Hemicelluloses

ANRV410-PP61-12 ARI 31 March 2010 16:8
ANNUAL
REVIEWS Further Hemicelluloses
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Annual Reviews content online,
including:
Henrik Vibe Scheller1 and Peter Ulvskov2
• Other articles in this volume 1
Feedstocks Division, Joint BioEnergy Institute, Lawrence Berkeley National Laboratory,
• Top cited articles Emeryville, California 94608; email: hscheller@lbl.gov
• Top downloaded articles 2
Annu. Rev. Plant Biol. 2010.61:263-289. Downloaded from www.annualreviews.org
• Our comprehensive search Department of Plant Biology and Biotechnology, University of Copenhagen, DK-1871
Frederiksberg C, Denmark; email: ulvskov@life.ku.dk
by University of Sussex on 05/12/12. For personal use only.
Annu. Rev. Plant Biol. 2010. 61:263–89 Key Words

First published online as a Review in Advance on xyloglucan, xylan, mannan, glucomannan, mixed-linkage glucan, plant
January 29, 2010
cell wall
The Annual Review of Plant Biology is online at
plant.annualreviews.org Abstract
This article’s doi: Hemicelluloses are polysaccharides in plant cell walls that have β-
10.1146/annurev-arplant-042809-112315
(1→4)-linked backbones with an equatorial configuration. Hemicel-
Copyright c 2010 by Annual Reviews. luloses include xyloglucans, xylans, mannans and glucomannans, and
All rights reserved
β-(1→3,1→4)-glucans. These types of hemicelluloses are present in
1543-5008/10/0602-0263$20.00 the cell walls of all terrestrial plants, except for β-(1→3,1→4)-glucans,
which are restricted to Poales and a few other groups. The detailed
structure of the hemicelluloses and their abundance vary widely be-
tween different species and cell types. The most important biological
role of hemicelluloses is their contribution to strengthening the cell wall
by interaction with cellulose and, in some walls, with lignin. These fea-
tures are discussed in relation to widely accepted models of the primary
wall.
Hemicelluloses are synthesized by glycosyltransferases located in the
Golgi membranes. Many glycosyltransferases needed for biosynthesis
of xyloglucans and mannans are known. In contrast, the biosynthesis
of xylans and β-(1→3,1→4)-glucans remains very elusive, and recent
studies have led to more questions than answers.
263
ANRV410-PP61-12 ARI 31 March 2010 16:8
to 100 times their original length, and the pri-

Contents mary wall surrounding such cells fulfills the
support and barrier functions while expanding
INTRODUCTION . . . . . . . . . . . . . . . . . . 264
with the growing cell. Primary cell walls are the
STRUCTURE AND
walls that surround growing cells. After cessa-
DISTRIBUTION . . . . . . . . . . . . . . . . . 265
tion of cell expansion, some cells (e.g., fibers
Xyloglucan . . . . . . . . . . . . . . . . . . . . . . . . 265
and tracheary elements) develop a secondary
Xylans . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 268
wall, which gives additional strength. Some cell
Mannans and Glucomannans . . . . . . . 269
walls in seeds are highly thickened due to accu-
β-(1→3,1→4)-glucans . . . . . . . . . . . . . 270
mulation of polysaccharides that serve as seed
BIOSYNTHESIS. . . . . . . . . . . . . . . . . . . . . 270
storage.
Xyloglucan . . . . . . . . . . . . . . . . . . . . . . . . 270
Polysaccharides make up most of the wall,
Xylans . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 273
but the wall also contains proteins. Phenolic
Mannans and Glucomannans . . . . . . . 276
compounds, notably lignin, constitute up to

Mixed-Linkage Glucans . . . . . . . . . . . . 277
30% of some secondary walls. Many kinds of
The CESA-CSL Superfamily . . . . . . . 277
polysaccharides are present in all cell walls, the
FUNCTION OF
specific makeup varying in different species and
HEMICELLULOSES . . . . . . . . . . . . . 278
tissues. Classically, cell wall polysaccharides
Biological Function—
have been grouped into cellulose, hemicellu-
Hemicelluloses in Cell
loses, and pectins. Of these different classes,
Wall Models . . . . . . . . . . . . . . . . . . . . 278
only cellulose is well defined, consisting en-
Source of Signal Molecules . . . . . . . . . 280
tirely of β-(1→4)-linked glucan chains. Pectins
Seed Storage Carbohydrates . . . . . . . . 281
are highly heterogeneous polysaccharides, tra-
ENGINEERING OF CELL
ditionally characterized by being relatively
WALLS . . . . . . . . . . . . . . . . . . . . . . . . . . . 281
easily extracted with hot acid or chelators and
by containing a large amount of galacturonic
acid residues. Hemicelluloses traditionally
INTRODUCTION comprise the remaining polysaccharides,
A strong wall—composed of polysaccha- which can be extracted with alkaline treatment.
rides, proteins, and in some cells, phenolic These polysaccharides are very different from
compounds—surrounds every cell of terrestrial each other structurally and in physicochemical
plants. The type of wall, composed mainly of properties. Definitions based on extractability
polysaccharides, probably evolved among the are not useful. Some pectins can be extracted
charophyte green algae but is more evidently only with alkaline treatment, and this is partic-
suited for life on land. The wall provides sup- ularly true in some species such as lycophytes
port and shape for the plant, allowing it to (50). Similarly, the β-(1→3,1→4)-glucans in
stand upright. Some plants reach heights of grass cell walls and part of the arabinoxylans
more than 100 m, and obviously cell walls in in cereal endosperm are considered hemicel-
such plants are capable of supporting very large luloses but are quite readily extracted without
physical forces and are very durable. The plant alkaline treatment. In this review we have
cell wall also provides a barrier against the en- grouped the hemicelluloses into xyloglucan,
vironment and potentially pathogenic organ- xylans, mannans and glucomannans, and
isms. However, in spite of the strong, rigid, and β-(1→3,1→4)-glucans. Some polysaccharides,
seemingly impenetrable properties of cell walls, such as galactans, arabinans, and arabinogalac-
they are metabolically active, allowing exchange tans are sometimes included in the hemicellu-
of material and signals between cells, and are lose group, but since these appear to be part of
capable of expanding. The cells generated in pectin molecules, at least in the initial synthesis,
meristems by cell division will typically expand and do not share the equatorial β-(1→4)-linked
264 Scheller · Ulvskov

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backbone structure, we think they should not a Hemicellulose repeating disaccharides

be included in the already heterogeneous Equatorial
group of hemicelluloses. We also consider
that callose, which has a backbone entirely 4 3 1
5 O 2
composed of β-(1→3) linked glucose residues, O
3 1 4 O
should not be considered a hemicellulose. 2 5
β1 4
Hemicelluloses are a heterogeneous group
of polysaccharides, and the term was coined at
O
a time when the structures were not well un- O
O
derstood and biosynthesis was completely un-
known. The term hemicelluloses is therefore β1 4 glucan
archaic and various researchers have suggested
O
that it should not be used. Alternative terms O
O
such as cross-linking glycans have been pro-

posed (138, 140), but that has other problems β1 4 xylan
since it is not obvious that cross-linking is a

major and common feature of the hemicellu- O
O
loses. Nevertheless, most workers in the field O
still use the term hemicelluloses as a convenient

β1 4 glucomannan
denominator for a group of wall polysaccha-
rides that are characterized by being neither
O
cellulose nor pectin and by having β-(1→4)- O
O
linked backbones of glucose, mannose, or xy-
lose. These glycans all have the same equato-
β1 4 mannan
rial configuration at C1 and C4 and hence the
backbones have significant structural similar-
ity (Figure 1). We suggest that hemicelluloses b Pectic RG-I side chain
should be used to describe only polysaccharides Equatorial
Axial
with this configuration. O
O
O
STRUCTURE AND
DISTRIBUTION β1 4 galactan
Xyloglucan Figure 1
(a) Hemicelluloses are characterized by a
Xyloglucan (XyG) has been found in every land β-(1→4)-linked backbone with an equatorial
plant species that has been analyzed, including configuration at C1 and C4. (b) Polysaccharides such
mosses, but has not been found in Charophytes as β-(1→4)-galactan have an axial configuration at
(93, 108, 109) (see Figure 2 for an overview C4 and should not be included with hemicelluloses.
of plant phylogeny). XyG is the most abun-
dant hemicellulose in primary walls of sper- while X denotes α-d-Xyl-(1→6)-Glc. The xy-
matophytes except for grasses (Table 1). The losyl residues can be substituted at O-2 with
basic structure of XyG is shown in Figure 3, but β-Gal (L side chain) or α-l-Araf (S side chain).
there are many variations to this general pat- A Gal residue substituted at O-2 with α-l-Fuc
tern. In spite of the variations, XyGs are made is designated F. Other less common side chains
of repetitive units, and a special one-letter code have other designations.
is used to denote the different XyG side chains The branching pattern of XyG is of both XyG: xyloglucan
(41). G denotes an unbranched Glc residue, functional and taxonomic significance. Less
www.annualreviews.org • Hemicelluloses 265

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Lycophyta (club mosses and spike mosses)

