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Plant Physiol, October 2000, Vol. 124, pp. 495-498
SCIENTIFIC CORRESPONDENCE
The Cellulose Synthase Superfamily1
Todd A.
Richmond* and
Chris R.
Somerville
Carnegie Institution of Washington, Department of Plant Biology,
260 Panama Street, Stanford, California 94305 (T.A.R., C.R.S.); and
Department of Biological Sciences, Stanford University, Stanford,
California 94305 (C.R.S.)
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INTRODUCTION |
The availability of a nearly
complete genome sequence for Arabidopsis has created many novel
opportunities to identify, by computational methods, the genes that
encode enzymes, which have been difficult to characterize by
conventional means. We have used this approach to identify a large
family of genes of unknown function that show sequence similarity to
cellulose synthase. Our working hypothesis is that these genes encode
enzymes that catalyze the synthesis of non-cellulosic polysaccharides
(Cutler and Somerville, 1997 ).
A recent breakthrough in research concerning the biogenesis of plant
cell walls was the identification, by genomic methods, of genes
encoding cellulose synthase in cotton fibers (Pear et al., 1996;
Delmer, 1999). The cotton cellulose synthase genes, now termed
CesA1 and CesA2, were identified in a collection
of expressed sequence tag (EST) sequences on the basis of weak sequence similarity to genes for cellulose synthase from bacteria. In addition, the genes were expressed at high levels in cotton fibers at the onset
of secondary wall synthesis and a purified fragment of one of the
corresponding proteins was shown to bind UDP-Glc, the proposed substrate for cellulose biosynthesis. The conclusion that the cotton
CesA genes are cellulose synthases is supported by results obtained with two cellulose-deficient Arabidopsis mutants,
rsw1 (Arioli et al., 1998) and irx3 (Turner
and Somerville, 1997; Taylor et al., 1999). The genes corresponding to
the RSW1 and IRX3 loci exhibit a high degree of
sequence similarity to the cotton CesA genes and are
considered orthologs. Ten full-length CesA genes have been
sequenced from Arabidopsis, and there is a genome survey sequence that
may indicate one additional family member (Fig. 1).
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Figure 1.
Unrooted, bootstrapped tree of the
CesA superfamily. ClustalX (version 1.8) was used to create
an alignment of the full-length, publicly available protein sequences
that was then bootstrapped (n = 5,000 trials) to create
the final tree. Subfamilies are boxed. At, Arabidopsis; Gh, cotton; Le,
tomato; Mt, Medicago truncatula; Os, rice; Pt, Populus
tremuloides; Pt/Pa, Populus tremula × Populus
alba.
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It is not known at this time whether other polypeptides are also
required for cellulose synthase activity (i.e. the CesA polypeptides may be a component of a multisubunit enzyme complex). Until this matter
is resolved we consider it expedient to simply refer to the CesA family
members as cellulose synthase. The observation that IXR3
(AtCesA7), which is required for secondary wall cellulose synthesis, is
in a different branch of the CesA tree than RSW1 (AtCesA1), which is required for primary wall synthesis (Fig. 1), may
indicate that there is sequence divergence between the enzymes involved
in primary and secondary wall synthesis.
Reiterative database searches using the Arabidopsis Rsw1
(AtCesA1) and the cotton CesA polypeptide sequences as the initial query sequences revealed a large superfamily of at least 41 CesA-like genes in Arabidopsis. Based on predicted protein
sequences, we have grouped these genes into seven clearly
distinguishable families (Fig. 1): the CesA family, which
includes RSW1 and IRX3 (AtCesA7), and
six families of structurally related genes of unknown function designated as the "cellulose synthase-like" genes (CslA,
CslB, CslC, CslD, CslE, and
CslG). The nomenclature for these families is still under
discussion
(http://mbclserver.rutgers.edu/CPGN/CelluloseWeb/CesA.proposal.html), so the Csl designation for these genes should be
considered temporary and may be revised as the enzymatic function of
the members of each family is determined.
