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Plant cell wall polymers as precursors for biofuels
Markus Pauly1 and Kenneth Keegstra
Current Opinion in Plant Biology 2010, 13:305–312
also qualitative differences in their components. Sensitive
analytical techniques can be used to identify and characterize specific wall components at the tissue or cellular
level. Sensitive mass spectrometric methods have been
developed to analyze wall fragments released by enzymes
from laser-dissected plant tissues [3]. Not surprisingly,
the vascular tissues contained very different components
from those in other leaf tissues. Even differences in the
substitution patterns of the hemicellulose xyloglucan
between the outer wall of leaf epidermal cells and the
walls derived from the entire layer were observed, indicating that there are local structural differences within
xyloglucan from different parts of a single cell. More
significantly, the use of molecular probes, such as specific
stains [4] and antibodies, reveals an amazing diversity of
patterns ([5]; Figure 1). A number of monoclonal antibodies that recognize different epitopes on xylan [6],
arabinan [7,8], or xyloglucan [9,10,11] have been used
to demonstrate very specific patterns of distribution among
cell types and within the wall of single cells. We need to
consider this compositional complexity of plant feedstocks
when evaluating and assessing the robustness of technical
processes converting biomass to biofuels.
This review comes from a themed issue on
Physiology and metabolism
Edited by Uwe Sonnewald and Wolf B. Frommer
Wall composition and fuel production
processes
The conversion of plant biomass into liquid transportation fuels
is a complex process that could be simplified by altering the
ratios of the cell wall polymers that constitute the main biomass
components. The composition of biomass varies naturally
depending upon plant species and cell type, including some
highly specialized walls that consist mainly of a single
component. Progress is being made in understanding the
molecular basis of these natural variations in wall composition.
This new knowledge will be a valuable resource that can be
used during efforts to generate designer biofuel crops using
either selected breeding methods or recombinant DNA
techniques.
Address
DOE Great Lakes Bioenergy Research Center, DOE Plant Research Lab,
Department of Biochemistry and Molecular Biology, Michigan State
University, East Lansing, MI 48824, USA
Corresponding author: Keegstra, Kenneth ([email protected])
1
Current address: Energy Biosciences Institute, Department of Plant
and Microbial Biology, Calvin Lab, University of California-Berkeley,
Berkeley, CA, USA.
Available online 22nd January 2010
1369-5266/$ – see front matter
# 2010 Elsevier Ltd. All rights reserved.
DOI 10.1016/j.pbi.2009.12.009
Introduction
Plant cell wall polymers have received significant attention in recent years because they are the major components in the plant biomass that is under consideration
as a source of reduced carbon to partially replace fossil
fuels. Although plant biomass is often considered as
having a uniform composition, there is in fact substantial
diversity in composition that arises from two important
areas. First, different species of plants have significant
differences in the proportions of cellulose, hemicellulose,
and lignin found in their biomass and, further, important
differences in the types of hemicelluloses and/or the
ratios of monomers in lignin [1,2]. In addition to these
species-specific differences, the average composition of a
single species, which is often quite uniform, hides a great
deal of diversity. Every plant consists of many different
cell types, each with a unique cell wall that contains not
only different ratios of wall components, but sometimes
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Lignocellulosic biomass can be utilized as a feedstock for
biofuel production in a number of ways. Depending on the
process, different attributes in wall composition are
required or desired. One approach, similar to that used
in the corn ethanol industry, entails degradation of the
polysaccharides in the lignocellulosic feedstock to monosaccharides, and their subsequent fermentation to ethanol
or other advanced biofuels. The remaining lignin residue
can be used to generate heat, for example, for ethanol
distillation. The major challenge in this process is that
plants have evolved wall structures that are recalcitrant to
biological degradation [1,12]. Hence, the biomass must be
subjected to such energy-intensive and cost-intensive
treatments as steam, weak acid, or non-aqueous ammonia
[13]. In addition, a high enzyme loading is required to
release fermentable glucose monomers from cellulose
because of its tight linkage with hemicelluloses and lignin
in native walls. Therefore, one major research objective of
plant scientists is to make walls more open and accessible
to enzymatic degradation. One way to enhance enzyme
accessibility would be to increase the water solubility of
polysaccharides. This shift in the ratio of less soluble to
more soluble polysaccharides could be achieved by an
increase in the abundance of amorphous glucan chains
rather than crystalline microfibrils of cellulose; addition of
side chain substitutions to the backbone of hemicelluloses,
Current Opinion in Plant Biology 2010, 13:305–312
306 Physiology and metabolism
Figure 1
Another issue is the fermentability of the released monosaccharides. Currently, yeasts used in the ethanol fermentation process utilize only hexoses such as glucose
and mannose. However, the most common hemicellulosic
polysaccharides consist mainly of xylose and arabinose,
pentoses that do not ferment so readily. Progress has been
made in developing specialized yeast and bacterial strains
that can ferment these pentoses, but they are not yet very
efficient [16]. Therefore, one desirable change in biomass
is an increased abundance of hexose-containing polymers
such as cellulose or mannans rather than xylans.