Eukaryota Vascular plants
Rhodophyta (red algae) +
Moniliformopses (horsetails +, ferns)
MY
1 BY Chlorophyta (green algae) 410
MY Coniferophyta (conifers )
Gre eage
380
lin
Charaphyacean green algae +

en
MY (algae with higher-plant-like walls) MY

470 325
pla
n
Marchantiophyta (liverworts) +
t
Flo ants
pl
Nympheales
we
MY
Em
450
Bryophyta (mosses) Basal dicots
rin
M Y
bry
140 Magnoliids
g
Y
op
25 M
An
1
hy
Rosids
gio
tes
Asterids Eudicots
spe
Ranunculales, etc.
rm
Vascular plants
s
Liliales
Arecales (palms) O
Mo
no
Zingiberales X O Commelinids
cot
s
Poales + X O
Figure 2
Simplified phylogenetic tree illustrating the main taxa mentioned in the text. Most taxa are not shown in the figure. Estimates of the age
of some diversifications (15) are indicated. Estimates of the age of the commelinid clade have often been in the range of 80 MY, but
studies of grass leaf silica bodies in dinosaur dung (113) have pushed the age of Poacea back to 80 MY and the basal taxa of Poales to ca.
100 MY, making dating of the diversification of angiosperm families uncertain. Symbols designate hemicellulose patterns: +,
β-(1→3,1→4)-glucan has been found in members of the group; X, taxa where (glucurono)arabinoxylan is the major hemicellulose in
primary walls (as opposed to xyloglucan, or XyG, in other groups); O, taxa where xylans are esterified with ferulic acid.
branched XyGs are less soluble and this may xyloglucan oligosaccharide (142). The less sub-
correlate with functional aspects in those fam- stituted XXGG structure predominates in cell
ilies with the lowly substituted XyGs. The walls of commelinid monocots, which are also
most profound difference in XyG structure is distinguished by the low content of XyG in
charged versus uncharged side chains, with the the primary walls, typically 1–5% compared
former found in mosses and liverworts (104) with 20% in dicots (Table 1). These figures re-
whereas vascular plant XyGs are neutral. fer to expanding cells. For example, elongating
The major divide among vascular plant light-grown pea internodes contained 19.1%
families is in regard to whether XXGG or XyG as compared with 8.2% in internodes af-
XXXG is the predominant, core repeating ter cessation of growth (102). Oligosaccharides
Table 1 Occurrence of hemicelluloses in primary and secondary walls of plants

Amount of polysaccharide in wall (% w/w)a
Dicot walls Grass walls Conifer walls
Polysaccharide Primary Secondary Primary Secondary Primary Secondary
Xyloglucan 20–25 Minor 2–5 Minor 10 −b
Glucuronoxylan − 20–30 − − − −
Glucuronoarabinoxylan 5 − 20–40 40–50 2 5–15
(Gluco)mannan 3–5 2–5 2 0–5 − −
Galactoglucomannan − 0–3 − − +b 10–30
β-(1→3,1→4)-glucan Absent Absent 2–15 Minor Absent Absent
a
Numbers are typical values; actual values vary between different species and tissue types. Numbers are obtained from several different sources (31, 17, 37,
59, 72, 101, 135, 143, 147, 156; C. Manisseri and H. V. Scheller, unpublished data).
b
−, absent or minor; +, present but quantitative data not available.

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O
O
D-Glucose Glcp
Ac Ac
O O O
D-Galactose Galp O O O O O O
O O O O O O O O
O
D-Mannose Manp
X X F G X X L G
COOH
O Xyloglucan [β-D-Glcp-(1 4)]n backbone substituted with side chains as seen in pea and arabidopsis.
D-Glucuronic acid GlcAp The arrow indicates the typical β-glucanase cleavage site.
O
L-Arabinose Araf O
O O
O
O O
D-Xylose Xylp O O
O O
O
O O
L-Fucose Fucp
O
L-Rhamnose Rhap
Mixed linkage β-glucan [β-D-Glcp-(1 4)]n-β-D-Glcp-(1 3)-[β-D-Glcp-(1 4)]m, where n and m are 3 or 4;
typical of Poales.
O O O O O O O O O
COOH
COOH
Ac
O
O
O
O
O
Fer Fer OMe

Glucuronoarabinoxylan, GAX, typical of commelinid monocots.
O O O O O O O O O
COOH
COOH
COOH
O
O
O
OMe
Glucuronoxylan, typical dicot structure.
O
O O O O O O O O
Galactomannan, typical of Fabaceae seeds.

O
O O O O O O O O
Galactoglucomannan, typical of conifer wood.
Figure 3
Schematic illustration of the types of hemicelluloses found in plant cell walls. The letters under the xyloglucan (XyG) molecule
illustrate the symbols used for the most common side chains. The structure of the hemicelluloses varies greatly in different plant species
and tissue types. “Fer” represents esterification with ferulic acid (3-methoxy-4-hydroxycinnamic acid), which is characteristic of xylans
in commelinid monocots.

ANRV410-PP61-12 ARI 31 March 2010 16:8
of the XXGG type are also found in solana- the secondary walls of dicots. In commelinid
ceous XyGs, which are further characterized monocots (which include grasses and some
by lacking fucosyl residues and featuring the related species; see Figure 2), xylans are the
Cell walls of
commelinid arabinose-containing S chain (152). S is also major noncellulosic polysaccharide in primary
monocots: primary found in XXXG-type units in olive (141). walls, constituting about 20% (Table 1) of the
walls of grasses and Hoffman et al. (57) have shown that the F and wall. These xylans usually contain many arabi-
other commelinid the S side chains coexist in the XyG of Nerium nose residues attached to the backbone and are
monocots with a high
oleander and have compiled an extensive list of known as arabinoxylans and glucuronoarabi-
content of (glu-
curono)arabinoxylan XyG-repeating units from a wide range of plant noxylans (GAXs). The distinction is not clear.
are often described as families. Their general conclusion is that while Cereal endosperm arabinoxylan has very little
Type II walls, as the XyG oligosaccharide module structures glucuronic acid, but heteroxylans in vegetative
opposed to the more correlate with taxonomical groupings, there are parts of grasses are often called arabinoxy-
xyloglucan-rich Type I
several convergent adaptations of XyG struc- lans, even though they tend to contain more
walls in other plants
(20). However, studies ture among Tracheophytes so that the XyG glucuronic acid and 4-O-methyl glucuronosyl
of different taxa have structures do not mirror evolution in any simple residues, making GAX a more appropriate
revealed a large way. name. Branching patterns in xylan, like those
diversity in wall The occurrence of the fucose contain- in XyGs, correlate with taxonomy. Arabinofu-
composition. While
ing XyG F-chain (see side chain structure in ranose substitutions in grass walls are mostly
the Type I/Type II
distinction can be Figure 3) in the grass family is particularly from O-3 of the backbone xylose residues, and
useful, we have enigmatic. Purified hemicellulose fractions of xylose residues doubly substituted with arabi-
decided not to use it in oat and rice did not contain detectable fucose nofuranose at both O-2 and O-3 are common
this review (65, 73), and such studies led Hayashi (55) to in grass endosperm (31). Gymnosperm walls
Glycosyltransferases state that grass XyG does not contain fucose. also contain arabinoxylans in relatively high
(GTs): biosynthetic However, fucosylated XyG has been detected amounts (6). Arabinofuranose substitutions
enzymes that use an
in Festuca arundinacea by feeding radioactive fu- are less frequent in dicot xylans, but they are
activated sugar—most
often a nucleotide cose to cell suspension cultures (89), and Peña abundant in sycamore primary walls (27) and in
sugar—to transfer a et al. (104) cite unpublished results that low seeds of certain species from diverse taxonomic
sugar molecule to an amounts of fucosylated XyG are found by this groups, e.g., flax and psyllium (36, 96). Data
acceptor. In the case of method in rice as well. These observations can by Zablackis et al. (155) suggest that GAX
hemicelluloses, the
be reconciled if XyG is fucosylated transiently with fewer arabinose substitutions is present in
acceptors are the
growing in these grasses during synthesis and most of arabidopsis, but unambiguous evidence has not
polysaccharide chains the fucose is removed during or following de- been presented. The arabinofuranose substitu-
and possible primer position in the wall. A transient fucosylation of tions on dicot xylans are normally at O-2 rather
molecules grass XyG has implications for the assignment than O-3 as in grasses (27, 155), but doubly sub-
GAX: of function to grass glycosyltransferases (GTs) stituted xylose residues have been described in
glucuronoarabinoxylan of family GT37 (discussed below). flax mucilage (96) and 3-linked arabinofuranose
is present in psyllium seeds (27).
Unlike XyGs, xylans do not have a repeated
Xylans structure, and there are many variations in the
Xylans are a diverse group of polysaccharides structure that are not well known. A common
with the common feature of a backbone of feature of grass xylans is the O-2 linked xylose
β-(1→4)-linked xylose residues (Figure 3). residues often found as substituents of feruloyl-
A common modification of xylans is substitu- arabinofuranosyl side chains (144). Other fea-
tion with α-(1→2)-linked glucuronosyl and tures have been described, e.g. α-galactose
4-O-methyl glucuronosyl residues. Xylans linked to O-2 of glucuronosyl residues in eu-
dominated with this type of substitution are calyptus (123) and α-arabinofuranosyl residues
often known as glucuronoxylans and are the linked to O-2 of arabinose residues that are di-
dominating noncellulosic polysaccharide in rectly bound to the backbone in sorghum (139).

