Genome-wide gene expression in uro mutant

Genome-wide expression profiling in seedlings of the
Arabidopsis mutant uro that is defective in the
secondary cell wall formation
Zheng Yuan1 , Xuan Yao2 , Dabing Zhang2 , Yue Sun3 and Hai Huang1*
1 Graduate School of Chinese Academy of Sciences, National Laboratory of Molecular
Genetics, Shanghai Institute of Plant Physiology and Ecology, Shanghai Institute for
Biological Sciences, 300 Fenglin Road, Shanghai 200032, China
2 SJTU-SIBS-PSU Joint Center for Life Sciences, Key laboratory of Microbial
Metabolism, Ministry of Education, School of Life Science and Biotechnology, Shanghai
Jiao Tong University, 800 Dongchuan Road, Shanghai 200240, China
3 College of Life Science, East China Normal University, 3663 North Zhongshan
Road, Shanghai 200062, China
Supported by the Hi-Tech Research and Development (863) Program of China
(20060110Z1012) to H.H. and by a grant from the National Natural Science Foundation
of China (30570159) to Y.S.
Author for correspondence
Phone: +86 (0)21 5492 4088;
Fax: +86 (0)21 5492 4015;
The plant secondary growth is of tremendous importance, not only for plant growth
and development but also for economic utility.
Secondary tissues such as xylem
and phloem are the conducting tissues in plant vascular systems, essentially for
water and nutrient transport, respectively.
On the other hand, products of plant
secondary growth are important raw materials and renewable sources of energy.
Although advances have been recently made towards describing molecular
mechanisms that regulate secondary growth, the genetic control for this process is
not yet fully understood.
Secondary cell wall formation in plants shares some
common mechanisms with other plant secondary growth processes.
Thus, studies
on the secondary cell wall formation using Arabidopsis may help to understand the
regulatory mechanisms for plant secondary growth.
We previously reported
phenotypic characterizations of an Arabidopsis semi-dominant mutant, upright
rosette (uro), which is defective in secondary cell wall growth and has an unusually
soft stem.
Here, we show that lignification in the secondary cell wall in uro is
aberrant by analyzing hypocotyl and stem.
We also show genome-wide expression
profiles of uro seedlings, using Affymetrix GeneChip that contains approximately
24,000 Arabidopsis genes.
Genes identified with altered expression levels include
those that function in plant hormone biosynthesis and signaling, cell division and
plant secondary tissue growth.
These results provide useful information for
further characterizations of the regulatory network in plant secondary cell wall
Key words: cell wall lignification; lignin; microarray; secondary growth; upright rosette
Plant tissues can be generally classified into two kinds, primary tissues and
secondary tissues. Plant growth and differentiation of apical meristems result in the
formation of primary tissues such as epidermis, vascular bundles and piths.
primary tissues undergo secondary growth, leading to the production of secondary
tissues, such as wood (Ko et al. 2004).
In the primary tissues, a primary cell wall is
comprised of cellulose microfibrils, hemicelluloses (or cross-linking glycans) and pectic
Some cell types, by contrast, develop secondary cell walls that are
comprised mostly of cellulose and cross-linking glycans and can also be lignified
(Cosgrove 2005).
Elucidation of regulatory mechanisms for plant secondary growth is of extremely
importance, as most products of the secondary growth can serve as widely used industry
raw materials.
However, our current understanding of genetic control of the plant
secondary growth is limited. The secondary growth is predominantly in trees, but the
inherent problems of tree species such as long generation time, large size and lack of
genetically pure lines blocked the in-depth studies of the molecular genetic basis of plant
secondary growth.
In recent years, the model plant Arabidopsis has been used in
researches of secondary growth (Chaffey et al. 2002), and progress has been made in the
study of gene expression and signaling mechanisms responsible for secondary cell wall
formation, lignin and cellulose biosynthesis, and xylem development ( Chaffey et al.
2002; Cosgrove et al. 2002; Doblin et al. 2002; Boerjan et al. 2003; Oh et al. 2003;
Fukuda 2004; Cosgrove 2005; Ehlting et al. 2005; Zhao et al. 2005; Groover and
Robischon 2006).
Plant secondary cell wall formation shares some common
mechanisms with other secondary growth processes. For example, secondary cell wall
formation and wood formation in trees both require lignin biosynthesis and deposition.
