Secondary cell wall biosynthesis Zhong, Ruiqin; Cui, Dongtao; Ye, Zheng-Hua
The New phytologist,
March 2019, Letnik:
221, Številka:
4
Journal Article
Recenzirano
Odprti dostop
Secondarywalls are synthesizedin specializedcells, suchas tracheary elements andfibers, and their remarkable strength andrigidityprovide strongmechanical support tothe cells andthe plant body. The ...main components of secondary walls are cellulose, xylan, glucomannan and lignin. Biochemical, molecular and genetic studies have led to the discovery of most of the genes involved in the biosynthesis of secondary wall components. Cellulose is synthesized by cellulose synthase complexes in the plasma membrane and the recent success of in vitro synthesis of cellulose microfibrils by a single recombinant cellulose synthase isoform reconstituted into proteoliposomes opens new doors to further investigate the structure and functions of cellulose synthase complexes. Most genes involved in the glycosyl backbone synthesis, glycosyl substitutions and acetylation of xylan and glucomannan have been genetically characterized and the biochemical properties of some of their encoded enzymes have been investigated. The genes and their encoded enzymes participating in monolignol biosynthesis andmodification have been extensively studied both genetically and biochemically. A full understanding of how secondary wall components are synthesized will ultimately enable us to produce plants with custom-designed secondary wall composition tailored to diverse applications.
Secondary walls are mainly composed of cellulose, hemicelluloses (xylan and glucomannan) and lignin, and are deposited in some specialized cells, such as tracheary elements, fibers and other ...sclerenchymatous cells. Secondary walls provide strength to these cells, which lend mechanical support and protection to the plant body and, in the case of tracheary elements, enable them to function as conduits for transporting water. Formation of secondary walls is a complex process that requires the co-ordinated expression of secondary wall biosynthetic genes, biosynthesis and targeted secretion of secondary wall components, and patterned deposition and assembly of secondary walls. Here, we provide a comprehensive review of genes involved in secondary wall biosynthesis and deposition. Most of the genes involved in the biosynthesis of secondary wall components, including cellulose, xylan, glucomannan and lignin, have been identified and their co-ordinated activation has been shown to be mediated by a transcriptional network encompassing the secondary wall NAC and MYB master switches and their downstream transcription factors. It has been demonstrated that cortical microtubules and microtubule-associated proteins play important roles in the targeted secretion of cellulose synthase complexes, the oriented deposition of cellulose microfibrils and the patterned deposition of secondary walls. Further investigation of many secondary wall-associated genes with unknown functions will provide new insights into the mechanisms controlling the formation of secondary walls that constitute the bulk of plant biomass.
Summary
Secondary cell wall biosynthesis has been shown to be regulated by a suite of transcription factors. Here, we identified a new xylem vessel‐specific NAC domain transcription factor, secondary ...wall‐associated NAC domain protein5 (SND5), in Arabidopsis thaliana and studied its role in regulating secondary wall biosynthesis.
We showed that the expression of SND5 and its close homolog, SND4/ANAC075, was specifically associated with secondary wall‐containing cells and dominant repression of their functions severely reduced secondary wall thickening in these cells. Overexpression of SND4/5 as well as their homologs SND2/3 fused with the activation domain of the viral protein VP16 led to ectopic secondary wall deposition in cells that are normally parenchymatous. SND2/3/4/5 regulated the expression of the same downstream target genes as do the secondary wall NAC master switches (SWNs) by binding to and activating the secondary wall NAC binding elements (SNBEs).
Furthermore, we demonstrated that the poplar (Populus trichocarpa) orthologs of SND2/3/4/5 also activated SNBEs and regulated secondary wall biosynthesis during wood formation.
Together, these findings indicate that SND2/3/4/5 and their poplar orthologs regulate the expression of secondary wall‐associated genes through activating SNBEs and they are positioned at an upper level in the SWN‐mediated transcriptional network.
Mannans are an abundant cell wall polysaccharide in bryophytes, seedless vascular plants and gymnosperms. A previous study has shown that mannan acetylation in Arabidopsis and konjac is mediated by ...mannan O-acetyltransferases belonging to the Domain of Unknown Function (DUF) 231 family. However, little is known about the acetylation patterns of mannans in bryophytes and seedless vascular plants, and the evolutionary origin of mannan O-acetyltransferases in land plants has not yet been studied.
Phylogenetic analysis of the DUF231 family revealed that DUF231 members were present in the charophycean green algae and evolved to form overlapped and divergent phylogenetic groups in different taxa of land plants.