Another process used to convert lignocellulosic biomass
to fuel is a catalyst-based chemical process [17,18]. However, this process is hampered by inhibiting components,
such as phenolic compounds or aliphatic acids, present to
varying degrees in the degraded biomass [19]. One plant
breeding goal should thus be to reduce the abundance of
such compounds to a minimum.
An alternative way to produce fuels is by combustion and
gasification of lignocellulosics to syngas (carbon-monoxide, carbon-dioxide, and hydrogen gas) that can be transformed to ethanol via microbes [20] or hydrocarbons by
the Fischer–Tropsch process. The advantage of the gasification process is that not only the polysaccharides but
also the carbon present in lignin is available for fuel
production. For these processes, the composition and
aggregation status of the various polymers within the
lignocellulosic material does not play a role, but low water
and ash content are desirable [21].
Native structural diversity of plant cell walls
The wall composition and structure of differentiated cells in plants are
diverse. Sections of plant tissues stained for lignin [69] and viewed with
an inverted microscope (panel a) or with fluorescent-tagged antibodies
directed against specific polysaccharide epitopes [7,8] and viewed by
fluorescence microscopy (panels b–f) reveals that the wall structural
diversity can be observed not only in different cell types (a, b, f), but also
in different layers or areas of a single cell (c, d, e).
a: Section of the first internode of a maize stem stained with
phloroglucinol (courtesy of Debra Goffner, CNRS Castanet Tolosan).
b: Section from the first internode of a maize stem stained with
Mirande’s reagent (courtesy of Debra Goffner, CNRS Castanet Tolosan).
c/d: Immunofluorescence detection of pectic arabinan epitopes present
in the parenchyma cells of an Arabidopsis inflorescence stem. Two
antibodies recognising different arabinan epitopes (c-LM13; d-LM16)
label distinct different regions of those cells (courtesy of Paul Knox,
University of Leeds).
e: In tobacco stem sections a certain pectic arabinan epitope (LM16) is
observed only in xylem fiber cells and phloem cells.
f: Mature fibers of hemp: localization of an arabinogalactan-protein
epitope (visulaized by JIM14) at the inner side of secondary walls
(courtesy of Paul Knox, University of Leeds).
thereby decreasing hydrogen bonding with cellulose
microfibrils; the creation of a more easily degradable lignin
through the introduction of specific easily cleavable monolignols [2,14]; and/or a reduction of lignin–hemicellulose
linkages [15].
Current Opinion in Plant Biology 2010, 13:305–312
When thinking about strategies for changing the composition of plant cell walls, whether in terms of abundance of
certain polymers or substitution patterns of specific polymers, one can gain significant insights by looking into
nature’s ‘laboratory’. Certain plant species have evolved
specialized tissues that have unusual wall compositions,
that is, they contain elevated levels of cellulose, hemicellulose, or lignin (for overview see Figure 2).
Specialized cells that make cellulose
One of the best-studied examples is the seed trichome of
cotton, in which the fiber cells have secondary walls
containing almost pure cellulose [22]. Studies of this
system have revealed many important features of cellulose biosynthesis, including the first identification of the
cellulose synthase genes in plants [23]. In recent years,
progress has been made in identifying the regulatory
events that allow the deposition of almost pure cellulose
in cotton fibers [24]. Cotton fiber development is a complex process that involves many events, including the
action of various hormones [25], but some of the key
transcription factors have been identified [26,27]. A
detailed understanding of the metabolic and regulatory
events needed for a single cell to convert almost all of its
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Cell Walls and Biofuels Pauly and Keegstra 307
Figure 2
Examples of specialized tissues in plants that produce predominantly a single cell wall polymer.
Cellulose—Mature cotton plants (upper left) produce cotton fibers (lower left), whose secondary walls that are nearly pure cellulose (courtesy of
Candice Haigler, E. Roberts, and E. Hequet, NC State University). Poplar trees (upper right) produce tension wood (lower right) with walls that are also
nearly pure cellulose (courtesy of Frank Telewski and Jameel Al-Haddad, Michigan State University).
Hemicelluloses—Fenugreek plants (upper left) produce seeds containing endosperm walls (lower left) that are largely galactomannan. Psyllium plants
(upper center) produce seeds surrounded by a mucilaginous layer (lower center) with walls rich in arabinoxylan. Nasturtium plants (upper right)
produce seeds where the cotyledon cells (lower right) have a wall that is largely xyloglucan (courtesy of Marlene Cameron, Curtis Wilkerson, Michigan
State University).
Lignin—Pine trees (upper panel) produce compression wood (lower panel) that is enriched in lignin with a different composition from normal wood
(courtesy of Frank Telewski and Jameel Al-Haddad, Michigan State University).
carbon resources into a single polysaccharide, cellulose,
should be useful in efforts to manipulate and enhance
cellulose deposition, thereby increasing C6 sugar abundance in biofuel crops.
the work of Cocuron et al. [35], who used studies of
developing nasturtium seeds, which store xyloglucan, to
provide evidence that the xyloglucan glucan synthase is
encoded by a CslC gene.