However, little is known about a particular plant secondary growth question: the
regulatory mechanism underlying the coordinated expression of genes for secondary cell
wall formation.
We previously reported the identification and phenotypic characterizations of a
semi-dominant Arabidopsis mutant, designated upright rosette (uro) (Sun et al. 2000).
The uro mutant plant displayed pleiotropic phenotypes, including a loss of apical
dominance with very soft stems.
More detailed analyses showed that processes of
xylem and fiber differentiation were aberrant in the uro mutant, and thickening of the
secondary cell wall was delayed (Guo et al. 2004). These results imply that the uro
mutant could be used as a genetic source for exploring mechanisms of secondary cell
wall formation, and such studies may provide important information in understanding
plant secondary growth.
In the present study, we extended our characterizations of the uro mutant by
analyzing lignification process in the uro cell wall. We found that lignification level of
the secondary cell wall in uro hypocotyl and stem is significantly reduced.
For a better
understanding of mechanisms by which the plant secondary cell wall is regulated, we
performed Arabidopsis whole-transcriptome profiling analyses.
Functions of some
genes that may be involved in secondary cell wall formation are discussed.
uro mutation perturbs lignification in the secondary cell wall formation
To better understand the biology of the uro cell wall, we first performed a series of
sectioning with hypocotyls at seedling stages.
On day 6 after germination, the overall
phenotypes between wild-type Ler (Figure 1 A) and uro (Figure 1 B) hypocotyls of
light-grown seedlings were nearly identical.
Sections of hypocotyls at this stage
consisted of a uniseriate epidermis, a cortex containing two layers of parenchyma and
endodermis, and a stele in the center (Figure 1A , B). The first indication of hypocotyl
secondary cell growth was the appearance of anticlinal and periclinal divisions in the
procambial and pericycle cells, which proliferate to generate the vascular cambium and
the cork cambium (Chaffey et al. 2002).
Although the cellular pattern of uro hypocotyl
(Figure 1D) at this stage was similar to that of wild-type Ler (Figure 1C), the number of
tracheary elements of newly differentiated xylem in uro was obviously reduced.
addition, the secondary cell wall started to construct in wild-type hypocotyls at this stage,
by lignin deposition in cell walls of xylem tissues (Figure 1I), whereas this process was
not noted in those of the same-stage uro mutant (Figure 1J).
During the subsequent hypocotyl growth, xylem and phloem tissues developed
rapidly in wild-type seedlings and the whole hypocotyl became thick, as shown in the
25- and 38-day-old plants, respectively (Figure 1E, G). Although xylem and phloem
tissues also developed in uro hypocotyls, cell proliferation appeared restrained, resulting
in less thickened hypocotyls (Figure 1F, H).
Strikingly, lignification of xylem in
hypocotyls was accelerated in the 25- and 38-day-old hypocotyls in the wild-type
seedlings (Figure 1K, M). By contrast, this process is dramatically delayed, with no or
very minor lignification appearing in the 25- and 38-day-old uro hypocotyls, respectively
(Figure 1L, N). We also investigated lignification process of cell walls in the
inflorescence stem. Similarly, much less lignification in the uro stem was noted
(Figure 1P) as compared with that in the wild-type stem (Figure 1O). These results
strongly indicate that the gain-of-function uro mutation perturbs secondary cell wall
Genome-wide analyses of altered gene expression in uro seedlings
To investigate the uro mutation that affects secondary cell wall formation, we
analyzed global expression profiles of uro seedlings, using Affymetrix GeneChip that
represents about 24000 genes of Arabidopsis.
To avoid the indirect effects caused by
morphological changes from later uro development, we used 6-day-old seedlings from
which morphological differences between wild-type and uro mutant were not visible
(Figure 1A, B). Probe sets were normalized for each microarray according to a
previously reported method (Redman et al. 2004).
From two biological replicates,
1769 genes were identified with consistent changes in transcript levels in uro, with the
increased and decreased transcription of 816 and 953 genes, respectively.
These genes
were grouped into 4 categories: (I) information storage and processing, (II) cellular
processes and signaling, (III) metabolism, and (IV) genes with unknown functions, and
could be further divided into 27 subgroups as shown in Figure 2.
Altered expression levels of the plant hormone-related genes
Our previous phenotypic characterizations of the mutant led us to propose that the
dominant uro phenotypes may be related to the defective auxin action in Arabidopsis
(Guo et al. 2004).