ANRV410-PP61-12 ARI 31 March 2010 16:8
O O O O Ferulate esters bound to cell walls have
O
been described in gymnosperms, but it is not
clear to which polysaccharide they are bound
O O (19). In Amaranthaceae sensu lato, i.e., includ-
COOH ing Chenopodiaceae, Rhamnogalacturonan-I
(RG-I) side chains are the sites of feruloyla-
Figure 4
tion, which occurs in both galactans and ara-
Schematic illustration of the oligosaccharide found
binans (115). The arabinosyl residues are pre-
in the reducing end of xylan. The β-d-Xylp-(1→4)-
β-d-Xylp-(1→3)-α-l-Rhap-(1→2)-α-d-GalpA- dominatly feruloylated at position 2 (60), but
(1→4)-d-Xylp structure has been found in several small amounts of feruloylation at position 5
different species. (as in GAX) have been detected (78). Recent
studies suggest that feruloylated pectins may
Most xylans are acetylated to various degrees, be present in many other plant groups but
especially in dicot secondary walls (31). Acetyl
restricted to stomata and therefore perhaps

groups are attached to O-3 of xylose residues present at a much lower level (64). The feruloyl
and to a lesser extent to O-2. transferases are unknown both in Chenopodi-
A somewhat surprising feature of xylans is aceae and in Poaceae, so it is not possible to
the conserved oligosaccharide that has been determine from the structures of the enzymes
found in the reducing end of xylan from dicots if they have a common origin. [See also (59) for
and conifers (Figure 4) (1, 63, 105, 124). This a comprehensive review of variations in feru-
structure has not been reported from grasses, loylated polysaccharides.]
but it appears that the genes responsible for Ferulate esters are important because they
making the structure are conserved in grasses can be oxidatively cross-linked in a variety of
as well (see below). ways. Ferulate dimers are easily detected in
grass walls and likely represent intra- and in-
Ferulate esters. An important feature of grass termolecular linkages in and between GAX
xylans is the presence of ferulic acid esters at- molecules. Ferulate can also be cross-linked
tached to O-5 of some of the arabinofuranosyl with lignin (48) and we can therefore assume
residues. Esters of p-coumaric acid are also that GAX and lignin become covalently cross-
abundant in grass cell walls, but it is not clear if linked through these linkages. Cross-linking
they can be attached directly to the xylans, and through ferulate esters is widely assumed to
they may be primarily associated with lignin render the cell wall recalcitrant to digestion,
(54). Feruloylated GAXs are found through- which would be an obvious benefit as a defense
out the commelinid monocots and not in other against microorganisms and herbivores. Simi-
groups of seed plants. While GAX is usually larly, the ferulate esters make grass cell walls
the dominating noncellulosic polysaccharide in recalcitrant to enzymatic saccharification prior
commelinid species, Arecales (palms), which is to fermentation into biofuels (11, 12).
the most basal group among the commelinids, is
an exception (Figure 2). The palm cell walls re-
semble those of the noncommelinid seed plants, Mannans and Glucomannans
i.e., with pectin as the major matrix polysac- β-(1→4)-linked polysaccharides containing
charide, most likely with fucosylated xyloglu- mannose are widely distributed and the main
can, but in addition, small amounts of truly 2,3- hemicellulose in Charophytes (108, 109). The
branched xylan carrying feruloyl esters (18, 53). backbones may consist entirely of mannose, as
These walls thus appear to represent a transi- in mannans and galactomannans, or with man-
tional form in agreement with its position as nose and glucose in a nonrepeating pattern
the least derived group among the commelinid as in glucomannans and galactoglucomannans.
monocots. Mannans and glucomanans are often acetylated.

ANRV410-PP61-12 ARI 31 March 2010 16:8
Mannans have been much studied in their grasses were a conserved ancient trait, then
role as seed storage compounds, but they are we would have to postulate the independent
found in variable amounts in all cell walls. In disappearance in a large number of Sper-
gymnosperms, galactoglucomannans are ma- matophyte taxa that have been investigated. It
jor components of the secondary walls (31). seems more likely that β-(1→3,1→4)-glucan
Mannans appear to have been very abundant in has evolved independently in grasses. Since
early land plants and are still abundant in mosses at least some of the genes responsible for
and lycophytes (50, 93). In spermatophytes, β-(1→3,1→4)-glucans biosynthesis in grasses
mannans and glucomannans are generally are known (see below), it should be readily
much less abundant and it appears that other testable if orthologs are conserved in Equi-
hemicelluloses have largely replaced them. setum and different algae while missing in
Nevertheless, mannans play essential roles, as dicots.
evidenced by the embryo lethal phenotype in
an arabidopsis mutant that is lacking the major

(gluco)mannan synthase in seeds (47). BIOSYNTHESIS
Xyloglucan
β-(1→3,1→4)-glucans Glycosyltransferases. Many of the biosyn-

β-(1→4)-linked glucans with interspersed sin- thetic enzymes involved in XyG biosynthesis
gle β-(1→3)-linkages are well known in grasses. have been identified. The fucosyltransferase
These mixed linkage glucans are dominated was one of the first cell wall biosynthetic en-
by cellotriosyl and cellotetrasyl units linked by zymes to be identified (106) (see Table 2 for a
β-(1→3) linkages, but longer β-(1→4)-linked list of GTs involved in hemicellulose biosynthe-
segments also occur (128). Mixed linkage glu- sis). XyG fucosyltransferase was purified from
can in primary walls plays a role in cell ex- pea using a traditional biochemical approach,
pansion and the amount is very growth-stage and the arabidopsis ortholog was expressed
dependent (23, 45, 97). and assayed in vitro. Subsequently, a fucose-
The β-(1→3,1→4)-glucans have not been deficient arabidopsis mutant, mur2, was shown
found in dicots but are found throughout Po- to be affected in the same gene (138). Analy-
ales, including the most basal family, Flag- sis of another fucose-deficient mutant, mur3,
ellariaceae (125). They have been suggested from the same mutant collection led to cloning
to be more abundant in the most derived of a gene, which turned out to encode a XyG
family, Poaceae (grasses; 125), but the strong β-(1→2)-galactosyltransferase (84). The galac-
growth-stage dependency of β-(1→3,1→4)- tosyltransferase has been shown to be highly
glucan content makes such quantitative argu- specific for the third galactose in the repeating
ments difficult. XXXG unit of xyloglucan. This is the galactose
Recent studies have shown that β- that is often fucosylated, explaining the fucose-
(1→3,1→4)-glucans are not restricted to deficient phenotype. The reduction in galactose
Poales but are present in Equisetum (38, is harder to detect since galactose is present in
126), and it has been suggested that they many other polymers. The galactose on the sec-
are also present in liverworts (109). Even ond position in the repeating unit must be in-
more recent work has shown the presence of corporated by a different galactosyltransferase.
β-(1→3,1→4)-glucans in Charophytes and Li et al. (80) have obtained evidence that a GT
red algae (Z. Popper and W. Willats, personal in subgroup A of the GT47 family is responsi-
communication) (Figure 2). The occurrence of ble for the activity, but the final evidence has not
β-(1→3,1→4)-glucans in many primitive taxa yet been reported. GT47 subgroup A contains
could indicate that they represent an ancient 10 members in arabidopsis and only MUR3 has
trait. However, if β-(1→3,1→4)-glucan in had the activity confirmed in vitro.

ANRV410-PP61-12 ARI 31 March 2010 16:8
Table 2 Glycosyltranserases involved in hemicellulose biosynthesis

Activitya GT name Identifierb CAZyc Reference Comment
Xyloglucan
β(1→4)-glucan synthase CSLC4 At3g28180 GT2 24
α(1→6)-XylT XXT1 At3g62720 GT34 34
XXT2 At4g02500 GT34
β(1→2)-GalT MUR3 At2g20370 GT47 84 Specific for the third xylose in the
XXXG repeating unit
β(1→2)-GalT GT47 79 An enzyme specific for the second
xylose in XXXG has not been
unambiguously identified
α(1→6)-FucT MUR2/FUT1 At2g03220 GT37 106
Xylan
β(1→4)-xylan synthase IRX9 At2g37090 GT43 2, 9, 75 Catalytic activity has not been
determined
β(1→4)-xylan synthase IRX14 At4g36890 GT43 9 Catalytic activity has not been
determined
β(1→4)-xylan synthase IRX10/GUT2 At1g27440 GT47 10, 149 Catalytic activity has not been
determined
IRX10-LIKE/GUT1 At5g61840 GT47
IRX7/FRA8 At2g28110 GT47 9, 105 Rhamnosyl β(1→3)-XylT?
F8H At5g22940 GT47 76
IRX8/GAUT12 At5g54690 GT8 9, 153 Xylosyl α(1→4)-GalAT?
PARVUS/GLZ1 At1g19300 GT8 74, 77 Involved in synthesis of reducing
end oligosaccharide. α-XylT?
α(1→2)-Araf T GT61? Predicted from expression data
α(1→3)-Araf T GT61? Predicted from expression data
α-Araf T transferring to GT61? Predicted from expression data
Ara-substituted Xyl
α(1→2)-GlcAT No candidate has been proposed
(Gluco)mannan
β(1→4)-mannan synthase CSLA/ManS AAR23313 GT2 28 From guar
α(1→6)-GalT TfGalT CAB52246 32 From fenugreek
Mixed-linkage glucan
β(1→3,1→4)-glucan OsCSLF2 AAL25132 GT2 14 From rice, catalytic activity not
synthase determined
OsCSLF4 AAL25134 GT2
β(1→3,1→4)-glucan HvCSLH1 ACN67534 GT2 29 From barley, catalytic activity not
synthase determined
a
Known and predicted enzymes involved in biosynthesis of the most common structures in hemicelluloses. The less common structures of XyGs and
xylans require a large set of additional activities.
b
Identifiers are given as gene locus IDs for Arabidopsis thaliana and as NCBI accession numbers for other species.
c
Glycosyltransferase (GT) family in CAZy database.