Specialized cells that make a single hemicellulose
The fact that these seeds are capable of making a single
hemicellulosic polysaccharide, while not making other
parts of the wall, indicates that these biosynthetic pathways can be regulated independently from other wall
components. Furthermore, the use of cell wall polymers
as reserve carbohydrates occurs in several unrelated
plants [28], indicating that this trait has arisen independently many times during the evolution of land plants. If
correct, this logic would lead to the conclusion that only a
few changes are needed to accomplish this change in
regulation and that it could be done by design to modify
the walls of biofuel crops.
Many plant species create a special cell wall in the
endosperm or cotyledon cells of developing seeds [28].
These cell wall polysaccharides serve as reserve carbohydrates, being synthesized during seed development
and later mobilized during seedling germination. Seeds
that store galactomannan or xyloglucan are abundant in
nature [28], but there are seeds or other tissues that
produce other polymers in specialized cells, such as
psyllium seeds, which make arabinoxylan in a special
layer of epidermal cells [29].
Studies of developing seed systems have led to the
identification of genes and enzymes involved in hemicellulose biosynthesis. For example, studies of developing guar seeds led to the conclusion that mannan
synthase is encoded by a CslA gene [30], and more recent
studies have confirmed that this conclusion is valid for
most plant species [31,32], including coffee [33].
Recently, Goubet et al. [34] used reverse genetics to
provide convincing in vivo evidence to further support
the earlier conclusions. Another example comes from
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Changes in wall composition due to environmental
responses
Plants have the capacity to react to environmental stimuli
by changing their metabolism. Reprogramming cell wall
polymer biosynthesis is no exception. For example, as a
response to mechanical stresses, such as wind or changes
in gravitational stimuli, trees can develop specialized
tissues known as reaction wood [36]. This type of wood
enables the return of stems back to a vertical orientation.
Current Opinion in Plant Biology 2010, 13:305–312
308 Physiology and metabolism
Reaction wood of gymnosperms, known as compression
wood, develops on the lower side of branches. Regular
gymnosperm wood contains lignin that lacks syringyl
units and consists almost entirely of guaiacyl units,
whereas compression wood contains higher amounts of
lignin that is particularly enriched in p-hydroxyphenyl
units [37]. The higher abundance is probably due to
elevated expression of enzymes in the lignin metabolic
pathway [38]. Consequently, silencing one of those genes
(4-coumarate-ligase) resulted in an up to 50% reduction of
lignin in the tracheary elements [39], severely dwarfing
the plant and altering bark and wood anatomy. Compression wood also has alterations in polysaccharides with
reduced levels of cellulose and glucomannans compared
to regular wood.
By contrast, the reaction wood of angiosperms, such as
poplar, develops on the upper side of branches and is
termed tension wood. Tension wood fibers form a distinct
additional inner gelatinous layer, the G-layer, with highly
elevated cellulose content (95% vs. 45% in regular vessel
elements; [40]). A detailed analysis of the transcriptome
and metabolome of the G-layer in poplar demonstrated a
higher transcript level of sucrose synthase, suggesting an
increased carbon flux into cellulose production [41]. Concomitantly, pathways for the production of the hemicelluloses and lignin were downregulated. Also, specific
cellulose synthase genes are upregulated in the G-layer,
probably because they contain mechanical stress-responsive elements in their promoters [42]. Despite its reduced
abundance, xyloglucan is present in the G-layer and its
metabolism by xyloglucan endotransglycosylases has
been proposed to play a major role in conferring the
mechanical properties of the G-layer and its connection
to the adjacent S2 layer [40,43].
Another example of a distinct wall structure made by a
plant cell is the papilla formed at the site where a
pathogenic fungus attempts to penetrate a plant cell.
A papilla, a local apposition of a multi-layered wall
structure, contains callose, structural proteins, and lignin [44]. All of these components are produced as a
result of the plant cell’s sensing mechanism triggered by
invading pathogens and are necessary to form a first line
of defense against this pathogen [45]. Genetic evidence
has been presented that components of the secretory
system are responsible for the distinct location of the
papilla [46].
The lesson that one can learn from these various wall
systems is that plant cells are able to undergo reprogramming of their wall biosynthetic machinery, including but not limited to diverting the flow of
assimilated carbon, altered regulation of glycan
synthases, glycosyltransferases, monolignol synthetic
enzymes, and the secretory system. This reprogramming results in fundamentally different and unique
Current Opinion in Plant Biology 2010, 13:305–312
wall materials that have an altered ratio of components
or even different components. Understanding how the
cell accomplishes this task will provide valuable knowledge that will enable rational changes of cell wall
composition that will allow enhanced biofuel production.
Strategies for manipulating wall composition
Knowledge regarding the regulation of wall polymer
biosynthesis remains largely elusive. The mechanisms
by which plant cells regulate the flow of carbon into wall
polymers and balance the quantities of the various wall
polymers are hot topics for research. Photosynthetic
assimilates are used as the building blocks for wall polysaccharide biosynthesis. One of the first enzymes that
utilizes the newly fixed carbon is sucrose synthase
(SuSy), which converts sucrose into UDP-glucose and
fructose. Recently, it has been shown that overexpressing
SuSy in poplar leads to a higher proportion and absolute
amount (2–6%) of cellulose in fiber cells [47], demonstrating that this enzyme might be a key determinant
regulating cellulose biosynthesis. Interestingly, the
increase in wall cellulose content had very little detrimental effect on the plant, as growth and biomass
remained similar to non-transformed plants when grown
in the greenhouse.
