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First published online November 17, 2006; 10.1105/tpc.106.047399 The Plant Cell 18:3158-3170 (2006) © 2006 American Society of Plant Biologists SND1, a NAC Domain Transcription Factor, Is a Key Regulator of Secondary Wall Synthesis in Fibers of Arabidopsis[W]
a Department of Plant Biology, University of Georgia, Athens, Georgia 30602 1 To whom correspondence should be addressed. E-mail zhye{at}plantbio.uga.edu; fax 706-542-1805.
Secondary walls in fibers and tracheary elements constitute the most abundant biomass produced by plants. Although a number of genes involved in the biosynthesis of secondary wall components have been characterized, little is known about the molecular mechanisms underlying the coordinated expression of these genes. Here, we demonstrate that the Arabidopsis thaliana NAC (for NAM, ATAF1/2, and CUC2) domain transcription factor, SND1 (for secondary wall–associated NAC domain protein), is a key transcriptional switch regulating secondary wall synthesis in fibers. We show that SND1 is expressed specifically in interfascicular fibers and xylary fibers in stems and that dominant repression of SND1 causes a drastic reduction in the secondary wall thickening of fibers. Ectopic overexpression of SND1 results in activation of the expression of secondary wall biosynthetic genes, leading to massive deposition of secondary walls in cells that are normally nonsclerenchymatous. In addition, we have found that SND1 upregulates the expression of several transcription factors that are highly expressed in fibers during secondary wall synthesis. Together, our results reveal that SND1 is a key transcriptional activator involved in secondary wall biosynthesis in fibers.
Secondary walls are the major constituent of wood, which is the most abundant biomass produced by plants. Secondary walls are composed mainly of cellulose, lignin, and hemicelluloses, including heteroxylans and glucomannans. During secondary wall formation, the biosynthesis of these cell wall components is highly coordinated. Three cellulose synthase (CesA) genes have been shown to be required for cellulose synthesis in secondary walls of Arabidopsis thaliana and rice (Oryza sativa) (Tanaka et al., 2003  ; Taylor et al., 2004). Most of the genes involved in the biosynthetic pathway of lignin have been isolated and functionally characterized (Boerjan et al., 2003). Recently, several genes were shown to participate in the biosynthesis of glucomannan and xylan (Dhugga et al., 2004; Liepman et al., 2005; Zhong et al., 2005). In addition, genomic analysis revealed a number of novel glycosyltransferases that might be involved in secondary wall synthesis (Aspeborg et al., 2005; Brown et al., 2005; Persson et al., 2005). Despite these advances in the study of secondary wall biosynthetic genes, little is known about the molecular mechanisms underlying the coordinated expression of these genes during wood formation.
Recent genomic studies in both poplar (Populus species) and Arabidopsis have identified a number of transcription factors that are potentially involved in the differentiation of xylem tracheary elements and fibers. It has been shown that several shoot apical meristem genes are also expressed in vascular cambium (Schrader et al., 2004
Noteworthy among these xylem- or secondary growth–associated transcription factors are a group of NAC (for NAM, ATAF1/2, and CUC2) domain transcription factors. NAC proteins are plant-specific transcription factors characterized by a conserved NAC domain located at the N-terminal region and a divergent C-terminal activation domain (Olson et al., 2005
Recently, two other NAC genes, NST1 (for NAC secondary wall thickening promoting factor1) and NST2, have been shown to be essential for normal anther dehiscence in Arabidopsis (Mitsuda et al., 2005
Because secondary walls largely determine wood quality, and the most abundant secondary wall–containing cells in wood of dicot species are fibers, it is essential to reveal transcriptional regulators regulating secondary wall synthesis in fibers. Although a number of genes encoding NAC and other transcription factors have been shown to be upregulated during xylem differentiation and secondary growth, none of them has been demonstrated to regulate secondary wall synthesis in fibers. Arabidopsis inflorescence stems develop interfascicular fibers with massive secondary wall thickening, which can be used as an excellent model to study the transcriptional control of secondary wall synthesis. A previous study demonstrated that INTERFASCICULAR FIBERLESS1 (IFL), a homeodomain Leu-zipper transcription factor, is essential for the normal differentiation of interfascicular fibers in Arabidopsis (Zhong and Ye, 1999
Developmental Expression of SND1 in Interfascicular Fibers and Xylem Cells Arabidopsis inflorescence stems develop three to four layers of interfascicular fibers between vascular bundles. After cessation of stem elongation, the interfascicular fiber cells undergo massive secondary wall thickening (Ye et al., 2002 ). During this stage, genes encoding secondary wall biosynthetic enzymes are coordinately turned on. To study the transcriptional regulators responsible for the coordinated expression of these genes, we searched for transcription factors that are highly expressed in interfascicular fiber cells. Among a group of NAC genes that are expressed at a much higher level in stems than in other organs (Figure 1A
), we have found that At1g32770 is specifically expressed in stems with no detectable expression in seedlings, leaves, flowers, and roots (Figure 1C). Further expression analysis in laser-microdissected cell types (Figures 1D and 1E) revealed that although At1g32770 was not expressed in pith parenchyma cells, it was highly expressed in developing interfascicular fibers and xylem cells, two cell types that undergo secondary wall thickening. Because of its close association with the development of secondary wall–containing cells, we named At1g32770 SND1 (for secondary wall–associated NAC domain protein). SND1 belongs to a subgroup of NAC transcription factors that includes VND6, VND7, NST1, and NST2 (Figure 1B; see Supplemental Figure 1 online).
