Editorial: An Emerging View of Plant Cell Walls as an
Apoplastic Intelligent System
Kazuhiko Nishitani1,* and Taku Demura2
1
Laboratory of Plant Cell Wall Biology, Graduate School of Life Sciences, Tohoku University, 6-3 Aoba, Aramaki, Aoba-ku, Sendai, 890-8578 Japan
Graduate School of Biological Sciences, Nara Institute of Science and Technology, 8916-5 Takayama-cho, Ikoma, Nara, 630-0192 Japan
2
*Corresponding author: E-mail, [email protected]; Fax, +81-22-795-6669.
An overview of plant cell walls from a
conventional perspective
Cell walls of land plants (embryophytes) are multifunctional
cellular structures characterized by a framework of cellulose
microfibrils embedded in an amorphous matrix containing various structural and functional components. The wall consists of
three layers: the middle lamella, the primary cell wall and the
secondary cell wall (Popper 2008, Albersheim et al. 2010).
The middle lamella is derived from the cell plate, which is
formed during cytokinesis, and remains deposited between the
two layers of the primary cell wall, which are formed after the
completion of cell division and continue to be remodeled
during cell expansion. These two layers are ubiquitous in all
tissues of land plants. They contain abundant hydrophilic
matrix polysaccharides including pectins and xyloglucans, and
are responsible for regulation of cell–cell adhesion, cell expansion and determination of cell shape (Yokoyama et al. 2014). In
contrast, secondary cell walls are deposited internally to primary cell walls in specific cell types, such as vessels and fiber
cells of vascular plants, once cell expansion ceases. The secondary wall is characterized by deposition of lignin and/or suberin,
which render the wall chemically hydrophobic and impermeable to water, and is mechanically resistant to compression
stress. These physical and chemical properties are evidently
crucial for all vascular plants to remain upright, to take up
and translocate water and nutrients, and to defend themselves
from external biotic stress and abiotic attack (Oda and Fukuda
2012, Demura 2014, Malinovsky et al. 2014).
Three and a half centuries of cell wall
research
It was the suberized secondary cell walls derived from cork oak
(Quercus suber L.) that Robert Hooke first observed under his
microscope in 1665, and which he termed ‘cells’ (Hooke 1665).
His observation was followed by a more comprehensive microscopic dissection of cell walls in plant tissues and organs by
Nehemiah Grew in the 17th century (Grew 1682). These pioneering studies described plant cell walls as static and rigid.
Although by the 19th century the cell wall became recognized
as dynamic and critical for plant growth and development, it
was not until the 1970s that Peter Albersheim and colleagues
proposed a molecular–structural model of the primary cell wall
(Keegstra et al. 1973). The basis of this model was that certain
cross-links between cellulose microfibrils serve as load-bearing
linkages of the cell wall, and that their separation and reunion
are required for the cell wall to loosen and expand during cell
growth and differentiation. By the end of the last century, a set
of key enzymes implicated in cell wall construction, modification and disassembly had been isolated and characterized, and
their genes identified (reviewed by Cosgrove 2005). Since the
beginning of this century, integrated-omics approaches based
on genomic, transcriptomic and proteomic databases have
facilitated the comprehensive molecular dissection of cell wall
construction and function (Albenne et al. 2009, Usadel and
Fernie 2013, Demura 2014, Mewalal et al. 2014). More recently,
plant cell wall research has entered a new era thanks to the
development of advanced imaging technologies, such as highspeed atomic force microscopy (HS-AFM) (Igarashi et al. 2011)
and super resolution confocal live imaging microscope (SCLIM)
(Fujimoto et al. 2015).
Emerging views of the plant cell wall
To date, the plant cell wall is progressively being considered not
simply a structure or even an apparatus, but a system in charge of
sensing, processing and responding to internal and external cellular signals (Somerville et al. 2004), thereby functioning as an
intelligent frontier capable of processing information from the
environment and co-ordinating whole-plant growth by optimizing individual cell growth and differentiation (Engelsdorf and
Hamann 2014). Despite its importance and unique features,
both the process of cell wall construction and the mechanisms
of its intelligent function remain largely unknown, the elucidation of which could pave the way for understanding how individual cells of land plants can co-ordinate each other to control
the whole body in the absence of a nervous system.
Three approaches to elucidate plant cell wall
function
In this issue, we focus on three aspects pertaining to recent
advances in research on the plant cell wall as an information
processing system: (i) the molecular mechanisms for its construction; (ii) the molecular bases for its function; and (iii) the
Plant Cell Physiol. 56(2): 177–179 (2015) doi:10.1093/pcp/pcv001, available online at www.pcp.oxfordjournals.org
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function of the cell wall as an interface between cells and their
environment.
Molecular mechanisms for cell wall construction
Several thousand genes in plants are known to be involved in
cell wall construction, and their expression is highly regulated
during growth and differentiation of plant cells (Carpita et al.
2001). Only little is known about transcriptional regulation
of genes related to construction of primary cell walls,
e.g. the brassinosteroid-activated transcription factor BRI1EMS-SUPPRESSOR 1 (BES1) might regulate the expression of
genes encoding cellulose synthase catalytic subunits (CESAs)
for primary cell walls. On the other hand, the transcriptional
regulation of genes related to secondary cell wall construction
has been very well illustrated since the identification of a number of key transcription factors, such as VASCULAR-RELATED
NAC-DOMAIN6 (VND6), VND7, NAC SECONDARY WALL
THICKENING PROMOTING FACTOR (NST1), SECONDARY
WALL-ASSOCIATED NAC DOMAIN PROTEIN (SND1),
MYB46 (AT5G12870) and MYB83 (AT3G08500) (Demura and
Ye 2010, Zhong et al. 2010, Demura 2014). In this issue, Zhong
and Ye (2015) provide an update on the latest research regarding transcriptional regulation, where they comprehensively
review genes involved in the biosynthesis of secondary cell
wall components including cellulose, hemicellulose and lignin.