Acetyltransferase activity assays of recombinant proteins demonstrated that a number of group II DUF231 members from moss, Selaginella, pine, spruce, rice and poplar were mannan 2-O- and 3-O-acetyltransferases, whereas the two group I DUF231 members from the alga Klebsormidium nitens were not. Structural analysis of mannans from moss and Selaginella showed they were composed of mannosyl and glucosyl residues and the mannosyl residues were acetylated at O-2 and O-3.
These findings indicate that although the DUF231 genes originated in algae, their recruitment as mannan O-acetyltransferases probably occurred in bryophytes, and the biochemical functions of these O-acetyltransferases are evolutionarily conserved throughout land plants.
One of the most prominent features of xylem conducting cells is the deposition of secondary walls. In Arabidopsis, secondary wall biosynthesis in the xylem conducting cells, vessels, has been shown ...to be regulated by two VASCULAR-RELATED NAC-DOMAIN (VND) genes, VND6 and VND7. In this report, we have investigated the roles of five additional Arabidopsis VND genes, VND1 to VND5, in regulating secondary wall biosynthesis in vessels. The VND1 to VND5 genes were shown to be specifically expressed in vessels but not in interfascicular fibers in stems. The expression of VND4 and VND5 was also seen specifically in vessels in the secondary xylem of the root-hypocotyl region. When overexpressed, VND1 to VND5 were able to activate the expression of secondary wall-associated transcription factors and genes involved in secondary wall biosynthesis and programmed cell death. As a result, many normally parenchymatous cells in leaves and stems acquired thickened secondary walls in the VND1 to VND5 overexpressors. In contrast, dominant repression of VND3 function resulted in reduced secondary wall thickening in vessels and a collapsed vessel phenotype. In addition, VND1 to VND5 were shown to be capable of rescuing the secondary wall defects in the fibers of the snd1 nst1 double mutant when expressed under the SND1 promoter. Furthermore, transactivation analysis revealed that VND1 to VND5 could activate expression of the GUS reporter gene driven by the secondary wall NAC binding element (SNBE). Together, these results demonstrate that VND1 to VND5 possess functions similar to that of the SND1 secondary wall NAC and are transcriptional regulators of secondary wall biosynthesis in vessels.
Celotno besedilo
Dostopno za:
DOBA, IZUM, KILJ, NUK, PILJ, PNG, SAZU, SIK, UILJ, UKNU, UL, UM, UPUK
MYB46 and MYB83 are two functionally redundant Arabidopsis thaliana MYB transcription factors that act as master switches regulating secondary wall biosynthesis. Here, we report the identification of ...the transcriptional responsive elements and global analysis of the direct targets of MYB46 and MYB83. Using the estrogen-inducible direct activation system, we found that a number of previously identified MYB46 downstream transcription factors, including MYB43, MYB52, MYB54, MYB58, MYB63 and KNAT7, are direct targets of MYB46. Promoter deletion coupled with transactivation analysis of the MYB63 promoter led to the identification of a 7 bp sequence that is sufficient to be responsive to MYB46 activation, and therefore this sequence is designated as the secondary wall MYB-responsive element (SMRE). Further single nucleotide mutation together with electrophoretic mobility shift assay mapped the SMRE consensus sequence as ACC(A/T)A(A/C)(T/C). Genome-wide analysis of direct targets of MYB46 demonstrated that it directly regulates the expression of not only a number of downstream transcription factors, but also a suite of secondary wall biosynthetic genes, some of which are also directly activated by secondary wall NAC (SWN) master switches or by MYB46 direct targets. Furthermore, MYB83 was found to bind to the same SMRE consensus sequence and activate the same set of direct targets as MYB46. Our study has revealed that the transcription program regulating secondary wall biosynthesis involves a multileveled feed-forward loop regulatory structure in which MYB46/MYB83 together with their regulators SWNs and their direct targets regulate an array of downstream genes thereby activating the secondary wall biosynthetic program.
•Secondary walls constitute the bulk of plant biomass.•Secondary wall biosynthesis is coordinated by a transcriptional network.•Secondary wall NAC master switches bind to and activate the SNBE ...sites.•Secondary wall MYB master switches bind to and activate the SMRE sites.•The transcriptional network employs a feed-forward loop regulatory structure.