UDP-glucose or other hexose-phosphates are used as a
substrate for the nucleotide sugar conversion pathway
that results in the synthesis of the 14 different nucleotide
sugars necessary for the various wall polymers [48].
Hence, manipulating these enzymes could lead to alteration in cell wall composition. Although most of the genes
encoding the nucleotide sugar conversion enzymes are
known and their activities have been demonstrated in
vitro [48], very few studies have demonstrated that
manipulation of their expression leads to significant cell
wall changes. Overexpression of these enzymes has so far
not yielded plants with altered wall compositions,
possibly because of the redundancy of genes encoding
many of the sugar nucleotide metabolizing enzymes. For
example, a concomitant reduction of several UDP-glucose epimerase transcripts led to not only a decrease in
wall galactose levels [49], but also severe changes in root
growth. Hence, such changes would presumably lead to
less biomass in the plant.
Another strategy for modifying the composition of cell
walls is to upregulate or downregulate the levels of
glycosyltransferases and glycan synthases that polymerize the sugars from nucleotide sugars into polysaccharides. Cavalier et al. [10] created an Arabidopsis plant
lacking two genes encoding xyloglucan xylosyltransferases and showed that xyloglucan could not be
detected in mutant plants. Interestingly, the mutant
plants grew and developed relatively normally, although
they were slightly smaller than wild-type plants and had
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Cell Walls and Biofuels Pauly and Keegstra 309
abnormal root hairs. It remains to be determined what
polymers are substituting for xyloglucans in the primary
wall of these mutant plants, but one important conclusion from these studies is that it is possible to make
dramatic alterations in the hemicellulose composition of
a plant without serious consequences for its ability to
grow and reproduce.
Reid et al. [50] were the first to successfully modify the
composition of a cell wall polysaccharide by overexpressing a gene encoding a glycosyltransferase. They used a
constitutive promoter to express the galactomannan
galactosyltransferase from fenugreek in tobacco plants.
The higher levels of galactosyltransferase activity led to
an increase in the galactosyl substitution of the galactomannan that is normally found in the walls of seed
endosperm cells. Efforts to modify the mannan content
of seeds by overexpression of a mannan synthase gene led
to a more complex result. Naoumkina et al. [51] used a
seed-specific promoter to overexpress the mannan
synthase gene from guar in Medicago truncatula plants.
The transgenic Medicago seeds had a lower rather than a
higher level of galactomannan, but the molecular weight
and viscosity of the polymers were significantly
increased. In addition, the authors found that overexpression of the mannan synthase gene caused large
changes in the levels of various sugars and sugar alcohols
as well as significant changes in the expression of more
than 900 genes, with more than 300 genes upregulated
and almost 600 genes expressed at lower levels. The
major conclusion from this study is that overproduction of
a cell wall polysaccharide cannot be accomplished simply
by upregulation of the gene responsible for polymer
backbone synthesis.
One system where considerable progress has been made
in understanding the regulation of wall polymer biosynthesis on a molecular level is differentiating vascular
elements, especially the deposition of secondary walls in
xylem cells (see the review by Demura and Ye [52] in
this issue). These unique cell walls are the most abundant component of harvested biomass crops and thus
deserve special mention. Many of the genes involved in
cellulose and lignin biosynthesis have been identified
and progress is being made on identifying the genes
required for the biosynthesis of xylan [53–55], the hemicellulose found in the vascular tissues of most potential
bioenergy crops. More importantly, key regulatory genes
that control the formation of vascular elements [56,57]
and many of the components in the transcriptional network that controls secondary wall biosynthesis have
been identified in recent years [58–61], including two
transcriptional activators of the lignin biosynthetic pathway [62]. It is interesting to consider the possibility
that discrete transcription factors independently
regulate the cellulose, hemicellulose, and lignin pathways. The deposition of these three components is
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normally coordinated during wall biosynthesis [63]. If
it is possible to control the deposition of each separately,
then it should be possible to modify secondary walls in
ways that will allow the production of designer walls in
biomass crops.
It should not be surprising that the flow of carbon into a
major reserve polysaccharide requires the coordinated
expression of many genes involved in the synthesis of
that polymer. Combining the information of key regulatory genes with the promoters specific for various cell
types of the vascular system [56,57] should make it
possible to modify the composition of the secondary cell
walls of various cell types in stems or other vegetative
tissues.
Investigating the biological consequences
Any strategy to improve the composition of lignocellulosics as feedstocks for the production of biofuels needs to
assess the performance of the modified plants. Owing to
the multiple functions of the wall during the life cycle of a
plant, there could be numerous problems, including a
reduction in plant growth and a concomitant reduction in
lignocellulosic biomass. Biomass yield concessions such
as dwarfism have been shown in a number of mutants
[64], whereas in others the yield under greenhouse conditions does not seem to be affected [65]. Altering the
walls can lead to changes in cell morphology. One detrimental example of changes in secondary wall structure
are irregular xylem cells [66] leading to a loss in watertransporting capacity resulting in a reduction in biomass.