All of the members of the cellulose synthase superfamily appear to be
integral membrane proteins, with three to six transmembrane domains in
the carboxy terminal region of the protein and one or two transmembrane
domains in the amino terminal region. It is thought that the CesA
proteins are located in the plasma membrane (Delmer, 1999). If the Csl
proteins participate in the synthesis of non-cellulosic
polysaccharides, they would be expected to be located in the Golgi
apparatus. Preliminary analysis of CslB, CslG, and CslE fusions to
green fluorescent protein appear to localize to the Golgi (T. Richmond
and C. Somerville, unpublished data). Also, immunolocalization studies
with an antibody to the CslA protein indicates that this family is
localized to the cytoplasm (i.e. the Golgi apparatus) rather than the
plasma membrane (N. Sprenger and C. Somerville, unpublished data).
Intron-exon organization is conserved among the CesA,
CslB, CslG, and CslE gene families,
but not the CslA, CslC, or CslD families (Fig. 2). However, the
C-terminus of a subset of the CslD genes is congruent with
this organization as well. The CslD gene family is the most
similar of the Csl gene families to the CesA
family (approximately 45% identical at the amino acid level). The gene
structure for this family is unusual in that the seven genes for which
complete genomic sequence information is available have four different
patterns of intron-exon organization. Based on recent thinking about
the evolution of intron/exon structure (de Souza et al., 1998),
the small number of introns in this family, and their divergent nature,
would seem to suggest that this gene family is the oldest in the
cellulose synthase superfamily and may predate the CesA
family.
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Figure 2.
Comparison of the gene structure of
representative genes of the Arabidopsis CesA superfamily.
Colored boxes represent exons and the lines connecting them denote
introns. Thick vertical black bars indicate predicted transmembrane
domains as predicted by HMMTOP (http://www.enzim.hu/hmmtop/). Thin blue
bars represent conserved Asp residues, and the thicker gray bar
represents the QxxRW domain. Thin lines connecting different genes
indicate conserved intron-exon junctions.
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All members of the CesA family contain a putative
LIM-like Zn-binding domain/RING finger domain in the
N-terminal region, which is similar to several putative plant Leu
zipper transcription factors (Kawagoe and Delmer, 1997a, 1997b; Arioli
et al., 1998). LIM domains are known to mediate
protein-to-protein interactions (Bach, 2000), whereas RING
finger domains are thought to play a role in ubiquitin-mediated
proteolysis (Freemont, 2000). These domains may play a role in
mediating CesA function via protein partners or targeted degradation.
All of the Csl proteins lack this amino terminus extension,
including the CslD family, which contains proteins similar
in size to the CesAs.
Although the various CesA and Csl proteins vary in their degree of
sequence similarity to one another (Table
I), they share several features that have
been proposed to be indicative of processive glycosyltransferases
(Saxena et al., 1995). All of the CesA and Csl
gene products contain a D,D,D,QxxRW motif (Fig. 2), which has been
proposed to define the nucleotide sugar-binding domain and the
catalytic site of these enzymes. Based on this motif, the proposed
topology of these proteins (discussed above), and sequence-based
classification, the various members of the Arabidopsis cellulose
synthase superfamily appear to belong to family 2 of the inverting
nucleotide-diphospho-sugar glycosyltransferases (Campbell et al., 1997)
that synthesize repeating  -glycosyl unit structures. To date, this
family includes over 500 putative members, including cellulose
synthase, chitin synthase, hyaluronan synthase, -1,3-glucan
synthase, and a number of uncharacterized genes from many organisms
(Campbell et al., 1997;
http://afmb.cnrs-mrs.fr/~pedro/CAZY/gtf_2.html). The
function of the various Csl families is not known, but
speculation is that they are responsible for producing some of the
other polysaccharides found in plant cell walls and in secretions such
as root cap or stylar mucilage (Cutler and Somerville,
1997). Although the D,D,D,QxxRW motif is thought to be indicative of
processive -glycosyltransferases, there is no comparative sequence
data available on processive  -glycosyltransferases. Therefore we
cannot rule out the possibility that some of these enzymes produce
polysaccharides with -linkages, such as
rhamnogalacturonan I or rhamnogalacturonan II. It is
possible that linkage specificity is determined by subtle features in
the active site of the proteins (Stasinopoulos et al., 1999) and that members of the Arabidopsis cellulose synthase superfamily make polysaccharides with both - and -linkages.
