scholarly journals Arabidopsis XTH4 and XTH9 contribute to wood cell expansion and secondary wall formation

2019 ◽  
Author(s):  
Sunita Kushwah ◽  
Alicja Banasiak ◽  
Nobuyuki Nishikubo ◽  
Marta Derba-Maceluch ◽  
Mateusz Majda ◽  
...  
Keyword(s):  
Cell Wall ◽  
Cell Expansion ◽  
Cell Walls ◽  
Secondary Wall ◽  
Secondary Xylem ◽  
Cell Wall Integrity ◽  
Wall Thickening ◽  
Xylem Cell ◽  
Secondary Wall Thickening ◽  
Secondary Wall Formation

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.

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 ◽  
...  
Keyword(s):  
Cell Wall ◽  
Plasma Membrane ◽  
Cell Expansion ◽  
Secondary Wall ◽  
Transition Period ◽  
Cellulose Synthase ◽  
Wall Thickening ◽  
Cellulose Synthesis ◽  
Primary Wall ◽  
Dynamic Behaviors

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.

scholarly journals THE FINE STRUCTURE OF DIFFERENTIATING XYLEM ELEMENTS

1965 ◽  
Vol 24 (3) ◽  
pp. 415-431 ◽  
Author(s):  
James Cronshaw ◽  
G. Benjamin Bouck
Keyword(s):  
Endoplasmic Reticulum ◽  
Cell Wall ◽  
Fine Structure ◽  
Secondary Wall ◽  
Osmium Tetroxide ◽  
Light And Electron Microscopy ◽  
Wall Thickening ◽  
Direction Parallel ◽  
Secondary Wall Thickening ◽  
Xylem Elements

Differentiating xylem elements of Avena coleoptiles have been examined by light and electron microscopy. Fixation in 2 per cent phosphate-buffered osmium tetroxide and in 6 per cent glutaraldehyde, followed by 2 per cent osmium tetroxide, revealed details of the cell wall and cytoplasmic fine structure. The localized secondary wall thickening identified the xylem elements and indicated their state of differentiation. These differentiating xylem elements have dense cytoplasmic contents in which the dictyosomes and elements of rough endoplasmic reticulum are especially numerous. Vesicles are associated with the dictyosomes and are found throughout the cytoplasm. In many cases, these vesicles have electron-opaque contents. "Microtubules" are abundant in the peripheral cytoplasm and are always associated with the secondary wall thickenings. These microtubules are oriented in a direction parallel to the microfibrillar direction of the thickenings. Other tubules are frequently found between the cell wall and the plasma membrane. Our results support the view that the morphological association of the "microtubules" with developing cell wall thickenings may have a functional significance, especially with respect to the orientation of the microfibrils. Dictyosomes and endoplasmic reticulum may have a function in some way connected with the synthetic mechanism of cell wall deposition.

scholarly journals Histone methyltransferase ATX1 dynamically regulates fiber secondary cell wall biosynthesis in Arabidopsis inflorescence stem

2020 ◽  
Author(s):  
Xianqiang Wang ◽  
Denghui Wang ◽  
Wenjian Xu ◽  
Lingfei Kong ◽  
Xiao Ye ◽  
...  
Keyword(s):  
Cell Wall ◽  
Secondary Wall ◽  
Histone Methyltransferase ◽  
Epigenetic Mechanism ◽  
Wall Thickening ◽  
Loss Of Function ◽  
Inflorescence Stem ◽  
Secondary Wall Thickening ◽  
Cell Wall Development ◽  
Stem Development

