regulate the secondary wall biosynthesis in a cell type speci?c manner.Nevertheless,they all lead to the acti-vation of the same groups of secondary wall biosynthetic genes.Fourth,available evidence indicates that some transcription factors,such as SND1and VND6/7,func-tion speci?cally in one cell type.Others,however,such as NST1and MYB46,may play roles in at least two different cell types (Figure 3).
Although NST1/2,SND1,VND6/7,MYB26,and MYB46are key transcriptional activators of secondary wall bio-synthesis,it is unlikely that they directly induce the expression of secondary wall biosynthetic genes.It is
more likely that these transcriptional switches activate a cascade of other transcription factors,including those directly regulating the biosynthetic genes of cellulose,xylan,and lignin,which lead to secondary wall biosyn-thesis (Figure 3).This transcriptional network hypothesis is supported by the ?ndings that overexpression of SND1upregulates the expression of a group of secondary wall associated transcription factors,including SND2(At4g28500),SND3(At1g28470),MYB20(At1g66230),MYB46,MYB85(At4g22680),MYB103(At1g63910),and KNAT7(At1g62990)[31 ],and that MYB46is a direct target of SND1and its overexpression activates the expression of MYB85and KNAT7[35 ].In addition,
568Cell Biology
Figure
3
Schematic diagram of a hierarchy of transcription factors involved in regulation of secondary wall biosynthesis in fibers,tracheary elements,and endothecium.MYB26is believed to act upstream of NST1and NST2that function redundantly in the regulation of secondary wall thickening in endothecium.VND6and VND7are key switches for the development of metaxylem and protoxylem,respectively.SND1and NST1function redundantly in the activation of secondary wall biosynthesis in fibers and MYB46,a direct target of SND1,further upregulates MYB85and KNAT7.Several other secondary wall
associated transcription factors,including SND2,SND3,MYB20,and MYB103,are induced by SND1and are proposed to be SND1
downstream targets involved in secondary wall biosynthesis.These secondary wall associated transcription factors are also induced during the in vitro Arabidopsis tracheary element development and some of them are upregulated by NST1overexpression,suggesting that they might also be downstream targets of VND6/7and NST1/2.Additional transcription factors in the LIM and MYB families directly regulate the expression of lignin biosynthetic genes.It is currently unknown what transcription factors directly activate the biosynthetic pathways of cellulose and xylan.
the expression of some of these secondary wall associated transcription factors is also upregulated by NST1over-expression[29 ].Considering that some lignin biosyn-thetic genes can be directly activated by several MYBs (see below),one appealing hypothesis is that different transcription factors might separately or collectively acti-vate the biosynthetic pathways of cellulose,xylan,and lignin.Clearly,the next critical step is to characterize the functions of secondary wall associated transcription fac-tors,and unravel their interrelationships in the transcrip-tional network.Most importantly,it is necessary to uncover the transcription factors directly activating the expression of secondary wall biosynthetic genes.Recent genomic studies have found a number of additional transcription factors associated with xylem differentiation [37–42],and it will be interesting to investigate whether any are involved in regulation of secondary wall biosyn-thesis.
Transcriptional regulation of lignin biosynthesis
Although it is currently unknown what transcription factors directly activate the biosynthetic genes of cellu-lose and xylan,several MYB genes have been proposed to be transcriptional activators of the phenylpropanoid bio-synthetic pathway leading to the biosynthesis of mono-lignols and anthocyanins[43–48,49 ,50,51].These MYB proteins are thought to directly induce the expression of phenylpropanoid biosynthetic genes by binding to the AC cis-element in their promoters.However,only a few MYB genes,including PtMYB4from pine[46]and EgMYB2from Eucalyptus[49 ],were shown to be associ-ated with wood formation and lignin biosynthesis (Table1).Both PtMYB4and EgMYB2were expressed in secondary xylem,and bind to the AC element in the promoters of lignin biosynthetic genes.When over-expressed in tobacco plants,they upregulated the expression of lignin biosynthetic genes.In addition,over-expression of PtMYB4results in ectopic deposition of lignin,and overexpression of EgMYB2increases second-ary wall thickness in?bers and vessels probably by increased lignin deposition.Although there is no direct evidence of PtMYB4and EgMYB2functions,the avail-able data indicate they are involved in transcriptional regulation of the lignin biosynthetic pathway.Another MYB gene,PttMYB21a from poplar,was expressed during wood formation,and its overexpression leads to suppres-sion in the gene expression of caffeoyl coenzyme A O-methyltransferase[52],an enzyme that catalyzes a key methylation step in monolignol biosynthesis.Moreover,a LIM transcription factor can bind to the Pal box cis-element in the promoters of monolignol biosynthetic genes,and repression of the LIM gene leads to inhibition of lignin biosynthesis in transgenic tobacco plants[53].It is important to further investigate how these transcription factors act together to regulate lignin biosynthesis.Concluding remarks
In the past few years,we have witnessed unprecedented progress in the characterization of cell wall biosynthetic genes and in studies of transcriptional regulation of secondary wall biosynthesis.The information gained provides foundation knowledge for further investigation of the molecular mechanisms underlying the biosyn-thesis and assembly of wall materials in different cell types.Following are a few important research direc-tions,which provide both challenges and opportunities in our understanding of how cell wall biosynthesis is regulated.
First,it is imperative to?nd the signals and signal trans-duction pathways that govern which cell wall biosynthetic pathways are turned on and how much wall material is produced in a given cell type.For example,to make secondary walls in?bers and tracheary elements,their parenchymatous precursors must receive signals to acti-vate the developmental program of secondary wall bio-synthesis.Uncovering the signals responsible for secondary wall biosynthesis will have tremendous impacts in tree biotechnology.Second,it is important to unravel the molecular mechanisms determining the wall heterogeneity in different cell types.Further identi-?cation of cell wall biosynthetic genes and study of their cell type level expression patterns is a?rst step toward solving this enigma.Third,it will be interesting to investigate the cellular mechanisms underlying the non-uniform or patterned deposition of walls in some specialized cells,such as collenchyma cells,epidermis, and tracheary elements.Fourth,available evidence indicates that a transcriptional network is involved in the regulation of secondary wall biosynthesis,and it is important to further investigate the hierarchy of transcrip-tional factors leading to secondary wall biosynthesis (Figure3).Uncovering the transcription factors directly regulating the biosynthetic genes of cellulose,xylan,and lignin has potentially tremendous biotechnological implications.Knowledge gained may make it possible to turn on or off the entire biosynthetic pathway of cellulose,xylan,or lignin by altering one or few transcrip-tion factors,and enable engineering of wood composition according to needs.Fifth,transcriptional networks may exist for the control of primary wall biosynthesis,thereby determining the amount and composition of walls in a given cell type.Understanding the transcriptional net-works regulating the biosynthetic pathways of cell wall components is essential to elucidate dynamic changes in cell walls during plant cell growth and development and in response to biotic and abiotic stresses.Finally,many additional factors can in?uence the amount and compo-sition of walls.In order to unravel the mechanisms underlying the complexity of cell wall heterogeneity,it is essential to use a systems biology approach to integrate all the players into the regulatory networks controlling cell wall biosynthesis.
Regulation of cell wall biosynthesis Zhong and Ye569
Acknowledgement
Research in ZHY’s laboratory is supported by a grant from the US Department of Energy-Bioscience Division(DE-FG02-03ER15415).
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