| |
DISCUSSION |
With six families of Csl genes and six major
non-cellulosic polysaccharides in Arabidopsis (i.e. callose,
xyloglucan, glucuronoarabinoxylan, homogalacturonan, rhamnogalacturonan
I, and rhamnogalacturonan II), it is tempting to speculate that each
family is responsible for the biosynthesis of one of the principal
polysaccharides of the cell wall. Although we consider it possible that
the gene superfamily described here encodes enzymes that catalyze the
synthesis of different polymers, there is at present no evidence for
this other than the observation that sequence divergence is frequently associated with functional divergence. It is also possible that there
are additional functional divisions within the gene families that are
not evident from our analysis. Recent results concerning the
relationship between enzyme structure and function, such as experiments
showing that as few as four amino acid changes can alter the catalytic
outcome of an enzymatic reaction from desaturation to hydroxylation
(Broun et al., 1998), emphasize the need for caution in using sequence
similarity to infer function based on sequence.
The amount of plant genome sequence and EST information in the public
sequence databases is expanding rapidly. At present there are more than
900,000 plant ESTs and genome survey sequences in GenBank, most
of which are from 35 species. In the first 8 months of the year 2000, more than 516,000 new ESTs and genome survey sequences from 16 plant
species were deposited. Thus except for species such as Arabidopsis,
which will soon be completely sequenced, any attempt at a comprehensive
compilation of CesA-related sequence information represents a
continuing challenge. To facilitate research on these genes, we have
established a website (http://cellwall.stanford.edu) that
summarizes the ever-increasing number of cellulose synthase and
cellulose synthase-like genes. At present, there are more than 1,250 CesA and Csl sequences, from 29 different plant
species in GenBank. Although the most extensive information available is for Arabidopsis where there are more than 330 partial or complete gene sequences, there is also a significant amount of information available for several other species, especially rice, maize, soybean, and tomato. A crude estimate of the relative abundance of mRNA for the
various family members can be calculated from the frequency with which
each gene family is represented by EST sequences in the public
databases (Fig. 3).
Polysaccharides found in other plant species, but not in Arabidopsis
(Zablackis et al., 1995), such as mixed linkage xylans, mannans,
or arabinans, may be synthesized by genes that are not represented by
orthologs in Arabidopsis. A number of gene sequences from plants in
GenBank show limited similarity (<50% identity) to the members of the
various Csl families in Arabidopsis. This and other issues
will undoubtedly become more transparent when the function of the
Csl genes in Arabidopsis is known from direct experimental
evidence. Our laboratory, along with others, is examining the patterns
of gene expression and protein localization of the Arabidopsis
Csl genes, and attempting to characterize their enzymatic function using reverse genetics. We are confident that in the next
several years the function of these genes will be understood and it
will then be possible to begin to unravel the challenge of
understanding how cell wall composition and deposition is controlled.
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FOOTNOTES |
Received May 25, 2000; accepted July 7, 2000.
1
This work was supported in part by the U.S.
Department of Energy (grant no. DOE-FG02-00ER20133).
*
Corresponding author; e-mail todd{at}andrew2.stanford.edu; fax
650-325-6857.
