scholarly journals Cellulose synthase complexes display distinct dynamic behaviors during xylem transdifferentiation

2018 ◽  
Vol 115 (27) ◽  
pp. E6366-E6374 ◽  
Author(s):  
Yoichiro Watanabe ◽  
Rene Schneider ◽  
Sarah Barkwill ◽  
Eliana Gonzales-Vigil ◽  
Joseph L. Hill ◽  
...  

In plants, plasma membrane-embedded CELLULOSE SYNTHASE (CESA) enzyme complexes deposit cellulose polymers into the developing cell wall. Cellulose synthesis requires two different sets of CESA complexes that are active during cell expansion and secondary cell wall thickening, respectively. Hence, developing xylem cells, which first undergo cell expansion and subsequently deposit thick secondary walls, need to completely reorganize their CESA complexes from primary wall- to secondary wall-specific CESAs. Using live-cell imaging, we analyzed the principles underlying this remodeling. At the onset of secondary wall synthesis, the primary wall CESAs ceased to be delivered to the plasma membrane and were gradually removed from both the plasma membrane and the Golgi. For a brief transition period, both primary wall- and secondary wall-specific CESAs coexisted in banded domains of the plasma membrane where secondary wall synthesis is concentrated. During this transition, primary and secondary wall CESAs displayed discrete dynamic behaviors and sensitivities to the inhibitor isoxaben. As secondary wall-specific CESAs were delivered and inserted into the plasma membrane, the primary wall CESAs became concentrated in prevacuolar compartments and lytic vacuoles. This adjustment in localization between the two CESAs was accompanied by concurrent decreased primary wall CESA and increased secondary wall CESA protein abundance. Our data reveal distinct and dynamic subcellular trafficking patterns that underpin the remodeling of the cellulose biosynthetic machinery, resulting in the removal and degradation of the primary wall CESA complex with concurrent production and recycling of the secondary wall CESAs.

1973 ◽  
Vol 51 (5) ◽  
pp. 1071-1073 ◽  
Author(s):  
J. A. Brushaber ◽  
R. H. Haskins

Two structurally distinct types of secondary wall layers are present in older hyphae in addition to the primary wall. A coarsely fibrous outer wall layer often becomes quite massive and frequently fuses with the outer wall layers of adjacent cells in the formation of hyphal strands. The uneven deposition of this outer layer often produces large verrucosities. The inner secondary wall layer is relatively electron transparent and contains a reticulum of electron-dense lines. The interface of the inner secondary wall with the cytoplasm is often very irregular, and sections of the plasma membrane are frequently overlain by wall material. The outer secondary wall of conidia is composed of an electron-dense material different from that of the outer wall of hyphae. Cells in the multicellular conidia tend to be polyhedral in shape with either very thick primary walls or thin primary walls having a thick inner wall deposit.


2020 ◽  
Author(s):  
Heather E. McFarlane ◽  
Daniela Mutwil-Anderwald ◽  
Jana Verbančič ◽  
Kelsey L. Picard ◽  
Timothy E. Gookin ◽  
...  

AbstractCellulose synthesis is essential for plant morphology, water transport and defense, and provides raw material for biomaterials and fuels. Cellulose is produced at the plasma membrane by Cellulose Synthase (CESA) protein complexes (CSCs). CSCs are assembled in the endomembrane system and then trafficked from the Golgi apparatus and trans-Golgi Network (TGN) to the plasma membrane. Since CESA enzymes are only active in the plasma membrane, control of CSC secretion is a critical step in the regulation of cellulose synthesis. However, the regulatory framework for CSC secretion is not clarified. In this study, we identify members of a family of seven transmembrane domain-containing proteins (7TMs) as important for cellulose production during cell wall integrity stress. 7TM proteins are often associated with guanine nucleotide-binding protein (G) protein signalling and mutants in several of the canonical G protein complex components phenocopied the 7tm mutant plants. Unexpectedly, the 7TM proteins localized to the Golgi apparatus/TGN where they interacted with the G protein complex. Here, the 7TMs and G proteins regulated CESA trafficking, but did not affect general protein secretion. Furthermore, during cell wall stress, 7TMs’ localization was biased towards small CESA-containing vesicles, specifically associated with CSC trafficking. Our results thus outline how a G protein-coupled module regulates CESA trafficking and reveal that defects in this process lead to exacerbated responses upon exposure to cell wall integrity stress.


2019 ◽  
Author(s):  
Sunita Kushwah ◽  
Alicja Banasiak ◽  
Nobuyuki Nishikubo ◽  
Marta Derba-Maceluch ◽  
Mateusz Majda ◽  
...  

