Volume 13 Supplement 15
Comparative genomic analysis of NAC transcriptional factors to dissect the regulatory mechanisms for cell wall biosynthesis
© Yao et al.; licensee BioMed Central Ltd. 2012
Published: 11 September 2012
NAC domain transcription factors are important transcriptional regulators involved in plant growth, development and stress responses. Recent studies have revealed several classes of NAC transcriptional factors crucial for controlling secondary cell wall biosynthesis. These transcriptional factors mainly include three classes, SND, NST and VND. Despite progress, most current analysis is carried out in the model plant Arabidopsis. Moreover, many downstream genes regulated by these transcriptional factors are still not clear.
In order to identify the key homologue genes across species and discover the network controlling cell wall biosynthesis, we carried out comparative genome analysis of NST, VND and SND genes across 19 higher plant species along with computational modelling of genes regulated or co-regulated with these transcriptional factors.
The comparative genome analysis revealed that evolutionarily the secondary-wall-associated NAC domain transcription factors first appeared in Selaginella moellendorffii. In fact, among the three groups, only VND genes appeared in S. moellendorffii, which is evolutionarily earlier than the other two groups. The Arabidopsis and rice gene expression analysis showed specific patterns of the secondary cell wall-associated NAC genes (SND, NST and VND). Most of them were preferentially expressed in the stem, especially the second internodes. Furthermore, comprehensive co-regulatory network analysis revealed that the SND and MYB genes were co-regulated, which indicated the coordinative function of these transcriptional factors in modulating cell wall biosynthesis. In addition, the co-regulatory network analysis revealed many novel genes and pathways that could be involved in cell wall biosynthesis and its regulation. The gene ontology analysis also indicated that processes like carbohydrate synthesis, transport and stress response, are coordinately regulated toward cell wall biosynthesis.
Overall, we provided a new insight into the evolution and the gene regulatory network of a subgroup of the NAC gene family controlling cell wall composition through bioinformatics data mining and bench validation. Our work might benefit to elucidate the possible molecular mechanism underlying the regulation network of secondary cell wall biosynthesis.
As a potential replacement for traditional fossil fuels, biofuels have received increased public and scientific attention in recent years . The current first generation biofuel is based on sugar and starch derived from feedstocks such as sugrarcane and corn; however, this platform is not sustainable for various reasons. Lignocellulosic biomass has been proposed as the major feedstock for second generation biofuels to enable the transition from fossil fuel-based energy to renewable energy for the various economic and environmental advantages gained over first generation biofuels [1, 2]. Generally speaking, lignocellulosic biomass is composed of cellulose, hemicellulose, pectin and/or lignin, but the amount and ratios between the components can vary considerably . In addition to the aforementioned components, even the amorphous portions of cellulose are purportedly important for lignocellulosic conversion to biofuel [4–7]. Since secondary cell walls in fibres and tracheary elements constitute the most abundant biomass produced by plants, it is necessary to elucidate the possible molecular mechanisms underlying the regulation of secondary cell wall biosynthesis for improved plant biomass production.