Such information is valuable for the genetic engineering of
secondary cell walls and, in this issue, Sakamoto and Mitsuda
(2015) clearly demonstrate that transmuted/artificial secondary cell walls with different characteristics can be synthesized in
Arabidopsis nst1 snd1/nst3 double mutants, which lack secondary cell walls in fiber cells, by the expression of chimeric proteins
comprising certain key transcription factors. While it has been
demonstrated that NAC transcription factors including VND1–
VND7, NST1 and SND1 are the main master switches in this
transcriptional network (Zhong and Ye 2015), knowledge about
the upstream elements regulating the expression of such
master switches is lacking. In this issue, Endo et al. (2015)
have now found that 14 transcription factors including
VND1–VND7, GATA12 and ANA075 are putative positive
regulators of one of these master switches, VND7.
The proper construction of plant cell walls is strongly dependent on the membrane trafficking system for a variety of
cell wall components (Sanchez-Rodriguez and Persson 2014). In
this issue, Fujimoto et al. (2015) reveal that phosphoinositides
potentially contribute to the localization and transport of one
of the primary cell wall CESAs, CESA3, and Oda et al. (2015)
show that novel coiled-coil proteins VETH1 and VETH2, which
interact with the conserved oligomeric Golgi complex 2
(COG2) protein, recruit an exocyst subunit EXO70A1 to cortical microtubules to ensure correct deposition of secondary
cell walls. During cell wall construction, various complex and
branched polysaccharides including pectins and hemicelluloses
are synthesized in the Golgi apparatus by Golgi membranelocalized glycosyltranferases. In this issue, Chou et al. (2015)
propose that several glycosyltranferases involved in xylogulucan
biosynthesis, including CSLC4, MUR3, XLT2, XXT2, XXT5 and
FUT1, form functional multiprotein complexes in the Golgi.
178
Molecular bases for cell wall function
As mentioned earlier, the cell wall model proposed by
Albersheim’s group in the 1970s envisaged pectin and xyloglucans as key components responsible for tethering cellulose
microfibrils, with xyloglucan coating most of the available
cellulose surface (Keegstra et al. 1973). Since then, this
model has been challenged and revised repeatedly (Carpita
and Gibeau 1993, Nishitani 1997, Cosgrove 2014). In this issue,
Park and Cosgrove (2015) put forward a revised structural
model for the cellulose–xyloglucan complex, in which they
propose that cellulose microfibrils are directly cross-linked
via xyloglucan at limited sites that function as load-bearing
bridges between cellulose microfibrils, termed ‘biochemical
hotspots’.
Pectin, on the other hand, seems to be more complicated
and versatile than xyloglucan in terms of both structure and
function (Atmodjo et al. 2013). It consists of several complex
domains including rhamnogalacturonan-I, rhamnogalacturonan-II and homogalacturonan. Although the biosynthesis
steps of these components are slowly being revealed, their overall structures are still controversial and their biological roles
remain largely unknown, especially in cereal plants. To address
this question, Sumiyoshi et al. (2015) targeted genes encoding
UDP-arabinopyranose mutase, which is responsible for synthesis of the arabinan side chain on rhamnogalacturonan-I. In this
issue, they demonstrate the critical role of the arabinan side
chain for development of reproductive tissues in rice.
The cell wall in rice is unique in that it contains abundant
(1;3/1;4)-b-D-glucan (or mixed linkage b-D-glucan; MLG) and
silicon. Although the individual roles of MLG and silicon in
growth and defense responses are known and their possible
association has been suggested (Fry et al. 2008), the molecular bases for their interactions are not well known. To gain
insight into the functional relationship between both compounds, Kido et al. (2015) have investigated the function and
distribution of silicon in the cell wall of transgenic rice in
which the MLG content is reduced. The authors propose
that MLG affects the function and distribution profile of
silicon in rice tissues without altering the uptake of silicon
by the plant.
The cell wall as an intelligent interface between
cells and their environment
A trade-off between growth promotion and resistance to environmental stress is a crucial strategy for the survival of all
organisms. In land plants, in which the cell wall plays a central
role in both growth regulation and defense response, such a
trade-off is often also mediated via the additional ‘intelligent
function’ of the cell wall. In this issue, Hofte (2015) reviews the
literature pertaining to an emerging view of how plant cells can
sense disruption of its cell wall and maintain its integrity via an
interplay between a positive (yin) and a negative (yang) signaling module. In addition, Hamann (2015) reviews the currently
available literature on the cell wall integrity maintenance mechanism of yeast and plants, paying special attention to the role of
turgor pressure in the latter.
Funding
This work is supported by a Grant-in-Aid for Scientific Research
on Innovative Areas for ‘Plant cell wall as information processing system’ (No. 24114001) from JSPS and MEXT, Japan.
Acknowledgments
Our special thanks are due to Professor Tomoyuki Yamaya,
Editor-in-Chief, for giving us the opportunity to organize and
edit this special focus issue on Plant Cell Walls, to Dr Liliana M.
Costa, Managing Editor, for helpful advice and assistance, and
to all the contributors and anonymous reviewers of these
articles.
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