ABSTRACTIn dicotyledons, xyloglucan is the major hemicellulose of primary walls affecting the load-bearing framework with participation of XTH enzymes. We used loss- and gain-of function approaches to study functions of abundant cambial region expressed XTH4 and XTH9 in secondary growth. In secondarily thickened hypocotyls, these enzymes had positive effects on vessel element expansion and fiber intrusive growth. In addition, they stimulated secondary wall thickening, but reduced secondary xylem production. Cell wall analyses of inflorescence stems revealed changes in lignin, cellulose, and matrix sugar composition, indicating overall increase in secondary versus primary walls in the mutants, indicative of higher xylem production compared to wild type (since secondary walls were thinner). Intriguingly, the number of secondary cell wall layers was increased in xth9 and reduced in xth4, whereas the double mutant xth4x9 displayed intermediate number of layers. These changes correlated with certain Raman signals from the walls, indicating changes in lignin and cellulose. Secondary walls were affected also in the interfascicular fibers where neither XTH4 nor XTH9 were expressed, indicating that these effects were indirect. Transcripts involved in secondary wall biosynthesis and in cell wall integrity sensing, including THE1 and WAK2, were highly induced in the mutants, indicating that deficiency in XTH4 and XTH9 triggers cell wall integrity signaling, which, we propose, stimulates the xylem cell production and modulates secondary wall thickening. Prominent effects of XTH4 and XTH9 on secondary xylem support the hypothesis that altered xyloglucan can affect wood properties both directly and via cell wall integrity sensing.SIGNIFICANCE STATEMENTXyloglucan is a ubiquitous component of primary cell walls in all land plants but has not been so far reported in secondary walls. It is metabolized in muro by cell wall-residing enzymes - xyloglucan endotransglycosylases/hydrolases (XTHs), which are reportedly abundant in vascular tissues, but their role in these tissues is unclear. Here we report that two vascular expressed enzymes in Arabidopsis, XTH4 and XTH9 contribute to the secondary xylem cell radial expansion and intrusive elongation in secondary vascular tissues.Unexpectedly, deficiency in their activities highly affect chemistry and ultrastructure of secondary cell walls by non-cell autonomous mechanisms, including transcriptional induction of secondary wall-related biosynthetic genes and cell wall integrity sensors. These results link xyloglucan metabolism with cell wall integrity pathways, shedding new light on previous reports about prominent effects of xyloglucan metabolism on secondary walls.One sentence summaryXTH4 and XTH9 positively regulate xylem cell expansion and fiber intrusive tip growth, and their deficiency alters secondary wall formation via cell wall integrity sensing mechanisms.


2021 ◽  
Vol 28 (1) ◽  
Author(s):  
Veronica Giourieva ◽  
Emmanuel Panteris

Abstract Background Cortical microtubules regulate cell expansion by determining cellulose microfibril orientation in the root apex of Arabidopsis thaliana. While the regulation of cell wall properties by cortical microtubules is well studied, the data on the influence of cell wall to cortical microtubule organization and stability remain scarce. Studies on cellulose biosynthesis mutants revealed that cortical microtubules depend on Cellulose Synthase A (CESA) function and/or cell expansion. Furthermore, it has been reported that cortical microtubules in cellulose-deficient mutants are hypersensitive to oryzalin. In this work, the persistence of cortical microtubules against anti-microtubule treatment was thoroughly studied in the roots of several cesa mutants, namely thanatos, mre1, any1, prc1-1 and rsw1, and the Cellulose Synthase Interacting 1 protein (csi1) mutant pom2-4. In addition, various treatments with drugs affecting cell expansion were performed on wild-type roots. Whole mount tubulin immunolabeling was applied in the above roots and observations were performed by confocal microscopy. Results Cortical microtubules in all mutants showed statistically significant increased persistence against anti-microtubule drugs, compared to those of the wild-type. Furthermore, to examine if the enhanced stability of cortical microtubules was due to reduced cellulose biosynthesis or to suppression of cell expansion, treatments of wild-type roots with 2,6-dichlorobenzonitrile (DCB) and Congo red were performed. After these treatments, cortical microtubules appeared more resistant to oryzalin, than in the control. Conclusions According to these findings, it may be concluded that inhibition of cell expansion, irrespective of the cause, results in increased microtubule stability in A. thaliana root. In addition, cell expansion does not only rely on cortical microtubule orientation but also plays a regulatory role in microtubule dynamics, as well. Various hypotheses may explain the increased cortical microtubule stability under decreased cell expansion such as the role of cell wall sensors and the presence of less dynamic cortical microtubules.