Plant NAC (NAM, ATAF1/2 and CUC2) domain proteins are one of the largest groups of plant-specific transcriptional factors and are known to play diverse roles in various plant development processes and stress response. NAM (no apical meristem) was the first characterized NAC gene in petunia. The NAM gene product is required for apical meristem formation and correct positioning of the cotyledons during petunia embryogenesis . ATAF1 and ATAF2 are the two NAC genes in Arabidopsis playing negative roles in response to drought and pathogen infection respectively [9, 10]. CUC2 (CUP-SHAPED COTYLEDON 2) gene was also characterized as a NAC gene in Arabidopsis . Arabidopsis RD26 (RESPONSIVE TO DEHYDRATION 26) encodes a NAC domain protein  with function in ABA-mediating gene expression under stress conditions . StNAC, one potato NAC gene, was shown to be rapidly and strongly induced by wounding . Over-expression of OsNAC6/SNAC2 in rice can enhance the seedling plants tolerance to drought, salt, and cold stresses [15, 16]. Recently, accumulating evidence has indicated that a considerable portion of NAC domain proteins play crucial roles in the processes of xylogenesis, fibre development and wood formation in vascular plants . In the model plant Arabidopsis, NST1 (NAC Secondary Wall Thickening Promoting Factor1), NST2 and NST3/SND1 (Secondary Wall-associated NAC Domain Protein1) are key switches in regulating secondary cell wall biosynthesis in a partially redundant manner [18–25]. NST1 and NST2 function redundantly in regulating secondary cell wall thickening in the endothecium of anthers whereas NST1 and NST3/SND1 were shown to regulate secondary wall thickening in fibres. In Medicago sativa, MtNST1 (Medicago truncatula NAC Secondary Wall Thickening Promoting Factor 1) has been identified as the only homologue of AtNSTs . Loss of function of the single MtNST1 gene resulted in lack of lignifications in interfascicular fibres, loss of anther dehiscence and stomatal phenotypes associated with loss of ferulic acid in guard cell walls. VND6 (Vascular-related NAC-domain6) and VND7 are key regulators in protoxylem and metaxylem development. VND6 is specifically expressed in the metaxylem of Arabidopsis primary roots whereas VND7 is expressed in the protoxylem. Recently, the VND6 gene was discovered to regulate xylem formation by directly targeting some genes related to secondary cell wall formation. VND6 also acts as a direct regulator of genes related to programmed cell death . SND2 and SND3 were also found to function in the formation of secondary cell walls in fibres, and were down-stream of NST1 and NST3/VND1. Six NAC genes associated with wood formation in Populus were also reported . Among the six genes, WND2B (Wood-Associated NAC Domain Transcription Factors) and WND6B were functional orthologues of Arabidopsis SND1 and master switches activating secondary wall biosynthesis during wood formation in Populus. Recently, XND1(Xylem NAC Domain1) was reported to influence the differentiation of tracheary elements and xylem development in Arabidopsis by negatively regulating terminal secondary wall biosynthesis and programmed cell death in xylem vessel cells .
Although several key switches in regulation of secondary wall formation have been found in the model plants Arabidopsis and Populus, key regulators in other plants and many downstream genes regulated by these transcriptional factors are still not clear. In order to identify key homologue genes and discover the network controlling cell wall biosynthesis, we carried out comparative genome analysis of NST, VND and SND genes across 19 higher plant species. The analysis revealed that the NAC domain transcription factors associated with the secondary cell wall evolutionarily first appeared in Selaginella moellendorffii. In fact, among the three groups, only VND genes were identified in S. moellendorffii, which is evolutionarily earlier than the other two groups. Gene expression analysis was carried out to analyse the regulation of NAC genes associated with secondary cell wall biosynthesis in different tissues and revealed that several of these transcriptional factors were co-regulated. To further characterize the candidate genes involved in the regulation of secondary cell wall biosynthesis, we performed a comprehensive co-regulatory network analysis and discovered that some secondary wall-associated NAC genes and MYB genes were co-regulated. In addition, co-regulatory network analysis also revealed many novel genes and pathways that may be involved in cell wall biosynthesis and regulation.
Sequence retrieval and phylogenetic analysis
Protein sequences and DNA binding domain alignment of the NAC transcriptional factor gene family were downloaded from Plant Transcriptional Factor Database http://planttfdb.cbi.pku.edu.cn. Multiple alignments were performed using ClustalX (1.83) software, and the Neighbour-Joining (NJ) method was used to construct a phylogenetic tree. Genes sharing the same clade with the NAC genes controlling cell wall composition from Arabidopsis were chosen for further study, which resulted in 199 proteins across 19 species.
Microarray data analysis
The expression profiling data was acquired from local and publically available databases (e.g. GEO and AtGenExpress). The signal intensity for each probe set of each GeneChip was extracted by Affymetrix software GCOS (MAS 5.0).