Our GeneChip results further supported this idea that auxin content
and signaling in uro may be abnormal.
It is known that the YUCCA genes encoding a
favin monooxygenase-like enzyme catalyze hydroxylation of the amino group of
tryptamine, a rate-limiting step in the tryptophan dependent auxin biosynthesis ( Zhao et
al. 2001;Cheng et al. 2006).
We found that the level of one YUCCA gene, YUCCA1,
was markedly elevated in uro (Table 1).
On the other hand, levels of several genes
involving auxin signaling, including IAA19 and a number of auxin responsive genes,
were decreased (Table 1).
These results strongly suggests that auxin signaling in uro
mutant is abnormal, consistent with the uro auxin defective phenotypes such as loss of
apical dominance and delayed vascular differentiation (Guo et al. 2004).
Crosstalk of different hormone signaling pathways has become clear in recent years
in higher plants (Gazzarrini and McCourt 2003). Our data showed that in addition to
the auxin pathway, expression of genes in other hormone pathways was also altered.
The IPT genes, encoding adenylate isopentenyltransferase, may play important roles in
the cytokinin biosynthesis (Sakakibara 2005).
However, transcription level of the IPT3
gene in uro was increased (Table 1). Similarly, the Arabidopsis AMP1 gene, which
plays roles in shoot apical meristems maintenances, cell proliferation,
photomorphogenesis, and flower timing, is also required for the regulation of the
endogenous cytokinin level (Helliwell et al. 2001), whereas was up-regulated in uro
(Table 1).
These results suggest that the altered gene expressions might affect hormone
levels and responses in the uro mutant, and thus cause the severe uro morphological
Expression of genes relating to the secondary tissue growth
As shown in the phenotypic analyses of uro hypocotyls and stems, secondary tissue
growth was markedly delayed and lignification level was reduced in the uro mutant
(Figure 1). Consistent with the uro phenotypes, our microarray data revealed that
expression of a number of genes involved in cell division and cell wall deposition was
changed in uro (Table 1).
Interestingly, 177 genes (more than 10% of all expression
altered genes) correlating to the secondary tissue growth (Ehlting et al. 2005; Zhao et al.
2005) changed their expression levels in the uro mutant (see supplementary Table 1).
These expression changes in the uro mutant were consistent with our cellular
observations of hypocotyls and stems, suggesting that the uro soft stem may be mainly
caused by defects in the secondary cell wall formation (Figure 1).
Validation of gene expression in profiling experiments by RT-PCR
To test the reliability of our microarray results, we performed RT-PCR analyses
using cDNAs from the same-stage wild type and uro seedlings.
different altered levels were selected in the RT-PCR experiments.
Genes that represent
These genes include
GA2 (At1g79460), IPT6 (At1g25410), RGL3 (At5g17490), IAA1 (At4g14560), IAA19
(At3g15540), FMO (YUCCA1) (At4g32540), AMP1 (At3g54720), CYC2b (At4g35620),
CYC1 (At4g37490), CYC2a (At2g17620), EXPL3 (At3g45960), XTR9 (At4g25820),
XTR6 (At4g25810), and genes encoding glycosyl hydrolase family protein 85
(At3g61000) and glycosyl transferase family protein 48 (At1g06490), respectively.
genes examined using RT-PCR showed the expression consistency with those from
genome-wide transcript profiles, indicating the reliability of our microarray data.
Despite the prominent roles of plant secondary growth in the economy as well as in
plant development, the molecular mechanisms are well understudied when trees were
used as experimental materials.
In recent years, several research groups have examined
the whole-genome gene expression pattern in developing xylem tissues and revealed
some components that might be important for secondary tissue growth ( Oh et al. 2003;
Ko and Han 2004; Ko et al. 2004; Ehlting et al. 2005; Zhao et al. 2005).
These studies
provided important information in elucidating the regulatory mechanisms by which the
plant secondary growth is controlled.
However, it is still far from fully understanding
of the complete process of plant secondary growth.
In this study, we demonstrate an
alternative approach by characterizing the Arabidopsis uro mutant, in which the
secondary cell wall formation is defective.
Hypocotyl is a tissue that was often used as a model for studying the mechanism of
cell development and a variety of biological events that participate in its developmental
control, because of the simplicity of its cell types and structures (Vandenbussche et al.
