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
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