Eisen's cluster software http://rana.lbl.gov/EisenSoftware.htm was applied for cluster analysis. The signal intensities of microarray experiments were directly used for hierarchical clustering analysis. We employed standard data adjustment and SOM (Self-Organizing Map) clustering in precedence of hierarchical clustering to achieve a better grouping result.
Gene ontology (GO) analysis was performed for differentially expressed genes using the EasyGO web server . During GO processing, the statistical test method used was the chi-square test with FDR p-value ≤ 0.05 as the cut-off.
The gene network data was constructed using Pathway Studio http://www.ariadnegenomics.com/products/pathway-studio/, ATTED http://atted.jp/ and Hans J. Bohnert's paper , and the map was constructed using Pathway Studio (version 6.2).
Seven tissue samples of rice (Oryza sativa subsp. japonica var. Nipponbare) were selected for real-time RT-PCR (reverse transcription polymerase chain reaction) analysis. Rice calli were cultured in N6 solid medium  and harvested after one month of induction. Root samples were harvested from rice seedlings that were cultured in a growth container for two weeks. The other five samples (penultimate leaf, flag leaf, spikelet, seed and stem) were harvested from rice plant grown for about four months under natural conditions in Beijing, China.
RNA isolation and real-time RT-PCR
All rice tissue samples were homogenized in liquid nitrogen before isolation of RNA. Total RNA was isolated using TRIZOL reagent (Invitrogen, CA, USA) and purified using Qiagen RNeasy columns (Qiagen, Hilden, Germany). Reverse transcription was performed using Moloney murine leukemia virus (M-MLV; Invitrogen). The cDNA samples were diluted to 8 ng/μL for real-time RT-PCR analysis.
Gene Ontology enrichment analysis for the gene list in SNDs-related network
GO acc num
secondary cell wall biogenesis
plant-type cell wall biogenesis
regulation of transcription
multicellular organismal development
anatomical structure development
cell wall macromolecule metabolic process
cellular polysaccharide biosynthetic process
phenylpropanoid biosynthetic process
response to organic substance
regulation of transcription, DNA-dependent
response to stress
reproductive developmental process
transcription factor activity
transcription activator activity
oxidoreductase activity, acting on diphenols and related substances as donors, oxygen as acceptor
oxidoreductase activity, acting on diphenols and related substances as donors
transition metal ion binding
transferase activity, transferring glycosyl groups
hydrolase activity, hydrolyzing O-glycosyl compounds
electron carrier activity
Results and discussion
Identification of genes of NAC transcriptional factors controlling the cell wall composition across different species
The NAC gene family associated with the secondary cell wall biosynthesis evolutionarily first appeared in S. moellendorffii (Figure 1). Among the three groups, only VND proteins appeared in S. moellendorffii, which was evolutionarily earlier than the other two groups.
Evolutionary relatedness of SND, NST, VND genes in different species
Expression patterns of SND, NST and VND genes in Arabidopsis
Expression patterns of SND, NST and VND orthologue genes in rice
Co-regulatory network analysis for secondary cell wall biosynthesis NAC transcriptional factors SND1, SND2 and SND3
Furthermore, some secondary cell wall metabolism-related genes were co-expressed with SND genes, such as LAC genes (LAC2, LAC5, LAC10, LAC12 and LAC17), IRX (IRREGULAR XYLEM) genes (IRX1, IRX3, IRX6, IRX9, IRX12 and IRX14), CESA4 (CELLULOSE SYNTHASE A4) and pectinase related protein. The knockout mutant of LAC2 had been reported to reduce root elongation under PEG-induced dehydration  and LAC17 mutants appear to have a reduced deposition of G lignin units . IRX1 encodes a member of the cellulose synthase family [42–44], IRX3 encodes a xylem-specific cellulose synthase , IRX6 encodes a member of the COBRA family (similar to phytochelatin synthetase) , IRX9 encodes a putative family 43 glycosyl transferase [47, 48], IRX12 (also known as LAC4) appears to have laccase activity , IRX14 encodes a putative family 43 glycosyl transferase [48, 49], CESA4 encodes a cellulose synthase [46, 50], and all these genes are involved in secondary cell wall biosynthesis.