Different from wild-type plant, cell proliferation and cell wall lignification in
the uro hypocotyl is severely blocked, resulting in reduced numbers of vascular cells and
much less accumulated lignin in the secondary cell walls of both hypocotyl and stem.
Cellulose is known to be another important composition in forming secondary cell walls.
In addition to lignin, cellulose contents in secondary cell wall of uro may also be reduced,
as transcription level of the IRX9 gene which encodes an important glycosyl transferase
for cellulose synthesis (Pena at al. 2007) was dramatically down-regulated (Table 1).
Furthermore, a group of genes, which encode putative xyloglucan endotransglycosylase
(XTH) and play a critical role in secondary cell wall formation (Vissenberg et al. 2005a,
b) were also negatively regulated in the uro mutant (Table 1).
We previously reported that the uro mutant has very soft inflorescence stem, due to
the poorly developed interfascicular fiber cells (Guo et al. 2004).
In the present study,
we propose that the cellular base of the soft uro stem is due to a lack of lignin and
cellulose accumulation in the secondary cell walls.
Plant cell lignification is a complex
process, undergoing from lignin biosynthesis in the cell to deposition to the place where
the plant secondary cell wall forms (Sederoff et al. 1999). Based on the uro phenotypic
analyses, we propose that cell states in uro may protect cells from lignification.
known that dividing cells or cells in the young stages are not lignified.
It is
Growth pattern
analyses showed that hypocotyls of uro were in a retarded cell division and
differentiation manner, which may result in an elongated primary cell growth phase
without secondary cell wall formation.
This hypothesis was supported by the
observation that cell division was slowed and xylem and phloem tissues were delayed to
form in the uro hypocotyl.
The plant lignification process is known to be closely related to the plant hormone
actions (Biemelt et al. 2004; Zhao et al. 2005; Groover and Robischon 2006).
In our
microarray analyses, a number of genes that are involved in the hormone biosynthesis
and signaling in uro were changed in their expression levels.
We previously proposed
that the uro mutation may affect auxin regulatory pathways, because uro single mutant
showed some auxin action defective phenotypes such as the loss of apical dominance.
In addition, uro mutation can genetically interact with pin1, a mutant with a defective
auxin polar transporter, and uro pin1 double mutant plants had very severe pleiotropic
phenotypes (Guo et al. 2004).
Several functional categories of auxin, including signal
perception/transduction, auxin transport, and auxin-mediated transcriptional regulation
and cellulose biosynthesis, were identified to be involved in secondary growth program
(Zhao et al. 2005).
The lignification defect in the secondary cell wall formation,
together with other auxin action defective phenotypes in the uro mutant, is consistent
with expression changes of the auxin-action related genes.
Additionally, our GeneChip
array data also showed that expressions of a number of genes that associate with other
hormone pathways were changed.
It was previously reported that several other plant
hormones can influence secondary cell wall formation. For example, cytokinins,
ethylene, GAs, brassinosteroids and xylogan all demonstrated their roles in affecting
vascular differentiation, though the underlying mechanisms are not clear ( Sachs 2000;
Fukuda 2004).
Since crosstalk among hormone pathways occurs in many plant growth
and developmental processes and the uro mutant demonstrated several auxin defective
phenotypes (Guo et al. 2004), it is possible that the altered expression levels of other
hormone related genes may be caused by an indirect effect.
Our data also revealed the altered expression levels of cell cycle and cell division
related genes as well as the cell wall deposition related genes in the uro mutant.
results might explain some of the uro mutant phenotypes, including the aberrant xylem
and phloem cell division and the abnormal lignin deposition in the secondary cell walls.
However, we cannot exclude a possibility that the expression changes of these genes may
occur downstream of the hormone regulation.
Since the uro phenotypes were caused
by a single nuclear gene mutation (Sun et al. 2000), isolation of the URO gene would
help further elucidation of molecular mechanisms of the secondary cell wall formation.
Materials and Methods
Plant materials and growth conditions
The Arabidopsis mutant uro, which is in the Landsberg erecta (Ler) genetic
background, was generated previously from a T-DNA mutagenesis experiment (Sun et al.