ANRV410-PP61-12 ARI 31 March 2010 16:8
The xylose residues in XyG are transferred The backbone of XyG is apparently syn-
by α-(1→6)-xylosyltransferases, which are re- thesized by members of cellulose synthase–
taining enzymes from family GT34. Two en- like proteins belonging to the CSLC family
zymes, XXT1 and XXT2 (originally named (Figure 5). Arabidopsis has five members of
XT1 and XT2), have been identified in ara- the CSLC subfamily and only CSLC4 has been
bidopsis and shown to be involved in the syn- shown to be involved in XyG biosynthesis (24).
thesis of XyG (21, 34). Somewhat surprisingly, It seems likely that the other CSLC members
a third GT34 enzyme, XXT5 from a sepa- are involved in XyG biosynthesis as well, but it
rate clade of GT34, has been implicated in cannot be excluded that some CSLC members
the same function, but the activity has not have a role in biosynthesis of other polymers.
been unambiguously demonstrated (156). The
XXT5 clade has two additional, uncharacter- Hydrolases. The GTs described above are all
ized arabidopsis members. In addition, GT34 Golgi-localized enzymes and work together to
has two arabidopsis members that are more produce a XyG precursor molecule that is trans-
closely related to galactomannan α-(1→6)- ported to the wall. However, important changes
galactosyltransferase (156). to the XyG molecules take place after the ini-
tial synthesis in the Golgi. Thus, it has been
shown that specific apoplastic glycosidases are

responsible for the trimming of nascent XyG
CSLF chains and important in determining the het-
CSLD erogeneity of the polymer in the wall (100).
The value of such apparently wasteful trim-
CESA
ming is unclear, but the higher substitution de-
CSLH gree of native hemicelluloses will help to keep
them soluble during transport and incorpora-
tion into the wall. In general, hydrolases are
likely to play an important role in determining
hemicellulose structures in the wall, and it may
CSLB CSLJ
be noted that many hydrolases are coexpressed
with polysaccharide biosynthetic enzymes. It is
interesting to note that the arabidopsis genome
contains about 300 membrane-bound GTs but
more than 500 glycoside hydrolases and lyases,
CSLE
many of which are involved in modification
CSLC
of wall polysaccharides. Plant hydrolases have
CSLG been described in recent reviews (82, 91).
Another important and well-studied modi-
fication of XyG is carried out by the XET en-
zymes. These are enzymes related to hydrolases
and carry out a transglycosylase reaction. The
CSLA
role of these enzymes is described below in the
Figure 5 section on Biological Function.
Schematic illustration of the phylogeny of the cellulose synthase (CESA) and
cellulose synthase–like (CSL) superfamily of GTs. Not all families are present
Polysaccharide acetylation. XyGs, like xy-
in the same species. CSLH and CSLF are only known from grasses, and CSLB
and CSLG are only known from dicots. CSLE is known from all angiosperms, lans, mannans, and pectins, are usually acety-
but not outside these groups. CESA, CSLA, CSLC, and CSLD are known lated to various degrees. Acetylation of XyG is
from all plant genomes analyzed so far. CSLJ is present in some angiosperms, on the galactose residues, mostly on O-6 (68).
both dicots and grasses, but not in arabidopsis and rice. Acetylation of cell wall polysaccharides occurs

ANRV410-PP61-12 ARI 31 March 2010 16:8
in the Golgi by means of transferases using and GT47 are predicted to be typical Type II
acetyl-CoA (103). Neither acetyltransferases membrane proteins with a single N-terminal
nor acetyl-CoA transporters required for this membrane anchor. See Table 2 to associate
XET: xyloglucan
process have been identified. A mutant of the each GT with the corresponding mutant and endotransglucosylases
fungus Cryptococcus neoformans lacks acetylation CAZy family. Although the GTs affected in belong to the
of the glucuronomannan coat polysaccharide these mutants belong to different families, xyloglucan endotrans-
and the affected gene has been suggested to they are all named irx for their irregular xylem glucosylase/hydrolase
(XTH) group of CAZy
be an acetyltransferase (62). Arabidopsis has four phenotype. Xylem cells are under negative
(see below) family
homologs of the C. neoformans protein, and we pressure, and compromised load-bearing abil- GH16 that also
have recently found that knockout mutants in ity is associated with vessel collapse or irregular comprises the
one of the corresponding genes, At3g06550, are walls. Secondary walls are rich in xylan in xyloglucan
deficient in wall-bound acetate (Y. Manabe and arabidopsis, and mutants in any of these genes endohydrolases
(XEH). The XETs
H. V. Scheller, unpublished data). Presently, it are deficient in xylan and xylan synthase activity
cleave xyloglucan
is unclear if the protein is an acetyltransferase, (2, 9, 10, 75, 77). However, so far no xylan (XyG) backbones,
but we think its topological model with mul- synthase activity has been reported for any of retain the energy of
tiple membrane-spanning segments suggests a these proteins when heterologously expressed. the glucosidic linkage,
transporter function. Presumably, several researchers have at- and graft the reducing
end of the cleaved

tempted to show xylan synthase activity, but
molecule onto the
without success. In our own work we have nonreducing end of an
Xylans expressed these proteins in E. coli and/or to- acceptor XyG.
The main chain of xylan as shown in Figure 1 bacco cells but failed to find xylan synthase XEH-catalyzed
may be differently substituted with side chains activity (A. Suttangkakul, A. Oikawa, H. V. hydrolysis proceeds
similarly, with water
and equipped with a unique oligosaccharide in Scheller, unpublished data). Obviously, it is
acting as the acceptor
its reducing end. Side chain structures vary with not possible to draw conclusions from nega- substrate
taxonomic origin (commelinid monocot ver- tive results, but the non-redundancy of IRX9,
CAZy: a
sus other flowering plants), and there is some IRX14, and IRX10 indicates that they are all comprehensive system
uncertainty as to how conserved the reducing required for backbone synthesis, perhaps in a and database
end oligosaccharide is. Biosynthesis is thus dealt complex containing more than one protein. A (www.cazy.org) for
with under three subheadings: Backbone Syn- homolog of IRX10 named NpGUT1 for glu- classifying
carbohydrate active
thesis, Reducing End Oligosaccharide, and Side curonosyltransferase was discovered in a Nico-
enzymes. Currently,
Chains. tiana plumbaginifolia cell adhesion mutant and glycosyltransferases
suggested to be involved in RG-II A-chain and glycoside
Backbone synthesis. Because of the struc- biosynthesis (61). IRX10 and IRX10-like ap- hydrolases in CAZy
tural similarity of xylan to the β-(1→4)-linked pear to be redundant and are unlikely to be or- are classified into 91
and 115 different
backbones of the other hemicelluloses, it has thologous to NpGUT1. The mutants do not
families, respectively
been widely assumed that the biosynthesis display a cell adhesion phenotype and should (16)
would involve members of the CSL protein rather be named for their pronounced irx phe-
families, as has been shown to be the case for the notype found when both genes are knocked
other hemicelluloses. However, investigations out (9, 149). Selaginella and Physcomitrella have
of CSL proteins have not provided evidence only a single IRX10/IRX10L ortholog (50) con-
that any of these proteins are involved in xylan firming that one gene product suffices. For
biosynthesis. Instead, characterization of xylan- IRX9 the situation is more complex. Arabidop-
deficient mutants irx9, irx14, irx10, and irx10- sis contains a homolog of IRX9, At1g27600,
like has indicated that the corresponding GTs the role of which has not been reported. Rice
belonging to families GT43 and GT47 are re- and other higher plants have members of both
sponsible for elongation of the xylan backbone. the IRX9 and the At1g27600 group, while Se-
Unlike the CLS proteins with multiple trans- laginella and Physcomitrella have orthologs only
membrane segments, the members of GT43 of At1g27600 (50). The most likely explanation

ANRV410-PP61-12 ARI 31 March 2010 16:8
for this is that IRX9 has a special role in sec- transferase. PARVUS (also known as GATL1)
ondary walls in seed plants. The At1g27600 is also a member of GT8, but belongs to the
protein and its orthologs in lycophytes and GATL group rather than the GAUT group
mosses would then have the same biochemi- (127). Rather than transferring a charged sugar,
cal function, but in other cell types. In agree- bacterial homologs of the GATL group are
ment with this, IRX9 is almost exclusively ex- lipopolysaccharide galactosyltransferases. Also,
pressed in cells with secondary wall growth, PARVUS has been reported to be located in
while At1g27600 is expressed in other cell types. the ER (77), indicating an earlier biosynthetic
IRX14 in arabidopsis has a close homolog, step than the subsequent Golgi-localized steps.
AT5G67230, which most likely would have the Hence, we suggest that PARVUS is an α-
same biochemical function. This could explain xylosyltransferase transferring the reducing end
the weak phenotype of the irx14 mutant (9). xylose to a primer, which may be a lipid. IRX7
is an inverting enzyme belonging to GT47. It is
Reducing end oligosaccharide. As men- a close homolog to IRX10, which as mentioned

tioned above, xylans in conifers and several above is implicated as a xylosyltransferase in-
dicots have been shown to have a reducing end volved in xylan backbone synthesis. Heterol-
with the unique structure β-d-Xylp-(1→4)-β- ogous expression of IRX7 has proved that it
d-Xylp-(1→3)-α-l-Rhap-(1→2)-α-d-GalpA- can function in vitro as a xylosyltransferase