Interestingly, several RIC (ROP-INTERACTIVE CRIB MOTIF-CONTAINING PROTEIN) genes were also co-regulated with SND genes, e.g. RIC2 (involved in pollen tube growth and function ) and RIC4 (interacts with ROP2 during pavement cell morphogenesis and with ROP1 to promote apical F-actin assembly ). In addition, the co-regulatory network analysis also revealed that many novel genes were co-expressed with SNDs.
There were a total of 134 genes involved in this network (Supplemental Table 2 in additional file 2). GO analysis  was also performed for these 134 SND co-regulated genes (Table 1) to decipher the possible biological pathways in which these genes were involved. Of the 134 genes queried, there were 131 genes with annotated GO items. We used 0.05 as the cut-off of FDR adjusted p-value. The most significantly enriched GO terms were 'secondary cell wall biogenesis process' (GO:0009834, FDR p-value = 2.40E-22), 'cellular polysaccharide biosynthetic process' (GO:0033692, FDR p-value = 4.30E-07), 'phenylpropanoid biosynthetic process' (GO:0009699, FDR p-value = 2.50E-06), 'transcription factor activity' (GO:0003700, FDR p-value = 3.00E-49) and 'laccase activity' (GO:0008471, FDR p-value = 3.00E-09). The GO terms related to other biological processes were also enriched, e.g. 'response to stress' (GO:0006950, FDR p-value = 5.60E-03), 'oxidoreductase activity' (GO:0016491, FDR p-value = 4.00E-04), 'transition metal ion binding' (GO:0046914, FDR p-value = 3.50E-05) and transporter activity. Also, most genes were localized in nuclear and membrane parts.
Co-regulatory network analysis of SNDs and GO enrichment analysis indicated that most co-expressed genes were involved in secondary cell wall biogenesis, while we also found that some oxidoreductase activity and phenylpropanoid biosynthesis pathway genes were co-expressed with SND genes, e.g. peroxidase 64, NADPH oxidase and FLS2. Some processes such as carbohydrate synthesis and transport were coordinately regulated toward cell wall biosynthesis. There may be cross-talk between secondary wall biosynthesis and other biological processes.
Combining the bioinformatics data mining and bench validation approach, we analysed the NST, VND and SND genes across plant species. The comparative genomic analysis revealed that the group VND of the NAC gene family evolutionarily first appeared in S. moellendorffii. The Arabidopsis and rice gene expression analysis showed the specific patterns of these NAC genes and the conservation of SNDs and NSTs in Arabidopsis and rice, and they were preferentially expressed in stems. The gene network analysis of SND genes in Arabidopsis showed that three SND genes (SND1, SND2 and SND3) co-expressed with multiple transcription factor genes, especially MYB genes and KNAT7, which are important in modulating cell wall biosynthesis. Additionally, the co-regulatory network analysis revealed many novel genes and pathways that could potentially be involved in cell wall biosynthesis and regulation. Nevertheless, there may be cross-talk between secondary wall biosynthesis and other biological process, such as stress response.
In summary, these results provided new insight into the evolution and the gene regulatory network of a subgroup of the NAC gene family controlling cell wall composition from the perspective of bioinformatics. These may help us to better understand the possible molecular mechanism underlying the regulation network of secondary cell wall biosynthesis and, therefore, improve plant biomass production.
This work was supported by grants from the Ministry of Science and Technology of China (2012CB215300 and 31171276).