Secondary walls in the form of wood and fibers are the most abundant biomass produced by vascular plants, and are important raw materials for many industrial uses. Understanding how secondary walls are constructed is of significance in basic plant biology and also has far-reaching implications in genetic engineering of plant biomass better suited for various end uses, such as biofuel production. Secondary walls are composed of three major biopolymers, i.e., cellulose, hemicelluloses and lignin, the biosynthesis of which requires the coordinated transcriptional regulation of all their biosynthesis genes. Genomic and molecular studies have identified a number of transcription factors, whose expression is associated with secondary wall biosynthesis. We comprehensively review how these secondary wall-associated transcription factors function together to turn on the secondary wall biosynthetic program, which leads to secondary wall deposition in vascular plants. The transcriptional network regulating secondary wall biosynthesis employs a multi-leveled feed-forward loop regulatory structure, in which the top-level secondary wall NAC (NAM, ATAF1/2 and CUC2) master switches activate the second-level MYB master switches and they together induce the expression of downstream transcription factors and secondary wall biosynthesis genes. Secondary wall NAC master switches and secondary wall MYB master switches bind to and activate the SNBE (secondary wall NAC binding element) and SMRE (secondary wall MYB-responsive element) sites, respectively, in their target gene promoters. Further investigation of what and how developmental signals trigger the transcriptional network to regulate secondary wall biosynthesis and how different secondary wall-associated transcription factors function cooperatively in activating secondary wall biosynthetic pathways will lead to a better understanding of the molecular mechanisms underlying the transcriptional control of secondary wall biosynthesis.
SUMMARY
Plant cell wall polysaccharides, including xylan, mannan, xyloglucan, and pectins, are often acetylated and members of the domain of unknown function 231 (DUF231)/trichome birefringence‐like ...(TBL) family have been shown to be O‐acetyltransferases mediating the acetylation of xylan, mannan, and xyloglucan. However, little is known about the O‐acetyltransferases responsible for pectin acetylation. In this report, we biochemically characterized a suite of Arabidopsis DUF231/TBL proteins for their roles in pectin acetylation. We generated 24 TBL recombinant proteins in mammalian cells and demonstrated that 10 of them were able to transfer acetyl groups from acetyl‐CoA onto the pectins homogalacturonan (HG) or rhamnogalacturonan‐I (RG‐I), and thus were named pectin O‐acetyltransferase 1 to 10 (POAT1 to 10). It was found that POAT2,4,9,10 specifically acetylated HG and POAT5,6 acetylated RG‐I, whereas POAT1,3,7,8 could act on both HG and RG‐I. The acetylation of HG and RG‐I by POATs was further corroborated by hydrolysis with pectin acetylesterases and by nuclear magnetic resonance spectroscopy. In addition, mutations of the conserved GDS and DXXH motifs in POAT3 and POAT8 were shown to lead to a loss of their ability to acetylate HG and RG‐I. Furthermore, simultaneous RNA interference downregulation of POAT1,3,6,7,8 resulted in reduced cell expansion, impaired plant growth, and decreased pectin acetylation. Together, our findings indicate that these POATs are pectin O‐acetyltransferases involved in acetylation of the pectin polysaccharides HG and RG‐I.
Significance Statement
The pectins homogalacturonan (HG) and rhamnogalacturonan‐I (RG‐I) are often acetylated at O‐2 and/or O‐3 of GalA moieties. We have demonstrated that 10 Arabidopsis DUF231/TBL proteins, POAT1 to 10, are pectin O‐acetyltransferases catalyzing the transfer of acetyl groups onto HG or RG‐I, which contributes to our understanding of the biochemical mechanisms controlling the acetylation of pectins.
We report the genome-wide analysis of direct target genes of SND1 and VND7, two Arabidopsis thaliana NAC domain transcription factors that are master regulators of secondary wall biosynthesis in ...fibers and vessels, respectively. Systematic mapping of the SND1 binding sequence using electrophoretic mobility shift assay and transactivation analysis demonstrated that SND1 together with other secondary wall NACs （SWNs）, including VND6, VND7, NST1, and NST2, bind to an imperfect palindromic 19-bp consensus sequence designated as secondary wall NAC binding element （SNBE）, （T/A）NN（C/T） （TICIG）TNNNNNNNA（AIC）GN（AJCIT） （A/T）, in the promoters of their direct targets. Genome-wide analysis of direct targets of SND1 and VND7 revealed that they directly activate the expression of not only downstream transcription factors, but also a number of non-transcription factor genes involved in secondary wall biosynthesis, cell wall modification, and programmed cell death, the promoters of which all contain multiple SNBE sites. SND1 and VND7 directly regulate the expression of a set of common targets but each of them also preferentially induces a distinct set of direct targets, which is likely attributed to their differential activation strength toward SNBE sites. Complementation study showed that the SWNs were able to rescue the secondary wall defect in the sndl nstl mutant, indicating that they are functionally interchangeable. Together, our results provide important insight into the complex transcriptional program and the evolutionary mechanism underlying secondary wall biosynthesis, cell wall modification, and programmed cell death in secondary wall-containing cell types.
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