(1→4)-d-Xylp (Figure 4) (1, 63, 105, 124). with several different sugars as acceptor (A.
Treatment of xylan with xylanases allows the Suttangkakul and H. V. Scheller, unpublished
isolation of the oligosaccharide. A number of data). Hence, IRX7 (and its close homolog
xylan-deficient mutants, irx7 (also known as F8H; 76) is a candidate for the Rha-specific
fra8), irx8, and parvus, have been shown to XylT. At present there is no clear candidate
retain in vitro xylan synthase activity while for the rhamnosyltransferase, nor for any addi-
being depleted in the reducing end oligosac- tional xylosyltransferases needed in the nonre-
charide (77, 105). In contrast, the reducing ducing end prior to IRX9, IRX14, and IRX10.
end oligosaccharide is present in irx9, irx14, What is the function of the reducing end
and irx10/irx10L mutants (9, 10, 105, 149). oligosaccharide? At first sight the most obvious
These observations indicate that IRX7, IRX8, function would be as a primer, since synthe-
and PARVUS are all specifically involved in sis of cell wall polysaccharides is generally as-
synthesizing the oligosaccharide. sumed to take place by transfer to the nonreduc-
It is unclear how many GTs are needed to ing end of the growing chain (121). However,
make the oligosaccharide. At the least, there York and O’Neill (153) have speculated that xy-
must be a XylT specific for Rha-GalA-Xyl, a lans may be synthesized in the other direction,
RhaT specific for GalA-Xyl, and a GalAT spe- i.e., growing in the reducing end and with the
cific for the terminal xylose, but it is possi- oligosaccharide functioning as a terminator se-
ble that additional xylosyl transferases would quence. This could explain why irx7 and irx8
be required to transfer the reducing end xy- mutants have unusually long xylan molecules
lose to a nonpolysaccharide primer and to trans- (105, 153). The fact that xylooligosaccharides
fer xylose onto the Xyl-Rha-GalA-Xyl acceptor. that are modified in the reducing end, e.g., by
The Rha-specific XylT and the GalA-specific attachment of fluorescent tags, are still excellent
RhaT are expected to be inverting enzymes, acceptors for xylan synthase in vitro suggests
while the Xyl-specific GalAT would be a retain- that synthesis does in fact proceed in the more
ing enzyme. IRX8 (also known as GAUT12) conventional way by transfer to the nonreduc-
is a homolog of GAUT1, which is a retaining ing end. However, as pointed out by York and
GalA transferase known to synthesize the back- O’Neill (153), the modified oligosaccharides
bone of homogalacturonan (127). Hence, IRX8 could be transferred to the reducing end of a
is the most obvious candidate for the GalA growing chain in the same way that a reducing

ANRV410-PP61-12 ARI 31 March 2010 16:8
end terminator sequence would normally HO O O O

O
be transferred. The reducing end oligosaccha-
ride has not been reported in grasses, although
the genes associated with its biosynthesis seem HO OH
HO OH
to be conserved. The absence of the oligosac-
OH
charide in grass xylan would also be in agree-
ment with the oligosaccharide being a termina- α-L-Araf α-L-Arap
tor rather than a primer. A primer would more
Figure 6
likely be indispensable. Clearly, much more
Most monosaccharides in cell wall polysaccharides
work is needed before xylan biosynthesis is are in the pyranose configuration. Arabinose,
understood. however, occurs mostly in the furanose
configuration.
Side chains. The most important side chains
of xylans should be formed by α-glucuron- us that GT61 would more likely include the
syltransferases and α-arabinofuranosyl- various arabinofuranosyltransferases needed
transferases. Both activities have been detected for xylan synthesis.
in vitro (3, 112, 157), but the GTs responsible The fact that the arabinose residues in xylan
for the transfer have not been identified. are in the arabinofuranose configuration while
FRA8 was originally proposed to be a xylan UDP-arabinopyranose is the nucleotide sugar
glucuronosyltransferase (158), but it is gen- known to be present in plants has been a co-
erally agreed that this is not correct and that nundrum (Figure 6). Intact Golgi vesicles can
FRA8 is involved in synthesis of the backbone. incorporate arabinofuranose residues into xylan
Xylan α-glucuronosyltransferase is expected using UDP-arabinopyranose as the substrate
to belong to a retaining GT family, but no (112). Most likely, the mechanism behind
obvious candidates have been proposed. this transfer involves formation of UDP-
Arabinosyl residues may be linked to posi- arabinofuranose by UDP-arabinopyranose
tion 2 or 3 or to both positions of the xylosyl mutase, as has been shown for arabinan
residues of the backbone. A monosubstituted biosynthesis (70, 71). Mutase activity has
xylosyl residue is expected to be a very different been found in reversibly glycosylated proteins
acceptor compared with an unsubstituted (RGPs) from rice and arabidopsis (71; C.
residue, and hence at least three inverting Rautengarten and H. V. Scheller, unpublished
arabinosyltransferase activities are required: an data). RGPs are abundant proteins, which
α(1→2) and an α(1→3) arabinosyltransferase are known to be located in the Golgi but
and a third for adding the second residue apparently as extrinsic membrane proteins on
to a monosubstituted xylose (no information the cytoplasmic side of the membranes. The
is available regarding the order of transfer). mutase catalyzes a reversible reaction, which
Members of GT61 (a family of inverting GTs) favors the pyranose configuration 10:1. Hence,
are highly expressed in grasses, which also it seems most likely that the mutase would
contain many grass-specific GT61 members. interact with a transporter and/or transferase
The only known activity of GT61 is the so that the generated UDP-arabinofuranose
β-(1→2)-xylosyltransferase activity involved can be used in a channeled reaction. The
in synthesis of N-linked glycans in plants (129). major UDP-xylose-4-epimerase required for
Hence, it has been speculated that GT61 generating UDP-arabinopyranose is predicted
members are involved in transferring xylose to to be located inside the Golgi (13). Therefore,
feruloyl-arabinofuranosyl side chains of xylan it is surprising that the mutase is located on the
(92). However, the abundant and conserved outside of the Golgi, since this would imply
RGP: reversibly
GT61 members in grasses and the presence that UDP-Arap is moved out of the Golgi, con- glycosylated protein
of GT61 members in other plants suggest to verted to UDP-Araf, and then moved back into

ANRV410-PP61-12 ARI 31 March 2010 16:8
the Golgi again. On the other hand, isolated putative acyl-transferases that are candidate fer-
wheat Golgi vesicles did not have detectable uloyl transferases based on a coexpression study
UDP-xylose-4-epimerase activity (112), so of rice genes. The candidate proteins are pre-
perhaps the topology and localization of the dicted to be cytoplasmic, which is consistent
epimerases need to be further investigated. with a role in feruloylation of a cytoplasmic
UDP-xylose is known to be synthesized both intermediate such as RGP but not with fer-
in the Golgi lumen and in the cytosol (52). uloylation of arabinoxylan in the Golgi. Very
recent data have confirmed that some of the
Hydrolases. GAX in primary walls has been candidate acyl-transferases are involved in xylan
shown to be synthesized in a more highly ara- feruloylation (107).
binosylated form and subsequently trimmed
by arabinofuranosides, resulting in much fewer
substituted polymers in mature cells (20, 43, Mannans and Glucomannans
97). Highly substituted arabinoxylan is more A mannan synthase involved in making the
soluble and does not interact with cellulose. backbone of galactomannan in guar was shown
Presumably, the soluble form is ideal for ini- to be a member of the CSLA family (28). Sub-
tial integration into an expanding wall, while sequently, several CSLA members have been
the less substituted polymer functions in the shown to have mannan and glucomannan syn-
mature wall by interaction between insoluble thase activity, apparently being able to utilize
xylan molecules and cellulose (20). both GDP-mannose and GDP-glucose as sub-
strates (81). Incorporation of glucose and man-
Ferulate esters. As mentioned above, ferulic nose in glucomannan does not follow a strict
acid esters are important components of grass pattern but is determined primarily by the rel-
arabinoxylans. The feruloyl transferases are not ative concentration of the substrates. How-
known, but the transfer takes place intracellu- ever, this may not necessarily be true in vivo.
larly in the Golgi (40, 98). The substrate has not The functional equivalence of CSLA proteins
been identified either, but feruloyl-CoA is the has also been confirmed in vivo since con-
most likely substrate, although other evidence structs with 35S promoter used to drive dif-
has suggested feruloyl-glucoside as a possible ferent CSLA homologs could complement the
substrate (98). In vitro synthesis of feruloylated embryo-lethal csla7 mutant in arabidopsis (46).
arabinoxylan has not been convincingly demon- Preliminary data from our laboratory have
strated, although some activity using feruloyl- indicated that CSLD proteins are also gluco-
CoA as donor and small oligosaccharides as ac- mannan synthases (150). These results were
ceptors has been reported (154). Other work obtained with microsomal preparations of ara-
using microsomal preparations from wheat or bidopsis CSLD5 expressed in tobacco and
parsley has shown that feruloyl-CoA incubation should be confirmed with purified protein. The
resulted in feruloylation of a protein rather than structure and phylogeny of CSLD proteins
a polysaccharide (69, 98). We tend to believe (Figure 5) (4) have led to suggestions that the
that the feruloylated protein is an intermedi- proteins would be glucan synthases using UDP-
ate in the feruloylation of arabinoxylan. The glucose as a substrate, so a GDP-sugar depen-
ferulic acid in wheat microsomes appeared to dent activity is unexpected.
be bound to arabinosyl residues on the pro- A galactosyltransferase involved in making
tein, although the structure was not unambigu- galactomannan was identified in fenugreek and
ously identified (N. Obel and H. V. Scheller, was the first GT involved in synthesis of plant
unpublished data), and the protein may be RGP. cell walls for which the activity of the pure en-
Most likely, feruloyl-arabinose is transferred as zyme was shown (32). Whereas the fenugreek
a unit from a precursor, perhaps RGP, onto enzyme, which belongs to GT34, is involved
the acceptor. Mitchell et al. (92) have identified in making seed galactomannan, it appears to