This article has been published as part of BMC Bioinformatics Volume 13 Supplement 15, 2012: Proceedings of the Ninth Annual MCBIOS Conference. Dealing with the Omics Data Deluge. The full contents of the supplement are available online at http://www.biomedcentral.com/bmcbioinformatics/supplements/13/S15
- Yuan JS, Tiller KH, Al-Ahmad H, Stewart NR, Stewart CN Jr: Plants to power: bioenergy to fuel the future. Trends plant sci 2008, 13(8):421–429. 10.1016/j.tplants.2008.06.001View ArticlePubMedGoogle Scholar
- Li H, Cann AF, Liao JC: Biofuels: Biomolecular Engineering Fundamentals and Advances. Annu Rev Chem Biomol Eng 2010, 1: 19–36. 10.1146/annurev-chembioeng-073009-100938View ArticlePubMedGoogle Scholar
- Keegstra MPaK: Plant cell wall polymers as precursors for biofuels. Curr Opin Plant Biol 2010, 13: 305–312.PubMedGoogle Scholar
- Abramson MSO, Shani Z: Plant cell wall reconstruction toward improved lignocellulosic production and processability. Plant Sci 2010, 178: 61–72. 10.1016/j.plantsci.2009.11.003View ArticleGoogle Scholar
- Himmel ME, Ding SY, Johnson DK, Adney WS, Nimlos MR, Brady JW, Foust TD: Biomass recalcitrance: engineering plants and enzymes for biofuels production. Science 2007, 315(5813):804–807. 10.1126/science.1137016View ArticlePubMedGoogle Scholar
- Ragauskas AJ, Williams CK, Davison BH, Britovsek G, Cairney J, Eckert CA, Frederick WJ Jr, Hallett JP, Leak DJ, Liotta CL, et al.: The path forward for biofuels and biomaterials. Science 2006, 311(5760):484–489. 10.1126/science.1114736View ArticlePubMedGoogle Scholar
- Simmons BA, Loque D, Ralph J: Advances in modifying lignin for enhanced biofuel production. Curr Opin Plant Biol 2010, 13(3):313–320.View ArticlePubMedGoogle Scholar
- Souer E, van Houwelingen A, Kloos D, Mol J, Koes R: The no apical meristem gene of Petunia is required for pattern formation in embryos and flowers and is expressed at meristem and primordia boundaries. Cell 1996, 85(2):159–170. 10.1016/S0092-8674(00)81093-4View ArticlePubMedGoogle Scholar
- Delessert C, Kazan K, Wilson IW, Van Der Straeten D, Manners J, Dennis ES, Dolferus R: The transcription factor ATAF2 represses the expression of pathogenesis-related genes in Arabidopsis. Plant J 2005, 43(5):745–757. 10.1111/j.1365-313X.2005.02488.xView ArticlePubMedGoogle Scholar
- Lu PL, Chen NZ, An R, Su Z, Qi BS, Ren F, Chen J, Wang XC: A novel drought-inducible gene, ATAF1, encodes a NAC family protein that negatively regulates the expression of stress-responsive genes in Arabidopsis. Plant mol biol 2007, 63(2):289–305.View ArticlePubMedGoogle Scholar
- Aida M, Ishida T, Fukaki H, Fujisawa H, Tasaka M: Genes involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon mutant. The Plant cell 1997, 9(6):841–857. 10.1105/tpc.9.6.841PubMed CentralView ArticlePubMedGoogle Scholar
- Yamaguchi-Shinozaki K, Koizumi M, Urao S, Shinozaki K: Molecular Cloning and Characterization of 9 cDNAs for Genes That Are Responsive to Desiccation in Arabidopsis thaliana: SequenceAnalysis of One cDNA Clone That Encodes a Putative Transmembrane Channel Protein. Plant Cell Physiol 1992, 33(3):217–224.Google Scholar
- Fujita M, Fujita Y, Maruyama K, Seki M, Hiratsu K, Ohme-Takagi M, Tran LS, Yamaguchi-Shinozaki K, Shinozaki K: A dehydration-induced NAC protein, RD26, is involved in a novel ABA-dependent stress-signaling pathway. Plant J 2004, 39(6):863–876. 10.1111/j.1365-313X.2004.02171.xView ArticlePubMedGoogle Scholar