The developmental expression pattern of SND1 was examined in transgenic Arabidopsis plants expressing the SND1 gene fused with the ß-glucuronidase (GUS) reporter gene. The SND1 gene used for expression analysis contains a 2.8-kb 5' upstream sequence, the entire exon and intron region, and a 2-kb 3' downstream sequence. Therefore, the observed GUS reporter gene expression should represent the endogenous SND1 gene expression pattern. Analysis of transgenic Arabidopsis plants expressing SND1:GUS revealed GUS staining exclusively in stems but not in other organs. Detailed examination in stems showed that in rapidly elongating internodes, the GUS staining was present only in elongating fiber cells in which no secondary wall was evident (Figure 2A ). No GUS staining was seen in protoxylem. In internodes that are near the cessation of elongation, GUS staining was observed in both interfascicular fibers and developing metaxylem (Figure 2B). In nonelongating internodes, intensive GUS staining was seen in interfascicular fibers and metaxylem cells, both undergoing massive secondary wall thickening (Figure 2C). Close examination of metaxylem revealed that GUS staining was evident in xylary fiber cells but absent in developing vessels (Figure 2E). At the late stage of stem development, although strong GUS staining was evident in developing secondary xylem, GUS staining in interfascicular fibers became much less intense (Figure 2D). These results demonstrate that the expression of the SND1 gene is associated with the process of secondary wall thickening in interfascicular fibers and xylary fibers. The SND1 protein is targeted to the nucleus when expressed in carrot (Daucus carota) cells (Figures 2F to 2I) and able to activate transcription in yeast cells (Figure 2J), indicating that it is a transcription activator.
Dominant Repression of SND1 Causes a Dramatic Reduction in Secondary Wall Thickening of Fiber Cells To investigate the potential role of SND1 in secondary wall thickening, the wall thickness of interfascicular fibers, xylem vessels, and xylary fibers in the stems of T-DNA knockout lines of SND1 (SALK_015495 and SALK_037737) was examined, and no alterations were observed (data not shown). This finding suggests that other NAC genes might compensate for the loss of SND1 expression. A similar scenario was observed for the VND genes that are expressed during vessel development (i.e., knockout of individual VND genes did not cause any phenotypes) (Kubo et al., 2005 ). It has been demonstrated that transcriptional factors fused with the EAR repression domain act as dominant repressors to inhibit the expression of their target genes (Hiratsu et al., 2003, 2004), and dominant repression of several redundant NACs, such as RD26, VND6, VND7, NST1, and NST2, results in loss-of-function phenotypes (Fujita et al., 2004; Kubo et al., 2005; Mitsuda et al., 2005). To overcome the problem of genetic redundancy, we used the same dominant repression strategy to study the SND1 functions. SND1 fused with the EAR repression domain was expressed under the control of a cauliflower mosaic virus (CaMV) 35S promoter in transgenic Arabidopsis plants. Among 64 transgenic plants in the first generation, the inflorescence stems of 15 of them did not stand as straight as wild-type stems (Figure 3B
). RT-PCR analysis confirmed the presence of the SND1 repressor transcripts in these plants (Figure 3A). Cross sections of the basal part of stems revealed that the wall thickness of interfascicular fibers in the SND1 repressors was reduced drastically compared with that of the wild type (Figures 3E to 3H, Table 1
). The wall thickness of xylary fibers was also reduced dramatically, whereas the vessel walls in metaxylem were only slightly affected (Figures 3I to 3L, Table 1). Longitudinal sections of stems showed that the length of fiber cells in the SND1 repressors was not altered compared with that of the wild type (Figures 3C and 3D). These results demonstrate that dominant repression of SND1 causes a specific inhibition in the secondary wall thickening of fiber cells.