ANRV410-PP61-12 ARI 31 March 2010 16:8
have orthologs in dicots that have not been do not need to be present simultaneously for
reported to have seed galactomannan, includ- β-(1→3,1→4)-glucan synthase activity to oc-
ing arabidopsis. We propose that the appar- cur. In support of this, CSLF and CSLH genes
ent orthologous GT34s in arabidopsis signify are not coexpressed. Comparison of Brachy-
that the seeds do contain galactomannan. Oil podium, wheat, and barley has recently shown
is probably the most important storage com- that CSLF6 is the major CSLF gene expressed
pound in arabidopsis seeds and the amount of in wheat and barley seedlings, while other CSLF
galactomannan may be quite low. Seed galac- isoforms and CSLH are expressed at a very low
tomannans are known outside legumes, e.g., level (23). In contrast, Brachypodium seedlings
in tobacco and coffee, and these species have show a high expression level of CSLH. It will be
galactosyltransferases similar to the fenugreek interesting to investigate whether these species
enzyme (114, 117). In vitro, the relative concen- have different β-(1→3,1→4)-glucan fine struc-
trations of UDP-galactose and GDP-mannose tures: e.g., perhaps one type of CSL protein
determine the substitution degree of the galac- is chiefly involved in making the short β-
tomannans (118). However, for several reasons, (1→4)-linked segments and the other CSL pro-
mannans are likely to be synthesized as more tein type is chiefly responsible for making the
highly substituted polymers that are subse- longer segments. The ability of arabidopsis to
quently trimmed by α-galactosidases. Thus, the synthesize β-(1→3,1→4)-glucan when trans-

mannans found in some seeds (e.g., in ivory nut) formed with a single gene related to universally
are very low in galactose and essentially insol- present CSL genes suggests that evolution of β-
uble, and therefore they are likely synthesized (1→3,1→4)-synthesis can take place relatively
as more soluble precursors with a much higher easily and supports the idea that occurrence of
galactose substitution. Similarly, coconut has a β-(1→3,1→4)-glucan in very different taxo-
mannan-rich endosperm with a low galactose nomic groups is the result of convergent evolu-
substitution. However, makapuno mutants of tion. Isoforms of CSLH and CSLF have been
coconut have a much softer and thicker en- localized in the Golgi (29, 35), and in vitro activ-
dosperm containing a galactomannan with a ity studies have been consistent with biosynthe-
higher galactose/mannose ratio. In the case of sis of β-(1→3,1→4)-glucan in the Golgi (44,
makapuno coconut, it has been shown that the 56). However, unlike other matrix polysaccha-
mutant is deficient in a galactosidase (95). rides, β-(1→3,1→4)-glucan has not been de-
tected in the Golgi (148). This would imply ei-
ther that the β-(1→3,1→4)-glucan epitope is
Mixed-Linkage Glucans completely masked in Golgi vesicles, perhaps
The biosynthesis of β-(1→3,1→4)-glucan has by acetylation, or that some stage of synthesis
recently been shown to involve CSLF and takes place in the plasma membrane.
CSLH proteins (Figure 5) (14, 29). The corre-
sponding gene families are absent in arabidopsis
and poplar and present in rice and Brachypodium The CESA-CSL Superfamily
consistent with a grass-specific occurrence. The The cellulose synthase and cellulose synthase–
involvement of CSLF and CSLH was shown like superfamily of GTs (Figure 5) is involved
by expressing isoforms of the rice proteins in in synthesis of cellulose (CESA), hemicellu-
arabidopsis and detecting small amounts of β- loses XyG (CSLC), glucomannan (CSLA and
(1→3,1→4)-glucan in the transgenic plants. It perhaps CSLD), and β-(1→3,1→4)-glucan
is surprising that both types of protein can pro- (CSLF and CSLH). This raises the question
duce β-(1→3,1→4)-glucan alone. Most likely, of what the other CSL proteins may do. Most
the heterologously expressed proteins inter- likely, they would all be involved in mak-
act with other proteins present in arabidopsis, ing hemicelluloses as defined in this review,
but obviously the CSLF and CSLH proteins i.e., β-(1→4)-linked glycans with an equatorial

ANRV410-PP61-12 ARI 31 March 2010 16:8
configuration at C1 and C4. However, all and Ray (131) presented a model that empha-
known hemicelluloses have already been ac- sized separability features of the wall. According
counted for. Only CESA, CSLA, CSLC, and to this model cellulose microfibrils were coated
Expansin: a class of
proteins that stimulate CSLD proteins are present outside of the with several sheaths, with the hemicelluloses
creep in cell walls. spermatophytes, e.g., in Selaginella (119) and forming the innermost and most tightly bound
They are related to Physcomitrella (120), so presumably the other sheath; this model is referred to as the multicoat
hydrolases of CAZy CSL groups are either involved in synthesis of model (25). An attractive feature of the model
GH45 but have no
spermatophyte-specific polymers or work to- was that its construction outside the protoplast
hydrolytic activity.
Their mode of action gether with the more conserved CSL proteins. could be understood in terms of thermodynam-
is thought to be ically reasonable self-assembly mechanisms of
unzipping of hydrogen affinities and phase separation (83). At the same
bonds between wall FUNCTION OF time McCann & Roberts (85) presented a cell
polysaccharides
HEMICELLULOSES wall model drawn to scale (Figure 7). This
model has become the most influential to date.

Biological Function—Hemicelluloses It is also based on noncovalent interactions but
in Cell Wall Models has a particular noncovalent interaction as the
Primary walls and cell expansion. Cell wall central tenet: the importance of tethering gly-
models that are created to illustrate how wall cans that cross-link cellulose microfibrils. It is
polymers are organized in higher-order struc- referred to as the sticky network model (25).
tures influence the thinking about biological Tethering glycans, i.e., XyG in typical primary
functions of the hemicelluloses. The first sig- non-commelinid walls, bind to cellulose mi-
nificant cell wall model viewed the wall as a crofibrils by two mechanisms: by being trapped
giant molecule, i.e., with covalent linkages be- in the microfibril during the crystallization just
tween many noncellulosic polysaccharides (66). after synthesis, and by multiple hydrogen bonds
A notable feature of this model was a glycosidic between XyG and cellulose. The evidence for
linkage between XyG and galactan side chains tethering by XyGs is circumstantial but very
of RG-I. This view contrasted with the sequen- strong: The XyG backbone adopts a helical
tial extractability of wall polysaccharides that conformation in solution, which together with
led to the old hemicellulose definition. Talbott the arrangements of side chains prevents self-
association in solution while at the same time fa-
voring adoption of a flat conformation upon in-
teracting with cellulose (79). Endo-glucanases
will more easily access substrate in solution
than substrate in semicrystalline or adsorped
Middle states and can thus be used for preferential
lamella
Pectin extraction of more solvated XyG domains of
the wall. The part of XyG, which is accessi-
ble for release from pea cell wall by endoglu-
Primary canase, differs by the predominance of GXXG
cell wall
and GXFG (see Figure 3) from the XyG that
could only be released by strong alkali (49, 99).
Cellulose The definition and biological significance of
Plasma
membrane these distinct XyG domains are corroborated by
Hemicellulose the observation that expansins induce creep
50 nm more effectively in artificial cellulose/XyG
Figure 7 composites in which the XyG chains are long
Simplified model of the primary cell wall. Reprinted from McCann and enough to tether the microfibrils than in com-
Roberts (85) with permission. posites made with short XyG fragments (145).