- Collinge M, Boller T: Differential induction of two potato genes, Stprx2 and StNAC, in response to infection by Phytophthora infestans and to wounding. Plant mol biol 2001, 46(5):521–529. 10.1023/A:1010639225091View ArticlePubMedGoogle Scholar
- Nakashima K, Tran LS, Van Nguyen D, Fujita M, Maruyama K, Todaka D, Ito Y, Hayashi N, Shinozaki K, Yamaguchi-Shinozaki K: Functional analysis of a NAC-type transcription factor OsNAC6 involved in abiotic and biotic stress-responsive gene expression in rice. Plant J 2007, 51(4):617–630. 10.1111/j.1365-313X.2007.03168.xView ArticlePubMedGoogle Scholar
- Hu H, You J, Fang Y, Zhu X, Qi Z, Xiong L: Characterization of transcription factor gene SNAC2 conferring cold and salt tolerance in rice. Plant mol biol 2008, 67(1–2):169–181. 10.1007/s11103-008-9309-5View ArticlePubMedGoogle Scholar
- Hu R, Qi G, Kong Y, Kong D, Gao Q, Zhou G: Comprehensive analysis of NAC domain transcription factor gene family in Populus trichocarpa . BMC plant biol 2010, 10: 145. 10.1186/1471-2229-10-145PubMed CentralView ArticlePubMedGoogle Scholar
- Zhong R, Richardson EA, Ye ZH: Two NAC domain transcription factors, SND1 and NST1, function redundantly in regulation of secondary wall synthesis in fibers of Arabidopsis. Planta 2007, 225(6):1603–1611. 10.1007/s00425-007-0498-yView ArticlePubMedGoogle Scholar
- Mitsuda N, Iwase A, Yamamoto H, Yoshida M, Seki M, Shinozaki K, Ohme-Takagi M: NAC transcription factors, NST1 and NST3, are key regulators of the formation of secondary walls in woody tissues of Arabidopsis. The Plant cell 2007, 19(1):270–280. 10.1105/tpc.106.047043PubMed CentralView ArticlePubMedGoogle Scholar
- Mitsuda N, Ohme-Takagi M: NAC transcription factors NST1 and NST3 regulate pod shattering in a partially redundant manner by promoting secondary wall formation after the establishment of tissue identity. Plant J 2008, 56(5):768–778. 10.1111/j.1365-313X.2008.03633.xView ArticlePubMedGoogle Scholar
- Mitsuda N, Seki M, Shinozaki K, Ohme-Takagi M: The NAC transcription factors NST1 and NST2 of Arabidopsis regulate secondary wall thickenings and are required for anther dehiscence. The Plant cell 2005, 17(11):2993–3006. 10.1105/tpc.105.036004PubMed CentralView ArticlePubMedGoogle Scholar
- Zhong R, Lee C, Zhou J, McCarthy RL, Ye ZH: A battery of transcription factors involved in the regulation of secondary cell wall biosynthesis in Arabidopsis. The Plant cell 2008, 20(10):2763–2782. 10.1105/tpc.108.061325PubMed CentralView ArticlePubMedGoogle Scholar
- Iwase A, Hideno A, Watanabe K, Mitsuda N, Ohme-Takagi M: A chimeric NST repressor has the potential to improve glucose productivity from plant cell walls. J biotechnol 2009, 142(3–4):279–284. 10.1016/j.jbiotec.2009.05.011View ArticlePubMedGoogle Scholar
- McCarthy RL, Zhong R, 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(11):1950–1964. 10.1093/pcp/pcp139View ArticlePubMedGoogle Scholar
- Zhong R, Lee C, Ye ZH: Global Analysis of Direct Targets of Secondary Wall NAC Master Switches in Arabidopsis. Mol plant 2010, 3(6):1087–1103. 10.1093/mp/ssq062View ArticlePubMedGoogle Scholar
- Zhao Q, Gallego-Giraldo L, Wang H, Zeng Y, Ding SY, Chen F, Dixon RA: An NAC transcription factor orchestrates multiple features of cell wall development in Medicago truncatula . Plant J 2010, 63(1):100–114.PubMedGoogle Scholar
