In plants, changes in cell size and shape during development fundamentally depend on the ability to synthesize and modify cell wall polysaccharides. The main classes of cell wall polysaccharides produced by terrestrial plants are cellulose, hemicelluloses, and pectins. Members of the cellulose synthase (CESA) and cellulose synthase-like (CSL) families encode glycosyltransferases that synthesize the β-1,4-linked glycan backbones of cellulose and most hemicellulosic polysaccharides that comprise plant cell walls. Cellulose microfibrils are the major load-bearing component in plant cell walls and are assembled from individual β-1,4-glucan polymers synthesized by CESA proteins that are organized into multimeric complexes called CESA complexes, in the plant plasma membrane. During distinct modes of polarized cell wall deposition, such as in the tip growth that occurs during the formation of root hairs and pollen tubes or de novo formation of cell plates during plant cytokinesis, newly synthesized cell wall polysaccharides are deposited in a restricted region of the cell. These processes require the activity of members of the CESA-like D subfamily. However, while these CSLD polysaccharide synthases are essential, the nature of the polysaccharides they synthesize has remained elusive. Here, we use a combination of genetic rescue experiments with CSLD-CESA chimeric proteins, in vitro biochemical reconstitution, and supporting computational modeling and simulation, to demonstrate that Arabidopsis (Arabidopsis thaliana) CSLD3 is a UDP-glucose-dependent β-1,4-glucan synthase that forms protein complexes displaying similar ultrastructural features to those formed by CESA6.
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Associations between phytohormones and cellulose biosynthesis in land plants
Abstract Background Phytohormones are small molecules that regulate virtually every aspect of plant growth and development, from basic cellular processes, such as cell expansion and division, to whole plant environmental responses. While the phytohormone levels and distribution thus tell the plant how to adjust itself, the corresponding growth alterations are actuated by cell wall modification/synthesis and internal turgor. Plant cell walls are complex polysaccharide-rich extracellular matrixes that surround all plant cells. Among the cell wall components, cellulose is typically the major polysaccharide, and is the load-bearing structure of the walls. Hence, the cell wall distribution of cellulose, which is synthesized by large Cellulose Synthase protein complexes at the cell surface, directs plant growth. Scope Here, we review the relationships between key phytohormone classes and cellulose deposition in plant systems. We present the core signalling pathways associated with each phytohormone and discuss the current understanding of how these signalling pathways impact cellulose biosynthesis with a particular focus on transcriptional and post-translational regulation. Because cortical microtubules underlying the plasma membrane significantly impact the trajectories of Cellulose Synthase Complexes, we also discuss the current understanding of how phytohormone signalling impacts the cortical microtubule array. Conclusion Given the importance of cellulose deposition and phytohormone signalling in plant growth and development, one would expect that there is substantial cross-talk between these processes; however, mechanisms for many of these relationships remain unclear and should be considered as the target of future studies.
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- Award ID(s):
- 1750359
- NSF-PAR ID:
- 10212322
- Date Published:
- Journal Name:
- Annals of Botany
- Volume:
- 126
- Issue:
- 5
- ISSN:
- 0305-7364
- Page Range / eLocation ID:
- 807 to 824
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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SUMMARY Plant cell walls are essential for defining plant growth and development, providing structural support to the main body and responding to abiotic and biotic cues. Cellulose, the main structural polymer of plant cell walls, is synthesized at the plasma membrane by cellulose synthase complexes (CSCs). The construction and transport of CSCs to and from the plasma membrane is poorly understood but is known to rely on the coordinated activity of cellulose synthase‐interactive protein 1 (CSI1), a key regulator of CSC trafficking. In this study, we found that Trs85, a TRAPPIII complex subunit, interacted with CSI1
in vitro . Using functional genetics and live‐cell imaging, we have shown thattrs85‐1 mutants have reduced cellulose content, stimulated CSC delivery, an increased population of static CSCs and deficient clathrin‐mediated endocytosis in the primary cell wall. Overall, our findings suggest that Trs85 has a dual role in the trafficking of CSCs, by negatively regulating the exocytosis and clathrin‐mediated endocytosis of CSCs. -