ANRV410-PP61-12 ARI 31 March 2010 16:8
The unequivocal existence of tethering gly- onto an RG-I side chain or by a transglycosy-
cans does not mean they are indispensable load- lation reaction. Resolving these questions re-
bearing structures of the wall. Celery appears mains a major challenge in the field of hemicel-
to have dispensed with tethering glycans and lulose biochemistry.
features a pure multicoated model wall. With Cell walls grow at constant wall thickness
only 2% XyG and 2% xylan, there are not if carbon is not limiting (8). The concurrent
enough hemicellulosic polysaccharides to coat insertion of new building blocks should not
the microfibrils, and no other polysaccharides strengthen the wall so as to impair cell expan-
appear to have taken the place of the hemicellu- sion. Whether insertion of new wall polysac-
losic polymers (134). A fully viable mutant de- charides even contributes to wall creep is still
void of any detectable XyG has been created unresolved (130, 137), but it is widely accepted
in arabidopsis (22). Finally, Thompson (136) that the insertion of newly synthesized XyG
has calculated that the combined strength of occurs by transglycosylation catalyzed by XET
all XyG/cellulose hydrogen bonds in typical di- (26). Attempts to identify transglycosylases that
cot walls cannot transmit all the stress that the act on other polysaccharides have been met with
wall sustains. The solution to the latter prob- limited success. A glucomannan transglycosy-
lem probably rests in the fact that current mod- lase has been reported (122), while the search
els ignore direct cellulose microfibril contacts for a homogalacturonan transglycosylase was
and entanglement, the structures that sustain negative (42). The situation in the grasses is
by far the major load from turgor and small de- quite enigmatic. β-(1→3,1→4)-glucans are de-
formations (146). Another desirable aspect in posited during cell expansion only to be de-
future models would be evidence for the pec- graded and replaced with GAX as expansion
tic matrix also tethering microfibrils via RG- ceases. Measurements of the β-(1→3,1→4)-
I side chains (159, 160). Finally, new models glucan content in developing wheat, barley,
should revisit the issue of covalent linkages be- and Brachypodium seedlings during develop-
tween pectin and XyG. The above-mentioned ment demonstrate net breakdown as opposed
proposal of the original Keegstra et al. (66) to simple dilution by xylan (23). The hydro-
model that XyG is synthesized onto an RG- lases that are responsible for degradation of
I side chain, e.g., galactan, has more recently β-(1→3,1→4)-glucan belong to CAZy family
received support. The possible occurrence of GH16. XETs, the XyG transglycosylases, are
a base-stable linkage between XyG and RG-I also classified in this family, and it would be
was rediscovered while developing a XyG la- conceivable that some of the grass members of
beling method (33), and the observations in GH16 could transglucosylate β-(1→3,1→4)-
the following decade pointing to the existence glucan, but this appears not to be the case
of such a linkage was reviewed by Mort (94). (39, 58). Grasses thus appear to rely on a β-
Popper and Fry (110) found alkali-stable, an- (1→3,1→4)-glucan/xylan replacement rather
ionic complexes in suspension cultures of both than transglycosylation, and a xylan transglyco-
grass and non-commelinid seed plant cells, im- sylase remains to be identified. In dicots, xylan is
plying that the link is also an evolutionarily con- mostly deposited in secondary walls, i.e., where
served feature in grasses, which contain five- expansion has ceased. We speculate that dicots
fold less XyG compared to typical dicot walls. do not have a xylan transglycosylase and hence
Covalent linkages between matrix polysaccha- restrict the use of substantial amounts of xylan
rides are often thought of as wall maturation to walls that do not expand. Recently, a sur-
phenomena occurring by transglycosylation or prising new class of transglycosylases has been
transesterification in the wall, but XyG and RG- identified. These are the mixed-linkage beta-
I may be linked already in the Golgi (111). The glucan:XyG endotransglycosylases, or MXEs.
nature of the linkage is unknown, as is the mode These enzymes, which graft β-(1→3,1→4)-
of its synthesis—whether by synthesizing XyG glucan onto XyG, have been found in horsetail

ANRV410-PP61-12 ARI 31 March 2010 16:8
and in Choleochaete, a Charophycean green alga, XETs, though XyG quantitatively is a minor
but not in higher plants (39). hemicellulose.
Secondary walls and xylans. Cell wall mod- Source of Signal Molecules
els depicted in textbooks often focus on the pri- XyG plays an additional role as a source of
mary wall. The reason for this is that primary signal molecules. Breakdown products of XyG,
cell wall models inspire working hypotheses re- most notably XXFG, were demonstrated to
garding mechanisms required for cell growth. counteract auxin-induced cell expansion (151).
Xylan thus receives less attention though it is a This finding was verified and extended in a
major load-bearing structure in grasses as ex- series of seminal papers by McDougall and Fry
plained above. The important role of xylans (86, 87). It is remarkable that the optimal con-
in strengthening secondary walls is very clear centration for the inhibitory activity of XXFG
from analysis of xylan-deficient mutants. All is as low as 1 nM, and the term oligosaccharins
these contain collapsed xylem vessels and have was coined for these signal molecules. Other
severely impacted growth and fertility. Since XyG oligomers, XXLG and XLLG in partic-
such mutants grow better at high humidity, it ular, can promote cell expansion, albeit at a
seems that the main reason for the poor growth 1000-fold higher concentration (88). However,
is that water transport is adversely affected by this response is not regarded as signaling but
the poorly developed xylem. Xylans are also related to the action of XET. Research in
abundant in fiber cells, which do not have a XyG oligomers as substrates for XET has
water-conducting role. Therefore, xylan in this received much attention, whereas studies of the
type of cell might be more dispensable, but this oligosaccharin inhibitory activities dwindled at
has not been tested. the end of the nineties, and it is thus still not
clear how important these responses are in vivo.
Mannans. Apart from the role of galactoman- Mutants in XyG biosynthesis can have very
nans as seed storage compounds, it is un- strong phenotypes (132, 133), but as mentioned
clear what specific roles the mannans have. above, mutants devoid of XyG do not (22).
Mannans/glucomannans are highly conserved Perhaps the modified XyG in single mutants
through plant evolution. However, the only gives rise to different or increased amounts of
known effect of mutating mannan biosynthetic signal molecules and hence invokes a stronger
genes is the embryo-lethal phenotype of the response than wild-type plants. On the other
arabidopsis cslA7 mutant (47). In contrast, dele- hand, the lack of obvious phenotype of the
tion of the three glucomannan synthase genes mur2 mutant, which lacks XXFG (138), and of
expressed in arabidopsis stems resulted in plants xxt1/xxt2 mutants devoid of XyG altogether
lacking detectable glucomannan but without (22) suggests that if signaling by XyG fragments
obvious phenotype (46). Mutants in CSLD plays a role in plant growth and development, it
genes show severe effects on tip growth, either is not a very important one. The small amount
in root hair or pollen tubes (5), and mutants in of XyG present in grass cell walls would seem
several CSLD genes are severely dwarfed (150). unlikely to have an important structural role.
However, while preliminary evidence suggests Perhaps XyG has been maintained in grasses
that mannan biosynthesis is affected in the mu- for two reasons that are not mutually exclusive:
tants, this still needs additional work. because the XyG-derived oligosaccharins
In conclusion, hemicelluloses play a key role indeed are indispensable, and because the
in both primary and secondary walls. XyG holds process of de novo wall formation during cell
a special position in the cell wall, as reflected in division generally is more conserved among
the repertoire of enzymes available for its ma- angiosperm families than is the mature primary
nipulation. This applies also to the commelinid wall structure and hence XyG is required for
monocots, which express a full complement of wall assembly during cytokinesis in grasses.

ANRV410-PP61-12 ARI 31 March 2010 16:8
Information on a signaling role for hemicel- and locust bean gums (galactomannans), kon-
luloses other than XyG is very limited. In con- jak gum (glucomannan), and tamarind gum
trast, many studies have shown that fragments (xyloglucan). In addition, the hemicelluloses
of pectin play a role in the signaling of pathogen give important properties to many food and
attack and induce a pathogen response (7, 30). feed products. In the baking industry, the
insoluble arabinoxylans affect baking quality.
β-(1→3,1→4)-glucans and arabinoxylans are
Seed Storage Carbohydrates well-known antinutritional compounds in an-
Hemicelluloses in the cell wall have the primary imal feed, and they can cause filtering and
role of interacting with other polymers to en- haze problems in the brewery industry due
sure the proper physical properties of the wall. to their viscosity. To alleviate these problems,
However, in a large number of cases, hemicel- hemicellulose-degrading enzymes are added to
luloses have been recruited to the function of feed and are used in the baking and brewery
seed storage carbohydrate (90, 116). This has industries. On the other hand, β-(1→3,1→4)-
happened independently many times in evo- glucan has a documented cholesterol-lowering
lution, and it has been suggested that from a effect in hypercholesterolemic humans (67) and
taxonomic viewpoint hemicelluloses are as im- daily intake of β-(1→3,1→4)-glucans is recom-
portant as starch is in the role as storage car- mended by the U.S. Food and Drug Adminis-
bohydrate in seeds (90). Much of our knowl- tration. In cellulosic biofuel production, hemi-
edge of hemicelluloses comes from the study of celluloses affect the saccharification of biomass,
seed polysaccharides rather than the polymers and the released sugars, largely pentoses, are
in vegetative tissues. XyG is abundant in plants less desirable for fermentation than hexoses.
such as nasturtium and tamarind. Galactoman- It is beyond the scope of this review to dis-
nans are known from a large number of eco- cuss all of these industrial applications. How-
nomically important plants, e.g., coconut, guar, ever, due to the economic and nutritional im-
and locust bean. Galactomannans are especially portance of hemicelluloses, several researchers
abundant in the endosperm of legumes but also have attempted or suggested modification in
occur in other seeds. Glucomannan is present in the hemicellulose composition of plants. Xy-
the konjak plant (Amorphophallus konjac); in this lan feruloylation has been decreased by express-
case the storage organ is a corm and not the ing ferulic acid esterases in transgenic plants
seed. Arabinoxylans are present in seeds of di- with mixed results (11, 12, 51). To overcome
cots such as flax and psyllium (36, 96) and also the problem of high-pentose content in bio-
in cereal endosperm. Cereal endosperm addi- fuel production, it has been suggested that xy-
tionally contains β-(1→3,1→4)-glucans. lan could be replaced with mannan (101). The
apparently highly specialized function of xylans
in vessels and lignin interactions suggests to us
ENGINEERING OF CELL WALLS that a complete substitution could be very dif-
Hemicelluloses have commercial significance. ficult. Instead, a more specific replacement in
Seed storage hemicelluloses are used directly fiber cells would seem to have a higher chance
as products in the food industry, e.g., guar of success.
SUMMARY POINTS
1. Hemicelluloses are wall polysaccharides, which are characterized by β-(1→4)-linked
backbones of sugars in an equatorial configuration. This definition includes xyloglucans,
xylans, mannans and glucomannans, and β-(1→3,1→4)-glucans.