- Ohashi-Ito K, Oda Y, Fukuda H: Arabidopsis VASCULAR-RELATED NAC-DOMAIN6 directly regulates the genes that govern programmed cell death and secondary wall formation during xylem differentiation. The Plant cell 2010, 22(10):3461–3473. 10.1105/tpc.110.075036PubMed CentralView ArticlePubMedGoogle Scholar
- Zhong R, Lee C, Ye ZH: Functional characterization of poplar wood-associated NAC domain transcription factors. Plant physiol 2010, 152(2):1044–1055. 10.1104/pp.109.148270PubMed CentralView ArticlePubMedGoogle Scholar
- Zhao C, Avci U, Grant EH, Haigler CH, Beers EP: XND1, a member of the NAC domain family in Arabidopsis thaliana, negatively regulates lignocellulose synthesis and programmed cell death in xylem. Plant J 2008, 53(3):425–436.View ArticlePubMedGoogle Scholar
- Zhou X, Su Z: EasyGO: Gene Ontology-based annotation and functional enrichment analysis tool for agronomical species. BMC genomics 2007, 8: 246. 10.1186/1471-2164-8-246PubMed CentralView ArticlePubMedGoogle Scholar
- Ma S, Gong Q, Bohnert HJ: An Arabidopsis gene network based on the graphical Gaussian model. Genome res 2007, 17(11):1614–1625. 10.1101/gr.6911207PubMed CentralView ArticlePubMedGoogle Scholar
- Raval M, Chattoo BB: Role of media constituents and proline in callus growth, somatic embryogenesis and regeneration of Oryza sativa cv Indica. Ind j exp biol 1993, 31(7):600–603.Google Scholar
- Chang S, Chen W, Yang J: Another formula for calculating the gene change rate in real-time RT-PCR. Mol biol rep 2009, 36(8):2165–2168. 10.1007/s11033-008-9430-1View ArticlePubMedGoogle Scholar
- Pylatuik JD, Fobert PR: Comparison of transcript profiling on Arabidopsis microarray platform technologies. Plant mol biol 2005, 58(5):609–624. 10.1007/s11103-005-6506-3View ArticlePubMedGoogle Scholar
- Wang L, Xie W, Chen Y, Tang W, Yang J, Ye R, Liu L, Lin Y, Xu C, Xiao J, et al.: A dynamic gene expression atlas covering the entire life cycle of rice. Plant J 61(5):752–766.Google Scholar
- Obayashi T, Kinoshita K, Nakai K, Shibaoka M, Hayashi S, Saeki M, Shibata D, Saito K, Ohta H: ATTED-II: a database of co-expressed genes and cis elements for identifying co-regulated gene groups in Arabidopsis. Nucleic acids res 2007, (35 Database issue):D863–869.Google Scholar
- Zhong R, Richardson EA, Ye ZH: The MYB46 transcription factor is a direct target of SND1 and regulates secondary wall biosynthesis in Arabidopsis. The Plant cell 2007, 19(9):2776–2792. 10.1105/tpc.107.053678PubMed CentralView ArticlePubMedGoogle Scholar
- Zhou J, Lee C, Zhong R, Ye ZH: MYB58 and MYB63 are transcriptional activators of the lignin biosynthetic pathway during secondary cell wall formation in Arabidopsis. The Plant cell 2009, 21(1):248–266. 10.1105/tpc.108.063321PubMed CentralView ArticlePubMedGoogle Scholar
- Li E, Bhargava A, Qiang W, Friedmann MC, Forneris N, Savidge RA, Johnson LA, Mansfield SD, Ellis BE, Douglas CJ: The Class II KNOX gene KNAT7 negatively regulates secondary wall formation in Arabidopsis and is functionally conserved in Populus. New phytol 2012, 194(1):102–115. 10.1111/j.1469-8137.2011.04016.xView ArticlePubMedGoogle Scholar
- Cai X, Davis EJ, Ballif J, Liang M, Bushman E, Haroldsen V, Torabinejad J, Wu Y: Mutant identification and characterization of the laccase gene family in Arabidopsis. J exp bot 2006, 57(11):2563–2569. 10.1093/jxb/erl022View ArticlePubMedGoogle Scholar