Another function of the wall is to ward off plant pathogens
such as bacteria and fungi [45]; structural changes in the
wall might lead to increased susceptibility. However, in a
few cases where pathogen infection has been tested on
wall mutants, resistance was not reduced [67], and in
some cases was even increased [68].
Concluding remarks
Plant biomass is being considered as a feedstock for the
production of biofuels and other chemicals. Because the
traits that are desirable for these uses vary depending
upon the method utilized for biomass processing, and
because the desirable traits differ from those needed for
more traditional uses of plants for food and fiber production, much discussion has focused on modifying the
composition and cell wall properties in ways that will
improve the biomass for these new applications. As such
modifications are considered, it is important to be aware
that nature has already created plant cells with diverse
walls, not only those surrounding the differentiated cells
found in every plant, but also those in various specialized
cells that occur in many plants. Understanding how the
walls of these differentiated and specialized cells are
synthesized will provide valuable clues on how to modify
the cell walls of plants that are grown as designer biofuel
crops.
Current Opinion in Plant Biology 2010, 13:305–312
310 Physiology and metabolism
Acknowledgements
The authors would like to thank Paul Knox, University of Leeds, Debra
Goffner, CNRS Castanet Tolosan, Candice Haigler, North Carolina State
University, and Frank Telewski, Jameel Al-Haddad, Curtis Wilkerson,
Marlene Cameron, Michigan State University for providing photographs
depicted in Figures 1 and 2. The authors would like to express their
appreciation of research funding by the US Department of Energy (DOE)
Great Lakes Bioenergy Research Center (DOE BER Office of Science DEFC02-07ER64494) and by the Chemical Sciences, Geosciences and
Biosciences Division, Office of Basic Energy Sciences, Office of Science,
U.S. Department of Energy (award no. DE-FG02-91ER20021).
References and recommended reading
Papers of particular interest, published within the annual period of
review, have been highlighted as:
of special interest
of outstanding interest
1.
Pauly M, Keegstra K: Cell-wall carbohydrates and their
modification as a resource for biofuels. Plant J 2008,
54:559-568.
2.
Vanholme R, Morreel K, Ralph J, Boerjan W: Lignin engineering.
Curr Opin Plant Biol 2008, 11:278-285.
Obel N, Erben V, Schwarz T, Kuhnel S, Fodor A, Pauly M:
Microanalysis of plant cell wall polysaccharides. Mol Plant
2009, 2:922-932.
The authors push the envelope on the microscale of chemical analyses of
wall materials using distinct wall collection techniques such as laserdissection catapulting or organelle fractionation in combination with mass
spectrometry. As a result clear structural differences in a wall polymer of
different areas of a single cell was demonstrated.
3.
4.
Anderson CT, Carroll A, Akhmentova L, Somerville C: Real time
imaging of cellulose reorientation during cell wall expansion in
Arabidopsis roots. Plant Physiol 2009 doi: 10.1104/
pp.109.150128.
5.
Knox JP: Revealing the structural and functional
diversity of plant cell walls. Curr Opin Plant Biol 2008,
11:308-313.
6.
Herve C, Rogowski A, Gilbert HJ, Knox JP: Enzymatic treatments
reveal differential capacities for xylan recognition and
degradation in primary and secondary plant cell walls. Plant J
2009, 58:413-422.
7.
Verhertbruggen Y, Marcus SE, Haeger A, Verhoef R, Schols HA,
MCCLEARY BV, Mckee L, Gilbert HJ, Knox JP: Developmental
complexity of arabinan polysaccharides and their processing
in plant cell walls. Plant J 2009, 59:413-425.
The authors characterized three new monoclonal antibodies specific for
different epitopes present on arabinan and other polysaccharides that
contain arabinose. They used the new antibodies to evaluation the
distribution of the arabinan epitopes. The results demonstrated that
polysaccharides containing these epitopes are distributed in complex
patterns that vary between various cell types that differ among plant
species.
8.
9.
Blake AW, Marcus SE, Copeland JE, Blackburn RS, Knox JP: In
situ analysis of cell wall polymers associated with phloem
fibre cells in stems of hemp, Cannabis sativa L. Planta 2008,
228:1-13.
Freshour G, Clay RP, Fuller MS, Albersheim P, Darvill AG,
Hahn MG: Developmental and tissue-specific structural
alterations of the cell-wall polysaccharides of Arabidopsis
thaliana roots. Plant Physiol 1996, 110:1413-1429.
10. Cavalier DM, Lerouxel O, Neumetzler L, Yamauchi K, Reinecke A,
Freshour G, Zabotina OA, Hahn MG, Burgert I, Pauly M et al.:
Disrupting two Arabidopsis thaliana xylosyltransferase genes
results in plants deficient in xyloglucan, a major primary cell
wall component. Plant Cell 2008, 20:1519-1537.
Disruption of two genes encoding xyloglucan xylosyltransferases resulted
in the production of plants that minor phenotypic consequences, but that
lacked dectectable xyloglucan. According to current models for the
organization of polymers in primary cell walls, this change should have
dramatic consequences. While it is not yet clear how the plants survive as
well as they do, the results demonstrate that it is possible to make
Current Opinion in Plant Biology 2010, 13:305–312
signficant changes to wall composition without major consequence for
the growth of the mutant plants.