1965 ◽  
Vol 43 (11) ◽  
pp. 1401-1407 ◽  
Author(s):  
James Cronshaw

Cambial derivatives of Acer rubrum have been examined at stages of their differentiation following fixation in 3% or 6% glutaraldehyde with a post fixation in osmium tetroxide. At early stages of development numerous free ribosomes are present in the cytoplasm, and elements of the endoplasmic reticulum tend to align themselves parallel to the cell surfaces. The plasma membrane is closely applied to the cell walls. During differentiation a complex system of cytoplasmic microtubules develops in the peripheral cytoplasm. These microtubules are oriented, mirroring the orientation of the most recently deposited microfibrils of the cell wall. The microtubules form a steep helix in the peripheral cytoplasm at the time of deposition of the middle layer of the secondary wall. During differentiation the free ribosomes disappear from the cytoplasm and numerous elements of rough endoplasmic reticulum with associated polyribosomes become more evident. In many cases the endoplasmic reticulum is associated with the cell surface. During the later stages of differentiation there are numerous inclusions between the cell wall and the plasma membrane.


1952 ◽  
Vol 5 (4) ◽  
pp. 385 ◽  
Author(s):  
ABW Ardrop ◽  
HE Dadswell

Cell division, the nature of extra-cambial readjustment, and the development of the secondary wall in the tracheids of conifer stems have been investigated in both compression wood and normal wood. It has been shown that the reduction in tracheid length, accompanying the development of compression wood and, in normal wood, increased radial growth after suppression, result from an increase in the number of anticlinal divisions in the cambium. From observations of bifurcated and otherwise distorted cell tips in mature tracheids, of small but distinct terminal canals connecting the lumen to the primary wall in the tips of mature tracheids, and of the presence of only primary wall at the tips of partly differentiated tracheids, and from the failure to observe remnants of the parent primary walls at the ends of differentiating tracheids, it has been concluded that extra-cambial readjustment of developing cells proceeds by tip or intrusive growth. It has been further concluded that the development of the secondary wall is progressive towards the cell tips, on the bases of direct observation of secondary wall formation in developing tracheids and of the increase found in the number of turns of the micellar helix per cell with increasing cell length. The significance of this in relation to the submicroscopic organization of the cell wall has been discussed. Results of X-ray examinations and of measurements of� tracheid length in successive narrow tangential zones from the cambium into the xylem have indicated that secondary wall formation begins before the dimensional changes of differentiation are complete.


2019 ◽  
Author(s):  
Christopher Kesten ◽  
Francisco M. Gámez-Arjona ◽  
Stefan Scholl ◽  
Alexandra Menna ◽  
Susanne Dora ◽  
...  

AbstractEnvironmental adaptation of organisms relies on fast perception and response to external signals, which lead to developmental changes. Plant cell growth is strongly dependent on cell wall remodeling. However, little is known about cell wall-related sensing of biotic stimuli and the downstream mechanisms that coordinate growth and defense responses. We generated genetically encoded pH sensors to determine absolute pH changes across the plasma membrane in response to biotic stress. A rapid apoplastic acidification by phosphorylation-based proton pump activation was followed by an acidification of the cortical side of the plasma membrane in response to the fungus Fusarium oxysporum. The proton chemical gradient modulation immediately reduced cellulose synthesis and cell growth and, furthermore, had a direct influence on the pathogenicity of the fungus. All these effects were dependent on the COMPANION OF CELLULOSE SYNTHASE proteins that are thus at the nexus of plant growth and defense. Hence, our discoveries show a remarkable connection between plant biomass production, immunity, and pH control, and advance our ability to investigate the plant growth-defense balance.


2020 ◽  
Author(s):  
Song Chen ◽  
Xin Lin ◽  
Xiyang Zhao ◽  
Su Chen

Abstract BackgroundCellulose is an essential structural component of plant cell wall and is an important resource to produce paper, textiles, bioplastics and other biomaterials. The synthesis of cellulose is among the most important but poorly understood biochemical processes, which is precisely regulated by internal and external cues.ResultsHere, we identified 46 gene models in 7 gene families which encoding cellulose synthase and related enzymes of Betula pendula, and the transcript abundance of these genes in xylem, root, leaf and flower tissues also be determined. Based on these RNA-seq data, we have identified 8 genes that most likely participate in secondary cell wall synthesis, which include 3 cellulose synthase genes and 5 cellulose synthase-like genes. In parallel, a gene co-expression network was also constructed based on transcriptome sequencing.ConclusionsIn this study, we have identified a total of 46 cell wall synthesis genes in B. pendula, which include 8 secondary cell wall synthesis genes. These analyses will help decipher the genetic information of the cell wall synthesis genes, elucidate the molecular mechanism of cellulose synthesis and understand the cell wall structure in B. pendula.


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