- Berthet S, Demont-Caulet N, Pollet B, Bidzinski P, Cezard L, Le Bris P, Borrega N, Herve J, Blondet E, Balzergue S, et al.: Disruption of LACCASE4 and 17 results in tissue-specific alterations to lignification of Arabidopsis thaliana stems. The Plant cell 2011, 23(3):1124–1137. 10.1105/tpc.110.082792PubMed CentralView ArticlePubMedGoogle Scholar
- Chen Z, Hong X, Zhang H, Wang Y, Li X, Zhu JK, Gong Z: Disruption of the cellulose synthase gene, AtCesA8/IRX1, enhances drought and osmotic stress tolerance in Arabidopsis. Plant J 2005, 43(2):273–283. 10.1111/j.1365-313X.2005.02452.xView ArticlePubMedGoogle Scholar
- Persson S, Caffall KH, Freshour G, Hilley MT, Bauer S, Poindexter P, Hahn MG, Mohnen D, Somerville C: The Arabidopsis irregular xylem8 mutant is deficient in glucuronoxylan and homogalacturonan, which are essential for secondary cell wall integrity. The Plant cell 2007, 19(1):237–255. 10.1105/tpc.106.047720PubMed CentralView ArticlePubMedGoogle Scholar
- Turner SR, Somerville CR: Collapsed xylem phenotype of Arabidopsis identifies mutants deficient in cellulose deposition in the secondary cell wall. The Plant cell 1997, 9(5):689–701.PubMed CentralView ArticlePubMedGoogle Scholar
- Bosca S, Barton CJ, Taylor NG, Ryden P, Neumetzler L, Pauly M, Roberts K, Seifert GJ: Interactions between MUR10/CesA7-dependent secondary cellulose biosynthesis and primary cell wall structure. Plant physiol 2006, 142(4):1353–1363. 10.1104/pp.106.087700PubMed CentralView ArticlePubMedGoogle Scholar
- Brown DM, Zeef LA, Ellis J, Goodacre R, Turner SR: Identification of novel genes in Arabidopsis involved in secondary cell wall formation using expression profiling and reverse genetics. The Plant cell 2005, 17(8):2281–2295. 10.1105/tpc.105.031542PubMed CentralView ArticlePubMedGoogle Scholar
- Bauer S, Vasu P, Persson S, Mort AJ, Somerville CR: Development and application of a suite of polysaccharide-degrading enzymes for analyzing plant cell walls. Proc Nat Acad Sci USA 2006, 103(30):11417–11422. 10.1073/pnas.0604632103PubMed CentralView ArticlePubMedGoogle Scholar
- Brown DM, Goubet F, Wong VW, Goodacre R, Stephens E, Dupree P, Turner SR: Comparison of five xylan synthesis mutants reveals new insight into the mechanisms of xylan synthesis. Plant J 2007, 52(6):1154–1168. 10.1111/j.1365-313X.2007.03307.xView ArticlePubMedGoogle Scholar
- Lee C, Teng Q, Huang W, Zhong R, Ye ZH: The Arabidopsis family GT43 glycosyltransferases form two functionally nonredundant groups essential for the elongation of glucuronoxylan backbone. Plant physiol 2010, 153(2):526–541. 10.1104/pp.110.155309PubMed CentralView ArticlePubMedGoogle Scholar
- 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 Nat Acad Sci USA 1996, 93(22):12637–12642. 10.1073/pnas.93.22.12637PubMed CentralView ArticlePubMedGoogle Scholar
- Wu G, Gu Y, Li S, Yang Z: A genome-wide analysis of Arabidopsis Rop-interactive CRIB motif-containing proteins that act as Rop GTPase targets. The Plant cell 2001, 13(12):2841–2856.PubMed CentralView ArticlePubMedGoogle Scholar
- Fu Y, Gu Y, Zheng Z, Wasteneys G, Yang Z: Arabidopsis interdigitating cell growth requires two antagonistic pathways with opposing action on cell morphogenesis. Cell 2005, 120(5):687–700. 10.1016/j.cell.2004.12.026View ArticlePubMedGoogle Scholar
This article is published under license to BioMed Central Ltd. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.