11. Zabotina OA, van de Ven WTG, Freshour G, Drakakaki G,
Cavalier D, Mouille G, Hahn MG, Keegstra K, Raikhel NV:
Arabidopsis XXT5 gene encodes a putative alpha-1,6xylosyltransferase that is involved in xyloglucan biosynthesis.
Plant J 2008, 56:101-115.
12. Carroll A, Somerville C: Cellulosic biofuels. Annu Rev Plant Biol
2009, 60:165-182.
13. Sousa LD, Chundawat SPS, Balan V, Dale BE: ‘Cradle-to-grave’
assessment of existing lignocellulose pretreatment
technologies. Curr Opin Biotechnol 2009, 20:339-347.
14. Grabber JH, Hatfield RD, Lu FC, Ralph J: Coniferyl ferulate
incorporation into lignin enhances the alkaline delignification
and enzymatic degradation of cell walls. Biomacromolecules
2008, 9:2510-2516.
The authors provide evidence for one promising approach of overcoming
the recalcitrance of plant cell wall degradation for biofuel production.
Here, a substitution of an ether linked monolignol with an ester-conjugate
increased lignin extractability at lower temperatures and thus reducing
the costly energy input into the process. The remaining fibers could then
be more readily converted into fermentable units.
15. Grabber JH, Mertens DR, Kim H, Funk C, Lu FC, Ralph J: Cell wall
fermentation kinetics are impacted more by lignin content and
ferulate cross-linking than by lignin composition. J Sci Food
Agric 2009, 89:122-129.
16. Van Vleet JH, Jeffries TW: Yeast metabolic engineering for
hemicellulosic ethanol production. Curr Opin Biotechnol 2009,
20:300-306.
17. Binder JB, Raines RT: Simple chemical transformation of
lignocellulosic biomass into furans for fuels and chemicals. J
Am Chem Soc 2009, 131:1979-1985.
18. Huber GW, Chheda JN, Barrett CJ, Dumesic JA: Production of
liquid alkanes by aqueous-phase processing of biomassderived carbohydrates. Science 2005, 308:1446-1450.
19. Larsson S, Reimann A, Nilvebrant NO, Jonsson LJ: Comparison
of different methods for the detoxification of lignocellulose
hydrolyzates of spruce. Appl Biochem Biotechnol 1999, 77–
79:91-103.
20. Datar RP, Shenkman RM, Cateni BG, Huhnke RL, Lewis RS:
Fermentation of biomass-generated producer gas to ethanol.
Biotechnol Bioeng 2004, 86:587-594.
21. Tijmensen MJA, Faaij APC, Hamelinck CN, van Hardeveld MRM:
Exploration of the possibilities for production of Fischer
Tropsch liquids and power via biomass gasification. Biomass
Bioenergy 2002, 23:129-152.
22. Kim HJ, Triplett BA: Cotton fiber growth in planta and in vitro.
Models for plant cell elongation and cell wall biogenesis. Plant
Physiol 2001, 127:1361-1366.
23. Pear JR, Kawagoe Y, Schreckengost WE, Delmer DP, Stalker DM:
Higher plants contain homologs of the bacterial celA genes
encoding the catalytic subunit of cellulose synthase. Proc Natl
Acad Sci USA 1996, 93:12637-12642.
24. Al-Ghazi Y, Bourot S, Arioli T, Dennis ES, Llewellyn DJ: Transcript
profiling during fiber development identifies pathways in
secondary metabolism and cell wall structure that may
contribute to cotton fiber quality. Plant Cell Physiol 2009,
50:1364-1381.
25. Singh B, Cheek HD, Haigler CH: A synthetic auxin (NAA)
suppresses secondary wall cellulose synthesis and enhances
elongation in cultured cotton fiber. Plant Cell Rep 2009,
28:1023-1032.
26. Shangguan XX, Xu B, Yu ZX, Wang LJ, Chen XY: Promoter of a
cotton fibre MYB gene functional in trichomes of Arabidopsis
and glandular trichomes of tobacco. J Exp Bot 2008,
59:3533-3542.
27. Machado A, Wu YR, Yang YM, Llewellyn DJ, Dennis ES: The MYB
transcription factor GhMYB25 regulates early fibre and
trichome development. Plant J 2009, 59:52-62.
www.sciencedirect.com
Cell Walls and Biofuels Pauly and Keegstra 311
28. Reid JSG: Cell-wall storage carbohydrates in seeds biochemistry of the seed gums and hemicelluloses. Adv Bot
Res 1985, 11:125-155.
29. Fischer MH, Yu NX, Gray GR, Ralph J, Anderson L, Marlett JA: The
gel-forming polysaccharide of psyllium husk (Plantago ovata
Forsk). Carbohydr Res 2004, 339:2009-2017.
30. Dhugga KS, Barreiro R, Whitten B, Stecca K, Hazebroek J,
Randhawa GS, Dolan M, Kinney AJ, Tomes D, Nichols S,
Anderson P: Guar seed beta-mannan synthase is a member of
the cellulose synthase super gene family. Science 2004,
303:363-366.