Abstract Secondary wall thickening in the sclerenchyma cells is strictly controlled by a complex network of transcription factors in vascular plants. However, little is known about the epigenetic mechanism regulating secondary wall biosynthesis. In this study, we identified that ARABIDOPSIS HOMOLOG of TRITHORAX1 (ATX1), a H3K4-histone methyltransferase, mediates the regulation of fiber cell wall development in inflorescence stems of Arabidopsis thaliana. Genome-wide analysis revealed that the up-regulation of genes involved in secondary wall formation during stem development is largely coordinated by increasing level of H3K4 tri-methylation. Among all histone methyltransferases for H3K4me3 in Arabidopsis, ATX1 is markedly increased during the inflorescence stem development and loss-of-function mutant atx1 was impaired in secondary wall thickening in interfascicular fibers. Genetic analysis showed that ATX1 positively regulates secondary wall deposition through activating the expression of secondary wall NAC master switch genes, SECONDARY WALL-ASSOCIATED NAC DOMAIN PROTEIN1 (SND1) and NAC SECONDARY WALL THICKENING PROMOTING FACTOR1 (NST1). We further identified that ATX1 directly binds the loci of SND1 and NST1, and activates their expression by increasing H3K4me3 levels at these loci. Taken together, our results reveal that ATX1 plays a key role in the regulation of secondary wall biosynthesis in interfascicular fibers during inflorescence stem development of Arabidopsis.

scholarly journals Knockdown of Arabidopsis ROOT UVB SENSITIVE4 Disrupts Anther Dehiscence by Suppressing Secondary Thickening in the Endothecium

2019 ◽  
Vol 60 (10) ◽  
pp. 2293-2306 ◽  
Author(s):  
Shu-Qing Zhao ◽  
Wen-Chao Li ◽  
Yi Zhang ◽  
Alison C Tidy ◽  
Zoe A Wilson
Keyword(s):  
Cell Wall ◽  
Secondary Wall ◽  
Secondary Cell Wall ◽  
Transcript Abundance ◽  
Myb Transcription Factor ◽  
Wall Thickening ◽  
Floral Buds ◽  
Highly Active ◽  
Secondary Thickening ◽  
Secondary Wall Thickening

Abstract ROOT UV-B SENSITIVE4 (RUS4) encodes a protein with no known function that contains a conserved Domain of Unknown Function 647 (DUF647). The DUF647-containing proteins RUS1 and RUS2 have previously been associated with root UV-B-sensing pathway that plays a major role in Arabidopsis early seedling morphogenesis and development. Here, we show that RUS4 knockdown Arabidopsis plants, referred to as amiR-RUS4, were severely reduced in male fertility with indehiscent anthers. Light microscopy of anther sections revealed a significantly reduced secondary wall thickening in the endothecium of amiR-RUS4 anthers. We further show that the transcript abundance of the NAC domain genes NAC SECONDARY WALL THICKENING PROMOTING FACTOR1 (NST1) and NST2, which have been shown to regulate the secondary cell wall thickenings in the anther endothecium, were dramatically reduced in the amiR-RUS4 floral buds. Expression of the secondary cell wall-associated MYB transcription factor genes MYB103 and MYB85 were also strongly reduced in floral buds of the amiR-RUS4 plants. Overexpression of RUS4 led to increased secondary thickening in the endothecium. However, the rus4-2 mutant exhibited no obvious phenotype. Promoter-GUS analysis revealed that the RUS4 promoter was highly active in the anthers, supporting its role in anther development. Taken together, these results suggest that RUS4, probably functions redundantly with other genes, may play an important role in the secondary thickening formation in the anther endothecium by indirectly affecting the expression of secondary cell wall biosynthetic genes.

scholarly journals A Transcriptomic Analysis of Xylan Mutants Does Not Support the Existence of A Secondary Cell Wall Integrity System in Arabidopsis

2018 ◽  
Author(s):  
Nuno Faria Blanc ◽  
Jenny C. Mortimer ◽  
Paul Dupree
Keyword(s):  
Cell Wall ◽  
Cell Walls ◽  
Secondary Cell Wall ◽  
Cell Wall Integrity ◽  
Wall Thickening ◽  
Similar System ◽  
Analogous System ◽  
A Cell ◽  
Secondary Cell Wall Thickening ◽  
Signalling Cascade