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SUMMARY Plant cells and organs grow into a remarkable diversity of shapes, as directed by cell walls composed primarily of polysaccharides such as cellulose and multiple structurally distinct pectins. The properties of the cell wall that allow for precise control of morphogenesis are distinct from those of the individual polysaccharide components. For example, cellulose, the primary determinant of cell morphology, is a chiral macromolecule that can self‐assemble
in vitro into larger‐scale structures of consistent chirality, and yet most plant cells do not display consistent chirality in their growth. One interesting exception is theArabidopsis thaliana rhm1 mutant, which has decreased levels of the pectin rhamnogalacturonan‐I and causes conical petal epidermal cells to grow with a left‐handed helical twist. Here, we show that inrhm1 the cellulose is bundled into large macrofibrils, unlike the evenly distributed microfibrils of the wild type. This cellulose bundling becomes increasingly severe over time, consistent with cellulose being synthesized normally and then self‐associating into macrofibrils. We also show that in the wild type, cellulose is oriented transversely, whereas inrhm1 mutants, the cellulose forms right‐handed helices that can account for the helical morphology of the petal cells. Our results indicate that when the composition of pectin is altered, cellulose can form cellular‐scale chiral structuresin vivo , analogous to the helicoids formedin vitro by cellulose nano‐crystals. We propose that an important emergent property of the interplay between rhamnogalacturonan‐I and cellulose is to permit the assembly of nonbundled cellulose structures, providing plants flexibility to orient cellulose and direct morphogenesis. -
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Summary Boron is a micronutrient that is required for the normal growth and development of vascular plants, but its precise functions remain a subject of debate. One established role for boron is in the cell wall where it forms a diester cross‐link between two monomers of the low‐abundance pectic polysaccharide rhamnogalacturonan‐
II (RG ‐II ). The inability ofRG ‐II to properly assemble into a dimer results in the formation of cell walls with abnormal biochemical and biomechanical properties and has a severe impact on plant productivity. Here we describe the effects onRG ‐II structure and cross‐linking and on the growth of plants in which the expression of aGDP ‐sugar transporter (GONST 3/GGLT 1) has been reduced. In theGGLT 1RG ‐II is reduced by up to 50%. This leads to a reduction in the extent ofRG ‐II cross‐linking in the cell walls as well as a reduction in the stability of the dimer in the presence of calcium chelators. The silenced plants have a dwarf phenotype, which is rescued by growth in the presence of increased amounts of boric acid. Similar to themur1 mutant, which also disruptsRG ‐II cross‐linking,GGLT 1GGLT 1 is probably the primary GolgiGDP ‐L‐galactose transporter, and providesGDP ‐L‐galactose forRG ‐II biosynthesis. We propose that the L‐galactose residue is critical forRG ‐II dimerization and for the stability of the borate cross‐link. -
Abstract The common ancestor of seed plants and mosses contained homo-oligomeric cellulose synthesis complexes (CSCs) composed of identical subunits encoded by a single CELLULOSE SYNTHASE (CESA) gene. Seed plants use different CESA isoforms for primary and secondary cell wall deposition. Both primary and secondary CESAs form hetero-oligomeric CSCs that assemble and function in planta only when all the required isoforms are present. The moss Physcomitrium (Physcomitrella) patens has seven CESA genes that can be grouped into two functionally and phylogenetically distinct classes. Previously, we showed that PpCESA3 and/or PpCESA8 (class A) together with PpCESA6 and/or PpCESA7 (class B) form obligate hetero-oligomeric complexes required for normal secondary cell wall deposition. Here, we show that gametophore morphogenesis requires a member of class A, PpCESA5, and is sustained in the absence of other PpCESA isoforms. PpCESA5 also differs from the other class A PpCESAs as it is able to self-interact and does not co-immunoprecipitate with other PpCESA isoforms. These results are consistent with the hypothesis that homo-oligomeric CSCs containing only PpCESA5 subunits synthesize cellulose required for gametophore morphogenesis. Analysis of mutant phenotypes also revealed that, like secondary cell wall deposition, normal protonemal tip growth requires class B isoforms (PpCESA4 or PpCESA10), along with a class A partner (PpCESA3, PpCESA5, or PpCESA8). Thus, P. patens contains both homo-oligomeric and hetero-oligomeric CSCs.more » « less
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1093/aob/mcaa121