47. Coleman HD, Yan J, Mansfield SD: Sucrose synthase affects
carbon partitioning to increase cellulose production and
altered cell wall ultrastructure. Proc Natl Acad Sci USA 2009,
106:13118-13123.
For the first time it has been demonstrated that the absolute abundance of
cellulose can be increased in a tree by overexpressing sucrose synthase.
This has been achieved without any apparent detrimental effect on plant
growth or biomass yield. The data in this seminal paper clearly underpin
the important role of carbon partitioning in wall polymer abundance.
48. Reiter W: Biochemical genetics of nucleotide sugar
interconversion reactions. Curr Opin Plant Biol 2008, 11:236-243.
31. Liepman AH, Wilkerson CG, Keegstra K: Expression of cellulose
synthase-like (Csl) genes in insect cells reveals that CslA
family members encode mannan synthases. Proc Natl Acad Sci
USA 2005, 102:2221-2226.
49. Rosti J, Barton CJ, Albrecht S, Dupree P, Pauly M, Findlay K,
Roberts K, Seifert GJ: UDP-glucose 4-epimerase isoforms
UGE2 and UGE4 cooperate in providing UDP-galactose for cell
wall biosynthesis and growth of Arabidopsis thaliana. Plant
Cell 2007, 19:1565-1579.
32. Liepman AH, Nairn CJ, Willats WGT, Sorensen I, Roberts AW,
Keegstra K: Functional genomic analysis supports
conservation of function among cellulose synthase-like a
gene family members and suggests diverse roles of mannans
in plants. Plant Physiol 2007, 143:1881-1893.
50. Reid JSG, Edwards ME, Dickson CA, Scott C, Gidley MJ:
Tobacco transgenic lines that express fenugreek
galactomannan galactosyltransferase constitutively have
structurally altered galactomannans in their seed endosperm
cell walls. Plant Physiol 2003, 131:1487-1495.
33. Pre M, Caillet V, Sobilo J, McCarthy J: Characterization
expression analysis of genes directing galactomannan
synthesis in coffee. Ann Bot 2008, 102:207-220.
51. Naoumkina M, Vaghchhipawala S, Tang YH, Ben YX, Powell RJ,
Dixon RA: Metabolic and genetic perturbations accompany the
modification of galactomannan in seeds of Medicago
truncatula expressing mannan synthase from guar (Cyamopsis
tetragonoloba L.). Plant Biotechnol J 2008, 6:619-631.
34. Goubet F, Barton CJ, Mortimer JC, Yu XL, Zhang ZN, Miles GP,
Richens J, Liepman AH, Seffen K, Dupree P: Cell wall
glucomannan in Arabidopsis is synthesised by CSLA
glycosyltransferases, and influences the progression of
embryogenesis. Plant J 2009, 60:527-538.
35. Cocuron JC, Lerouxel O, Drakakaki G, Alonso AP, Liepman AH,
Keegstra K, Raikhel N, Wilkerson CG: A gene from the cellulose
synthase-like C family encodes a beta-1,4 glucan synthase.
Proc Natl Acad Sci USA 2007, 104:8550-8555.
36. Koehler L, Telewski FW: Biomechanics and transgenic wood.
Am J Bot 2006, 93:1433-1438.
37. Timell TE: Recent progress in the chemistry and topochemistry
of compression wood. Wood Sci Technol 1982, 16:83-122.
38. Zhang XH, Chiang VL: Molecular cloning of 4coumarate:coenzyme A ligase in loblolly pine and the roles of
this enzyme in the biosynthesis of lignin in compression wood.
Plant Physiol 1997, 113:65-74.
39. Wagner A, Donaldson L, Kim H, Phillips L, Flint H, Steward D,
Torr K, Koch G, Schmitt U, Ralph J: Suppression of 4coumarate-CoA ligase in the coniferous gymnosperm Pinus
radiata. Plant Physiol 2009, 149:370-383.
40. Mellerowicz EJ, Sundberg B: Wood cell walls: biosynthesis,
developmental dynamics and their implications for wood
properties. Curr Opin Plant Biol 2008, 11:293-300.
41. Andersson-Gunneras S, Mellerowicz EJ, Love J, Segerman B,
Ohmiya Y, Coutinho PM, Nilsson P, Henrissat B, Moritz T,
Sundberg B: Biosynthesis of cellulose-enriched tension wood
in Populus: global analysis of transcripts and metabolites
identifies biochemical and developmental regulators in
secondary wall biosynthesis. Plant J 2006, 45:144-165.
42. Lu SF, Li LG, Yi XP, Joshi CP, Chiang VL: Differential expression
of three eucalyptus secondary cell wall-related cellulose
synthase genes in response to tension stress. J Exp Bot 2008,
59:681-695.
43. Mellerowicz EJ, Immerzeel P, Hayashi T: Xyloglucan: the
molecular muscle of trees. Ann Bot 2008, 102:659-665.
44. Bhuiyan NH, Selvaraj G, Wei YD, KING J: Gene expression
profiling and silencing reveal that monolignol biosynthesis
plays a critical role in penetration defence in wheat
against powdery mildew invasion. J Exp Bot 2009,
60:509-521.
45. Hematy K, Cherk C, Somerville S: Host-pathogen warfare at the
plant cell wall. Curr Opin Plant Biol 2009, 12:406-413.