Overexpression of SND1 Induces Ectopic Deposition of Secondary Walls in Normally Nonsclerenchymatous Cells The dominant repression study suggests that SND1 might be a transcriptional activator involved in secondary wall biosynthesis in fibers. To test whether overexpression of SND1 induces secondary wall synthesis, we generated transgenic Arabidopsis plants with overexpression of SND1. Among 57 transgenic lines, 28 of them exhibited a prominent visual phenotype that shows small rosette size and stunted growth of leaves with severely upward-curling blades (Figures 4B and 4C ). RT-PCR analysis demonstrated that although the SND1 mRNA was not detected in wild-type seedlings, it was highly accumulated in the seedlings of these transgenic plants (Figure 4A). Examination of the leaf epidermal cells and mesophyll cells of SND1 overexpressors revealed that a large number of these cells had massive deposition of lignified secondary walls (Figure 5 ), which was likely the cause of the stunted growth of leaves. The ectopically deposited secondary walls formed thick bands in the epidermis (Figures 5C, 5D, 5G, and 5H) or a reticulated pattern in mesophyll cells (Figures 5E, 5F, 5I, and 5J), which are different from the helical pattern of vessels in wild-type leaves (Figures 5A and 5B).
The ectopic secondary wall thickening was also observed in the floral organs and stems of SND1 overexpressors. The flowers of SND1 overexpressors were often sterile and had severely shortened sepals, petals, stamens, and carpels (Figure 4E). In these organs, many cells that are parenchymatous in the wild type had lignified secondary wall thickening in SND1 overexpressors (Figures 6B and 6C ; data not shown). In the stems, ectopic lignified secondary wall thickening was evident in many epidermal cells (Figures 6E and 6G) but seldom seen in cortical and pith cells. Similar to those in the epidermal cells of leaves, the ectopic secondary walls in the epidermal cells of stems are deposited as thick bands (Figure 6G). Examination of cotyledons, hypocotyls, and roots of SND1 overexpressors revealed that the ectopic secondary wall thickening was only occasionally observed in the epidermal cells of hypocotyls and cortical cells of roots but was not seen in other cell types of these organs.
The Secondary Wall Thickening of Fibers Is Drastically Inhibited in SND1 Overexpressors Despite the fact that many epidermal cells in the stems of SND1 overexpressors had ectopic secondary wall thickening, it was surprising to find that the inflorescence stems were often pendent after they bore siliques (Figure 4D). Cross sections of stems revealed that interfascicular fiber cells, which normally deposit a massive amount of secondary walls in the wild type, had extremely thin walls in the SND1 overexpressors (Figures 6H and 6I, Table 1). Examination of xylem cells showed that xylary fibers, which also have a thick layer of secondary walls in the wild type, nearly lacked secondary walls, whereas the thickness of vessel walls appeared to be increased slightly in the SND1 overexpressors (Figures 6J and 6K, Table 1). Longitudinal sections showed that the length of fiber cells in the SND1 overexpressors was indistinguishable from that of the wild type (data not shown). It was confirmed that SND1 was indeed overexpressed in the stems of the SND1 overexpressors (Figure 4A). These results demonstrate that although SND1 overexpression induces ectopic secondary wall deposition in cells that are normally parenchymatous, excess SND1 apparently inhibits normal secondary wall thickening in fibers.
SND1 Overexpression Induces the Expression of Secondary Wall Biosynthetic Genes and Several Fiber-Associated Transcriptional Factors
It is known that tracheary elements undergo secondary wall thickening followed by programmed cell death, whereas fibers are believed to produce secondary walls without immediate cell death. Because the ectopically deposited secondary walls in SND1 overexpressors shared similar patterns with those of tracheary elements, we were prompted to investigate whether SND1 overexpression also induces programmed cell death. Three hydrolase genes, XYLEM CYSTEINE PEPTIDASE1 (XCP1), XCP2, and BIFUNCTIONAL NUCLEASE1 (BFN1), have been shown to be associated with programmed cell death during xylem differentiation (Funk et al., 2002 ; Ito and Fukuda, 2002). Quantitative PCR analysis demonstrated that none of these genes was induced by SND1 overexpression (Figure 7A), indicating that SND1 specifically activates the developmental program of secondary wall thickening without induction of programmed cell death. This is consistent with the observation that although the strongly curled leaves of SND1 overexpressors had a large number of cells with massive deposition of secondary walls, they exhibited no chlorosis, indicating that these cells were still alive.