ANRV410-PP61-12 ARI 31 March 2010 16:8
2. All the hemicelluloses show differences in structural details between different species and
in different cell types within plants.
3. The main role of hemicelluloses is to tether cellulose microfibrils, thereby strengthening
the cell wall.
4. Xyloglucans dominate in primary walls of dicots and conifers, whereas (glu-
curono)arabinoxylans dominate in commelinid monocots.
5. Hemicelluloses are synthesized by glycosyltransferases located in the Golgi membranes.
The backbones of xyloglucan, mannan, and β-(1→3,1→4)-glucans are synthesized by
members of the cellulose synthase–like gene family, which are multimembrane-spanning
proteins.
6. Xylan backbones are apparently synthesized by glycosyltransferases that are Type II
membrane proteins with a single membrane-spanning segment, but none of these has
been unambiguously identified. Xylans in many, if not all, plants have a unique tetrasac-
charide in the reducing end, which appears to be involved in biosynthesis either as a
primer or a termination sequence.

7. Hemicelluloses are important components in food and feed and constitute a major part
of lignocellulosic biomass.
DISCLOSURE STATEMENT
The authors are not aware of any affiliations, memberships, funding, or financial holdings that
might be perceived as affecting the objectivity of this review.
ACKNOWLEDGMENTS
The work of H. V. Scheller on hemicelluloses is supported by the U.S. Department of Energy,
Office of Science, Office of Biological and Environmental Research, through contract DE-AC02-
05CH11231 between Lawrence Berkeley National Laboratory and the U.S. Department of En-
ergy. The work of P. Ulvskov is supported via grants from the Villum-Kann Rasmussen Foundation
and from the Danish Agency for Science, Technology and Innovation. The work of both authors
is supported by a grant from the 7th Framework Programme of the European Commission to the
project “Renewall,” project no. 211982.
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Annual Review of
Plant Biology
Contents Volume 61, 2010
A Wandering Pathway in Plant Biology: From Wildflowers to

Phototropins to Bacterial Virulence
Winslow R. Briggs p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 1
Structure and Function of Plant Photoreceptors

Andreas Möglich, Xiaojing Yang, Rebecca A. Ayers, and Keith Moffat p p p p p p p p p p p p p p p p p p p p p21
Auxin Biosynthesis and Its Role in Plant Development

Yunde Zhao p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p49
Computational Morphodynamics: A Modeling Framework to
Understand Plant Growth
Vijay Chickarmane, Adrienne H.K. Roeder, Paul T. Tarr, Alexandre Cunha,
Cory Tobin, and Elliot M. Meyerowitz p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p65
Female Gametophyte Development in Flowering Plants
Wei-Cai Yang, Dong-Qiao Shi, and Yan-Hong Chen p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p89
Doomed Lovers: Mechanisms of Isolation and Incompatibility in Plants
Kirsten Bomblies p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 109
Chloroplast RNA Metabolism
David B. Stern, Michel Goldschmidt-Clermont, and Maureen R. Hanson p p p p p p p p p p p p p p 125
Protein Transport into Chloroplasts
Hsou-min Li and Chi-Chou Chiu p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 157
The Regulation of Gene Expression Required for C4 Photosynthesis
Julian M. Hibberd and Sarah Covshoff p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 181
Starch: Its Metabolism, Evolution, and Biotechnological Modification
in Plants
Samuel C. Zeeman, Jens Kossmann, and Alison M. Smith p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 209
Improving Photosynthetic Efficiency for Greater Yield
Xin-Guang Zhu, Stephen P. Long, and Donald R. Ort p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 235
Hemicelluloses
Henrik Vibe Scheller and Peter Ulvskov p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 263
Diversification of P450 Genes During Land Plant Evolution
Masaharu Mizutani and Daisaku Ohta p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 291
v
AR410-FM ARI 6 April 2010 15:25
Evolution in Action: Plants Resistant to Herbicides

Stephen B. Powles and Qin Yu p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 317
Insights from the Comparison of Plant Genome Sequences
Andrew H. Paterson, Michael Freeling, Haibao Tang, and Xiyin Wang p p p p p p p p p p p p p p p p 349
High-Throughput Characterization of Plant Gene Functions by Using
Gain-of-Function Technology
Youichi Kondou, Mieko Higuchi, and Minami Matsui p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 373
Histone Methylation in Higher Plants
Chunyan Liu, Falong Lu, Xia Cui, and Xiaofeng Cao p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 395
Genetic and Molecular Basis of Rice Yield

Yongzhong Xing and Qifa Zhang p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 421
Genetic Engineering for Modern Agriculture: Challenges and
Perspectives
Ron Mittler and Eduardo Blumwald p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 443
Metabolomics for Functional Genomics, Systems Biology, and
Biotechnology
Kazuki Saito and Fumio Matsuda p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 463
Quantitation in Mass-Spectrometry-Based Proteomics
Waltraud X. Schulze and Björn Usadel p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 491
Metal Hyperaccumulation in Plants
Ute Krämer p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 517
Arsenic as a Food Chain Contaminant: Mechanisms of Plant Uptake
and Metabolism and Mitigation Strategies
Fang-Jie Zhao, Steve P. McGrath, and Andrew A. Meharg p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 535
Guard Cell Signal Transduction Network: Advances in Understanding
Abscisic Acid, CO2 , and Ca2+ Signaling
Tae-Houn Kim, Maik Böhmer, Honghong Hu, Noriyuki Nishimura,
and Julian I. Schroeder p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 561
The Language of Calcium Signaling
Antony N. Dodd, Jörg Kudla, and Dale Sanders p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 593
Mitogen-Activated Protein Kinase Signaling in Plants
Maria Cristina Suarez Rodriguez, Morten Petersen, and John Mundy p p p p p p p p p p p p p p p p p 621
Abscisic Acid: Emergence of a Core Signaling Network
Sean R. Cutler, Pedro L. Rodriguez, Ruth R. Finkelstein, and Suzanne R. Abrams p p p p 651
Brassinosteroid Signal Transduction from Receptor Kinases to
Transcription Factors
Tae-Wuk Kim and Zhi-Yong Wang p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 681
vi Contents
AR410-FM ARI 6 April 2010 15:25
Directional Gravity Sensing in Gravitropism

Miyo Terao Morita p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 705
Indexes
Cumulative Index of Contributing Authors, Volumes 51–61 p p p p p p p p p p p p p p p p p p p p p p p p p p p 721
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Errata
An online log of corrections to Annual Review of Plant Biology articles may be found at
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ANRV410-PP61-12 ARI 31 March 2010 16:8

Annu. Rev. Plant Biol. 2010. 61:263–89 Key Words

to 100 times their original length, and the pri-

compounds, notably lignin, constitute up to

264 Scheller · Ulvskov

backbone structure, we think they should not a Hemicellulose repeating disaccharides

such as cross-linking glycans have been pro-

since it is not obvious that cross-linking is a

still use the term hemicelluloses as a convenient

www.annualreviews.org • Hemicelluloses 265

Lycophyta (club mosses and spike mosses)

Charaphyacean green algae +

MY (algae with higher-plant-like walls) MY

Table 1 Occurrence of hemicelluloses in primary and secondary walls of plants

266 Scheller · Ulvskov

Fer Fer OMe

Galactomannan, typical of Fabaceae seeds.

Galactoglucomannan, typical of conifer wood.

www.annualreviews.org • Hemicelluloses 267

268 Scheller · Ulvskov

O O O O Ferulate esters bound to cell walls have

restricted to stomata and therefore perhaps

www.annualreviews.org • Hemicelluloses 269

an arabidopsis mutant that is lacking the major

β-(1→3,1→4)-glucans Glycosyltransferases. Many of the biosyn-

270 Scheller · Ulvskov

Table 2 Glycosyltranserases involved in hemicellulose biosynthesis

www.annualreviews.org • Hemicelluloses 271

shown that speciﬁc apoplastic glycosidases are

272 Scheller · Ulvskov

end of the cleaved

www.annualreviews.org • Hemicelluloses 273

Reducing end oligosaccharide. As men- a close homolog to IRX10, which as mentioned

d-Xylp-(1→3)-α-l-Rhap-(1→2)-α-d-GalpA- can function in vitro as a xylosyltransferase

274 Scheller · Ulvskov

end terminator sequence would normally HO O O O

www.annualreviews.org • Hemicelluloses 275

276 Scheller · Ulvskov

quently trimmed by α-galactosidases. Thus, the synthesize β-(1→3,1→4)-glucan when trans-

www.annualreviews.org • Hemicelluloses 277

model has become the most inﬂuential to date.

278 Scheller · Ulvskov

www.annualreviews.org • Hemicelluloses 279

280 Scheller · Ulvskov

www.annualreviews.org • Hemicelluloses 281

primer or a termination sequence.

282 Scheller · Ulvskov

www.annualreviews.org • Hemicelluloses 283

in the grasses. Plant Physiol. 149:27–37

Press. 330 pp.

284 Scheller · Ulvskov

www.annualreviews.org • Hemicelluloses 285

286 Scheller · Ulvskov

www.annualreviews.org • Hemicelluloses 287

132. Tamura K, Shimada T, Kondo M, Nishimura M, Hara-Nishimura I. 2005. KATAMARI1/MURUS3 is

288 Scheller · Ulvskov

trisaccharide by feruloyl-CoA: arabinoxylan-trisaccharide O-hydroxycinnamoyl transferase from Oryza

www.annualreviews.org • Hemicelluloses 289

Contents Volume 61, 2010

A Wandering Pathway in Plant Biology: From Wildﬂowers to