46. Lipka U, Fuchs R, Lipka V: Arabidopsis non-host resistance to
powdery mildews. Curr Opin Plant Biol 2008, 11:404-411.
www.sciencedirect.com
52. SPACE HOLDE FOR DEMURA ARTICLE IN CURRENT ISSUE.
53. York WS, O’Neill MA: Biochemical control of xylan biosynthesis
- which end is up? Curr Opin Plant Biol 2008, 11:258-265.
54. Brown DM, Zhang ZN, Stephens E, Dupree P, Turner SR:
Characterization of IRX10 and IRX10-like reveals an essential
role in glucuronoxylan biosynthesis in Arabidopsis. Plant J
2009, 57:732-746.
55. Wu AM, Rihouey C, Seveno M, Hornblad E, Singh SK,
Matsunaga T, Ishii T, Lerouge P, Marchant A: The Arabidopsis
IRX10 and IRX10-LIKE glycosyltransferases are critical for
glucuronoxylan biosynthesis during secondary cell wall
formation. Plant J 2009, 57:718-731.
56. Demura T, Fukuda H: Transcriptional regulation in wood
formation. Trends Plant Sci 2007, 12:64-70.
57. Zhong RQ, Ye ZH: Regulation of cell wall biosynthesis. Curr
Opin Plant Biol 2007, 10:564-572.
58. Zhong RQ, Lee CH, Zhou JL, McCarthy RL, Ye ZH: A battery of
transcription factors involved in the regulation of secondary
cell wall biosynthesis in Arabidopsis. Plant Cell 2008,
20:2763-2782.
59. Endo S, Pesquet E, Yamaguchi M, Tashiro G, Sato M, Toyooka K,
Nishikubo N, Udagawa-Motose M, Kubo M, Fukuda H, Demura T:
Identifying new components participating in the secondary
cell wall formation of vessel elements in Zinnia and
Arabidopsis. Plant Cell 2009, 21:1155-1165.
60. Ko JH, Kim WC, Han KH: Ectopic expression of MYB46
identifies transcriptional regulatory genes involved in
secondary wall biosynthesis in Arabidopsis. Plant J 2009,
60:649-665.
61. McCarthy RL, Zhong RQ, Ye ZH: MYB83 is a direct target of
SND1 and acts redundantly with MYB46 in the regulation of
secondary cell wall biosynthesis in Arabidopsis. Plant Cell
Physiol 2009, 50:1950-1964.
62. Zhou JL, Lee CH, Zhong RQ, Ye ZH: MYB58 and MYB63 are
transcriptional activators of the lignin biosynthetic pathway
during secondary cell wall formation in Arabidopsis. Plant Cell
2009, 21:248-266.
Two proteins that are part of the complex cascade of transcription factors
regulating secondary cell wall formation are shown to function as activators of lignin biosynthesis. As the authors point out in the discussion,
this observation raises the possibility that the various components present in secondary cell walls, that is, cellulose, xylan, and lignin, may each
be activated by pathway-specific transcription factors. Identification and
characterization of such transcription factors has important practical
consequences for efforts to manipulate biomass composition.
Current Opinion in Plant Biology 2010, 13:305–312
312 Physiology and metabolism
63. Mutwil M, Ruprecht C, Giorgi FM, Bringmann M, Usadel B,
Persson S: Transcriptional wiring of cell wall-related genes in
Arabidopsis. Mol Plant 2009, 2:1015-1024.
64. Desprez T, Juraniec M, Crowell EF, Jouy H, Pochylova Z, Parcy F,
Hofte H, Gonneau M, Vernhettes S: Organization of cellulose
synthase complexes involved in primary cell wall synthesis
in Arabidopsis thaliana. Proc Natl Acad Sci USA 2007,
104:15572-15577.
65. Mansfield SD: Solutions for dissolution-engineering cell walls
for deconstruction. Curr Opin Biotechnol 2009, 20:286-294.
66. Turner SR, Somerville CR: Collapsed xylem phenotype of
Arabidopsis identifies mutants deficient in cellulose
deposition in the secondary cell wall. Plant Cell 1997,
9:689-701.
Current Opinion in Plant Biology 2010, 13:305–312
67. Jacobs AK, Lipka V, Burton RA, Panstruga R, Strizhov N, SchulzeLefert P, Fincher GB: An Arabidopsis callose synthase, GSL5, is
required for wound and papillary callose formation. Plant Cell
2003, 15:2503-2513.
68. Hernandez-Blanco C, Feng DX, Hu J, Sanchez-Vallet A,
Deslandes L, Llorente F, Berrocal-Lobo M, Keller H, Barlet X,
Sanchez-Rodriguez C et al.: Impairment of cellulose
synthases required for Arabidopsis secondary cell wall
formation enhances disease resistance. Plant Cell 2007,
19:890-903.
69. Guillaumie S, San-Clemente H, Deswarte C, Martinez Y,
Lapierre C, Murigneux A, Barriere Y, Pichon M, Goffner D:
MAIZEWALL. Database and developmental gene expression
profiling of cell wall biosynthesis and assembly in maize. Plant
Physiol 2007, 143:339-363.
www.sciencedirect.com