Although SND1 overexpression activates the expression of genes involved in secondary wall synthesis, it seems unlikely that all secondary wall biosynthetic genes are regulated directly by SND1. It has been shown that genes in the lignin biosynthetic pathway are regulated by MYB transcription factors (Tamagnone et al., 1998
Secondary wall deposition is the most prominent hallmark of wood formation. It not only helps vascular plants to build powerful conduits for water transport but also provides strong mechanical force to support the heavy plant body, thus enabling trees to grow up to hundreds of feet tall. Understanding the molecular switches controlling secondary wall deposition in wood is of importance in basic plant biology as well as for potential genetic engineering of wood quality and quantity in tree species. Our finding that SND1 regulates secondary wall synthesis in fibers marks an important step toward the understanding of how secondary wall synthesis is regulated during wood formation.
We have demonstrated that SND1 is a transcriptional activator regulating secondary wall synthesis in fibers based on the following lines of evidence. First, the SND1 gene is specifically expressed in interfascicular fibers and xylary fibers in stems. Second, SND1 is targeted to the nucleus and able to activate transcription. Third, dominant repression of SND1 inhibits secondary wall deposition but not the elongation of fiber cells. Fourth, overexpression of SND1 induces the expression of secondary wall biosynthetic genes, leading to massive ectopic deposition of secondary walls in cells that are normally nonsclerenchymatous. Considering the facts that SND1 is not expressed in vessels and that dominant repression of SND1 causes a dramatic reduction in the secondary wall thickness of fibers but has only a slight effect on the wall thickness of vessels, we suggest that the secondary wall synthesis in vessels of stems is regulated by transcription factors other than SND1. This is consistent with the transcriptional profiling study of genes upregulated during tracheary element differentiation in cultured Arabidopsis cells, in which SND1 is not induced (Kubo et al., 2005
It is interesting that although SND1 overexpression induced many parenchyma cells in leaves and floral organs and epidermal cells in stems to produce secondary walls, ectopic secondary wall deposition was seldom seen in the parenchyma cells of other organs. This finding indicates that parenchyma cells in different organs exhibit differential competence to induction by SND1. The incompetence of some cells to induction by SND1 could be attributable to the lack of another factor that is required for SND1 functions, the presence of an SND1 inhibitor or the rapid degradation of the SND1 protein in these cells. Nevertheless, the finding that SND1 overexpression results in the massive ectopic deposition of secondary walls in many nonsclerenchymatous cells of leaves, stems, and floral organs indicates that the expression of SND1 is sufficient to induce the developmental program for secondary wall synthesis in certain cell types. Overexpression of NST1 or NST2, both of which are required for secondary wall thickening in endothecium of anthers, was also shown to induce the ectopic deposition of secondary walls in certain organs (Mitsuda et al., 2005
It was found that the deposition patterns of the ectopic secondary walls in SND1 overexpressors were different from the uniformly thickened walls of fibers. Instead, they resemble the patterns of tracheary elements. Walls of tracheary elements can have annular, helical, scalariform, reticulate, and pitted patterns. In SND1 overexpressors, the secondary walls in leaf epidermal cells are deposited in thick bands similar to the scalariform pattern, whereas those in leaf mesophyll cells form a reticulated pattern. However, the ectopic secondary wall thickening in the parenchyma cells of carpels tends to have a helical pattern. This indicates that the ectopic secondary walls induced by SND1 overexpression can be deposited in different patterns depending on the cell type; therefore, SND1 may not control the pattern of secondary wall deposition. Because secondary wall deposition is thought to be regulated by cortical microtubules (Baskin, 2001 In conclusion, we have demonstrated that the secondary wall–specific transcription factor, SND1, is essential for normal secondary wall synthesis in fibers and that overexpression of SND1 is able to activate secondary wall biosynthetic pathways, leading to the ectopic deposition of secondary walls. Identification of SND1 as a key switch for the developmental program of secondary wall thickening in fibers opens a new avenue to dissect the transcriptional networks coordinating the complex process of wood formation. Our finding that SND1 induces the expression of secondary wall–associated transcription factors suggests that SND1 is a key regulator in coordinating the expression of other transcription factors, which in turn might activate different sets of genes involved in secondary wall biosynthesis. A GenBank BLAST search revealed that SND1 homologs are present in several other plants species, including cotton (Gossypium hirsutum), poplar, and spruce (Picea abies) (data not shown), indicating that the regulation of secondary wall synthesis by SND1-like genes might be a common mechanism in plants. Because the most abundant secondary wall–containing cells in wood of dicot species are fibers, and wood is the most important raw material for traditional forest products and potentially for biofuel production, the identification of SND1 as a transcriptional switch for secondary wall formation in fibers has significant biotechnological implications.