For histological and microarray analyses, wild-type and uro seeds were
sterilized with 70% ethanol for 15 min, followed by 5 washes using distilled water.
sterilized seeds were sowed on plates containing 1% agar and PNS salts (Estelle and
Somerville 1987), kept in 4 °C for 3 days and then moved to a growth chamber in 22 °C
under white fluorescent light (200 μmol m-2 s-1) with a photo period of 16 h light and 8 h
Histology and microscopy
Six- to 38-day-old plants were used for hypocotyl and stem section observations.
Hypocotyls of Ler and uro mutant were fixed in FAA (formalin:acetic acid:50% ethanol
= 5:5:90, v/v), and then dehydrated through a graded series of ethanol. The hypocotyl
specimens were embedded in resin overnight according to a previously described method
(Chaffey et al. 2002), and sliced into 10–15 m sections, which were subsequently
stained with 0.05% toluidine blue O (TBO) for 1.5 minutes, rinsed with water. The
resultant sections were then sealed for observation.
For lignin examination, resin
sections of hypocotyls (Ruellanda et al. 2003) or manual sections of stems (Guo et al.
2004) were stained with 1% phloroglucinol containing 70% ethanol for 2 minutes,
followed by treatment with the concentrated HCl.
Photos were taken according to our
previous method (Guo et al. 2004).
Microarray and data analyses
Seedlings of 6-day-old wild-type and homozygous uro plants were collected for total
RNA extraction, using the RNAiso Reagent (TaKaRa, Dalian). RNAs from two
duplicate plant materials were used for labelling and hybridization, performed by Gene
Tech Biotechnology Company (Shanghai), according to the standard Affymetrix
protocol (Affymetrix, Santa Clara, CA, USA, The Affymetrix GeneChip
ATH1 array was used in the array experiment.
A coefficient of log 2 was used as the
selection criterion for differential gene expression between wild-type Ler and uro mutant
The value for gene expression is average of the two corresponding duplicates,
and changes of transcript levels greater than twice were used for functional category
analyses, using the COG software (, with manual
adjustment when necessary (Tatusov et al. 2001).
Reverse transcription-polymerase chain reaction
Reverse transcription-polymerase chain reaction (RT-PCR) was performed
according our previous method (Xu et al. 2003), with ACTIN as an internal control.
Genes and their specific primers that were used in the RT-PCR are listed below: for
ent-kaurene synthase gene, 5-CGGTTGCTTCTGGTTTCTTTATGTCTATCA-3 and
5-TGGTTTCTGTATGGTTTCATCAGTGAC-3; for adenylate isopentenyltransferase 6
5-CTCCTCTACTCCTATCGTCTTCCGAA-3; for gibberellin response modulator gene,
5-TTCAGGTAGGGACACGAGTCGTAG-3; for auxin-responsive protein gene,
5-AGACAATGGATCATAAGGCAGTAGG-3; for indoleacetic acid-induced protein 19
5-TGTTCAAGTCATCATCACTCGTCTAC-3; for flavin-containing monooxygenase
5-TGACCATCCATAAACTTTGCTCC-3; for putative glutamate carboxypeptidase gene,
5-ATCCTCCATCTCAACTTCTTCC-3; for G2/mitotic-specific cyclin gene,
5-TGCGAGGTCATTCTCAACATCAGC-3; for putative cyclin gene,
5-CCACTGTTACATCCTCCATCTCAACT-3; for expansin family protein gene,
5-TGACCTCCTTGGTACAATAGCTTTATC-3; for endo-xyloglucan transferase gene,
5-TCTCGTTGTTCTTGAACACCCG-3; for putative endo-xyloglucan transferase gene,
5-GAATTCTCTTATGGGAGTTCCATCCA-3; for glycosyl hydrolase family protein 85
5-CCATGTTTAGAGGTTTCATCTGATGT-3; for glycosyl transferase family 48
protein gene, 5-GGAACTTCGTACCGTAGCTCA-3 and
5-TAGTTTGGAACTCAGACACAAATG-3; and for cyclin family protein,
The authors would like to thank B. Xu for critical reading of this manuscript.
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Figure Legends
Figure 1. Secondary cell wall formation is defective in the uro mutant.
From (A) to (H), sections were from the central part of hypocotyls and were stained with
0.05% toluidine blue O.
(A) A section from 6-day-old wild-type Ler.
(B) A section from 6-day-old uro.
(C) A section from 12-day-old Ler.