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N. G. Taylor, R. M. Howells, A. K. Huttly, K. Vickers, and S. R. Turner
Interactions among three distinct CesA proteins essential for cellulose synthesis
PNAS,
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[Abstract]
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F. Goubet, A. Misrahi, S. K. Park, Z. Zhang, D. Twell, and P. Dupree
AtCSLA7, a Cellulose Synthase-Like Putative Glycosyltransferase, Is Important for Pollen Tube Growth and Embryogenesis in Arabidopsis
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M. S. Doblin, I. Kurek, D. Jacob-Wilk, and D. P. Delmer
Cellulose Biosynthesis in Plants: from Genes to Rosettes
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A. W. Roberts, E. M. Roberts, and D. P. Delmer
Cellulose Synthase (CesA) Genes in the Green Alga Mesotaenium caldariorum
Eukaryot. Cell,
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F. Roudier, G. Schindelman, R. DeSalle, and P. N. Benfey
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Plant Physiology,
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I. Kurek, Y. Kawagoe, D. Jacob-Wilk, M. Doblin, and D. Delmer
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C. Ellis, I. Karafyllidis, C. Wasternack, and J. G. Turner
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PLANT CELL,
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[Abstract]
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F. M. Ausubel
Summaries of National Science Foundation-Sponsored Arabidopsis 2010 Projects and National Science Foundation-Sponsored Plant Genome Projects That Are Generating Arabidopsis Resources for the Community
Plant Physiology,
June 1, 2002;
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M. Orsel, A. Krapp, and F. Daniel-Vedele
Analysis of the NRT2 Nitrate Transporter Family in Arabidopsis. Structure and Gene Expression
Plant Physiology,
June 1, 2002;
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[Abstract]
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S. P. Hazen, J. S. Scott-Craig, and J. D. Walton
Cellulose Synthase-Like Genes of Rice
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L. Peng, Y. Kawagoe, P. Hogan, and D. Delmer
Sitosterol-beta -glucoside as Primer for Cellulose Synthesis in Plants
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R. Yokoyama and K. Nishitani
A Comprehensive Expression Analysis of all Members of a Gene Family Encoding Cell-Wall Enzymes Allowed us to Predict cis-Regulatory Regions Involved in Cell-Wall Construction in Specific Organs of Arabidopsis
Plant Cell Physiol.,
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[Abstract]
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W.-R. Scheible, R. Eshed, T. Richmond, D. Delmer, and C. Somerville
Modifications of cellulose synthase confer resistance to isoxaben and thiazolidinone herbicides in Arabidopsis Ixr1 mutants
PNAS,
August 17, 2001;
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[Abstract]
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L. Peng, F. Xiang, E. Roberts, Y. Kawagoe, L. C. Greve, K. Kreuz, and D. P. Delmer
The Experimental Herbicide CGA 325'615 Inhibits Synthesis of Crystalline Cellulose and Causes Accumulation of Non-Crystalline {beta}-1,4-Glucan Associated with CesA Protein
Plant Physiology,
July 1, 2001;
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[Abstract]
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B. Scheres and J. Browse
Playing with Arabidopsis
Plant Physiology,
June 1, 2001;
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X. Wang, G. Cnops, R. Vanderhaeghen, S. De Block, M. Van Montagu, and M. Van Lijsebettens
AtCSLD3, A Cellulose Synthase-Like Gene Important for Root Hair Growth in Arabidopsis
Plant Physiology,
June 1, 2001;
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[Abstract]
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D. R. Lane, A. Wiedemeier, L. Peng, H. Höfte, S. Vernhettes, T. Desprez, C. H. Hocart, R. J. Birch, T. I. Baskin, J. E. Burn, et al.
Temperature-Sensitive Alleles of RSW2 Link the KORRIGAN Endo-1,4-{beta}-Glucanase to Cellulose Synthesis and Cytokinesis in Arabidopsis
Plant Physiology,
May 1, 2001;
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[Abstract]
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M. S. Doblin, L. De Melis, E. Newbigin, A. Bacic, and S. M. Read
Pollen Tubes of Nicotiana alata Express Two Genes from Different {beta}-Glucan Synthase Families
Plant Physiology,
April 1, 2001;
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[Abstract]
[Full Text]
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W.-R. Scheible, R. Eshed, T. Richmond, D. Delmer, and C. Somerville
Modifications of cellulose synthase confer resistance to isoxaben and thiazolidinone herbicides in Arabidopsis Ixr1 mutants
PNAS,
August 28, 2001;
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TOP
INTRODUCTION
DISCUSSION