Gene Expression Analysis The expression data of Arabidopsis thaliana NAC genes in different organs are derived from the AtGenExpress project (Schmid et al., 2005 ; http://www.weigelworld.org/resources/microarray/AtGenExpress/).
For RT-PCR analysis, total RNA was isolated using a Qiagen RNA isolation kit. The seedlings used were 2 weeks old. Mature leaves were from 6-week-old plants. Inflorescence apices and mature roots were from 8-week-old plants. Stems 1 and 2 were from 4- and 8-week-old plants, respectively. The purified RNA was treated with DNase I to remove any potential genomic DNA contamination before use for first-strand cDNA synthesis. The first-strand cDNA was used as a template for PCR amplification of the SND1 transcripts. PCR was performed for variable cycles to determine the logarithmic phase of amplifications for the samples. RT-PCR was repeated three times, and identical results were obtained. The expression level of the EF1
The interfascicular fiber cells, xylem cells, and pith cells of Arabidopsis stems were captured using the PALM microlaser system (PALM Microlaser Technologies) as described (Nakazono et al., 2003
The developmental expression pattern of the SND1 gene was studied using the GUS reporter gene. A 6-kb genomic DNA fragment containing a 2.8-kb 5' upstream sequence, the entire SND1 exon and intron region, and a 2-kb 3' downstream sequence was used. The GUS reporter gene was inserted in-frame just before the stop codon of the SND1 gene and then cloned into the binary vector pBI101 (Clontech) to create the SND1:GUS construct. The construct was transformed into Arabidopsis plants by the Agrobacterium tumefaciens–mediated transformation procedure (Bechtold and Bouchez, 1994
For quantitative PCR analysis, total RNA isolated from 2-week-old seedlings of wild-type plants and SND1 overexpressors was treated with DNase I and used for first-strand cDNA synthesis. The first-strand cDNA was used as a template for real-time quantitative PCR analysis with the QuantiTect SYBR Green PCR kit (Qiagen). PCR was performed in the Smart Cycler (Cepheid). Relative mRNA levels were determined by normalizing the PCR threshold cycle number of each gene with that of the EF1
Phylogenetic Analysis
Dominant Repression of SND1
Overexpression of SND1
Protein Targeting and Transcriptional Activation Analysis For transcriptional activation analysis, the full-length or partial sequence of SND1 cDNA was fused in-frame with the GAL4 DNA binding domain in the pAS2-1 vector (Clontech). The constructs were transformed into yeast strain CG-1945 containing the His3 and LacZ reporter genes. The transformed yeast cells were grown on SD plates with or without His and subjected for ß-galactosidase assay.
Microscopy
Examination of Secondary Walls
For detection of cellulose in the ectopically deposited secondary walls, one-micrometer-thick sections of leaves and stems were stained with 0.01% Calcoflour White and observed with a UV fluorescence microscope as described (Hughes and McCully, 1975
For detection of xylan in the ectopically deposited secondary walls, 1-µm-thick sections of leaves and stems were incubated with the LM10 monoclonal antibody (McCartney et al., 2005
Accession Numbers
Supplemental Data
We thank E.A. Richardson and G. Zhou for their help with microscopy, J.H. Leebens-Mack for his help with phylogenetic analysis, and the editors and reviewers for their constructive comments and suggestions. This work was supported by grants from the U.S. Department of Energy, Bioscience Division (Z.-H.Y.) and the Japan Society for the Promotion of Science (T.D.).
The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantcell.org) is: Zheng-Hua Ye (zhye{at}plantbio.uga.edu).
[W] Online version contains Web-only data. www.plantcell.org/cgi/doi/10.1105/tpc.106.047399 Received September 15, 2006; Revision received October 15, 2006. accepted November 1, 2006.
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ABSTRACT
INTRODUCTION
105 NAC genes have been identified, and some of them have been shown to play diverse roles in plant growth and development and plant defense (Ooka et al., 2003
gene was used as an internal control.