(D) A section from 12-day-old uro.
(E) A section from 25-day-old Ler.
(F) A section from 25-day-old uro.
(G) A section from38-day-old Ler.
(H) A section from 38-day-old uro hypocotyl.
Note that the cell division and differentiation of xylems in uro were retarded (arrow).
From (I) to (P), sections were from the central part of hypocotyls and were stained with
1% phloroglucinol-HCl for lignin content analyses.
(I) A section from 12-day-old Ler.
(J) A section from 12-day-old uro.
(K) A section from 25-day-old Ler.
(L) A section from 25-day-old uro.
(M) A section from 38-day-old Ler.
(N) A section from 38-day-old uro showing that a few tracheary elements started to be
(O) and (P) Sections from central inflorescence stems of 5-week-old plants.
(O) A section from Ler.
(P) A section from uro.
Note that the lignin deposition was blocked in both uro hypocotyl and stem (arrows).
co, cortex; cop, cortex parenchyma; cz, cambial zone; e, epidermis; en, endodermis; if,
interfascicular fiber; ip, interfascicular fiber precursor; pc, procambium; pe, pericycle; ph,
phloem; pi, pith; st, stele; te, tracheary elements; v, vessel element; x, xylem.
From (A)
to (P), bars = 50 μm.
Figure 2. Functional categorizations of genes that showed altered expression levels in
the uro mutant.
The software Clusters of Orthologous Groups (COG) from web site was used for gene functional categorization.
Translation, ribosomal structure and biogenesis; 2, RNA processing and modification; 3,
Transcription; 4, Replication, recombination and repair; 5, Chromatin structure and
dynamics; 6, Cell cycle control, cell division, chromosome partitioning; 7, Nuclear
structure; 8, Defense mechanisms; 9, Signal transduction mechanisms; 10, Cell
wall/membrane/envelope biogenesis; 11, Cell motility; 12, Cytoskeleton; 13,
Extracellular structures; 14, Intracellular trafficking, secretion, and vesicular transport;
15, Posttranslational modification, protein turnover, chaperones; 16, Energy production
and conversion; 17, Carbohydrate transport and metabolism; 18, Amino acid transport
and metabolism; 19, Nucleotide transport and metabolism; 20, Coenzyme transport and
metabolism; 21, Lipid transport and metabolism; 22, Inorganic ion transport and
metabolism; 23, Secondary metabolites biosynthesis, transport and catabolism; 24,
General function prediction only; 25, Unnamed genes; 26, Function unknown; 27, genes
that are not found in this category system.
Figure 3. RT-PCR analyses of selected genes with altered expression levels in the uro
ACTIN transcripts were used as the internal control. RT-PCR was performed using
cDNA from the same stage seedlings as those used in GeneChip arrays.
Genes were
selected from three clusters, including the hormone-correlated, cell cycle/division-related,
and cell wall deposition-related clusters. G, genomic DNA.
Table 1 Selected genes from the initial 1769 genes that showed altered expression levels
in the uro seedling.
Plant hormone-related
Gene description
Log2 ratio
Auxin-responsive protein, putative
Auxin-responsive protein, putative
Auxin-responsive protein (IAA1)
Auxin efflux carrier family protein
Auxin-responsive family protein
Indoleacetic acid-induced protein 19 (IAA19)
Flavin-containing monooxygenase (YUCCA1)
Gibberellin 2-oxidase (GA2OX3)
Cytokinin synthase (IPT3)
Glutamate carboxypeptidase (AMP1)
Tubulin beta-1 chain (TUB1)
Actin depolymerizing factor 5
Actin-depolymerizing factor, putative
D-type cyclin
Cyclin, putative
Cyclin, putative
Cyclin family protein
Glycosyl transferase family 43 protein (IRX9)
Putative pectinesterase
Endo-xyloglucan transferase (EXT) (EXGT-A1)
Similar to xyloglucan endotransglycosylase (XTH19)
Similar to xyloglucan endotransglycosylase (XTH20)
Putative xyloglucan endo-transglycosylase
Similar to xyloglucan endotransglycosylase (XTH17)
Endo-xyloglucan transferase, putative (XTR7)
Glycosyl hydrolase family protein 85
Endo-xyloglucan transferase, putative (XTR6)
Cell cycle/division-related
Cell wall deposition-related