AbstractYeast have long been known to possess a cell wall integrity (CWI) system, and recently an analogous system has been described for the primary walls of plants (PCWI) that leads to changes in plant growth and cell wall composition. A similar system has been proposed to exist for secondary cell walls (SCWI). However, there is little data to support this. Here, we analysed the stem transcriptome of a set of cell wall biosynthetic mutants in order to investigate whether cell wall damage, in this case caused by aberrant xylan synthesis, activates a signalling cascade or changes in cell wall synthesis gene expression. Our data revealed remarkably few changes to the transcriptome. We hypothesise that this is because cells undergoing secondary cell wall thickening have entered a committed programme leading to cell death, and therefore a SCWI system would have limited impact. The absence of transcriptomic responses to secondary cell wall alterations may facilitate engineering of the secondary cell wall of plants.

Molecular mechanism of AtGA3OX1 and AtGA3OX2 genes affecting secondary wall thickening in stems in Arabidopsis

2013 ◽  
Vol 35 (5) ◽  
pp. 655-665 ◽  
Author(s):  
Zeng-Guang WANG ◽  
Guo-Hua CHAI ◽  
Zhi-Yao WANG ◽  
Xian-Feng TANG ◽  
Chang-Jiang SUN ◽  
...  
Keyword(s):  
Molecular Mechanism ◽  
Secondary Wall ◽  
Wall Thickening ◽  
Secondary Wall Thickening

Cell wall ultrastructure of palm leaf fibers

IAWA Journal ◽  
2014 ◽  
Vol 35 (2) ◽  
pp. 127-137 ◽  
Author(s):  
Shengcheng Zhai ◽  
Yoshiki Horikawa ◽  
Tomoya Imai ◽  
Junji Sugiyama
Keyword(s):  
Cell Wall ◽  
Secondary Wall ◽  
Secondary Xylem ◽  
Polarized Light ◽  
Leaf Sheath ◽  
Mean Value ◽  
Attenuated Total Reflection ◽  
Cellulose Microfibrils ◽  
Palm Species ◽  
Palm Leaf

The cell wall organization of leaf sheath fibers in different palm species was studied with polarized light microscopy (PLM) and transmission electron microscopy (TEM). The secondary wall of the fibers consisted of only two layers, S1 and S2. The thickness of the S1 layer in leaf sheath fibers from the different palm species ranged from 0.31 to 0.90 μm, with a mean value of 0.57 μm, which was thicker than that of tracheids and fibers in secondary xylem of conifers and dicotyledons. The thickness of the S2 layer ranged from 0.44 to 3.43 μm, with a mean value of 1.86 μm. The ratio of S1 thickness to the whole cell wall thickness in palm fibers appears to be higher than in secondary xylem fibers and tracheids. The lignin in the fiber walls is very electron dense which makes it difficult to obtain high contrast of the different layers in the secondary wall. To clarify the cell wall layering with cellulose microfibrils in different orientations, the fibrovascular bundles of the windmill palm (Trachycarpus fortunei) were delignified with different reaction time intervals. The treated fibers were surveyed using attenuated total reflection Fourier transform infrared (ATR-FTIR) spectroscopy analysis and TEM. The secondary fiber walls of windmill palm clearly showed only two layers at different reaction intervals with different lignin contents, even after almost all lignin was removed. We suggest that the two-layered structure in the secondary wall of palm leaf fibers, which presumably also applies to the homologous fibers in palm stems, is a specific character different from the fibers in other monocotyledons (such as bamboo and rattan) and dicot wood.

scholarly journals Cell fusion in yeast is negatively regulated by components of the cell wall integrity pathway

2019 ◽  
Vol 30 (4) ◽  
pp. 441-452 ◽  
Author(s):  
Allison E. Hall ◽  
Mark D. Rose
Keyword(s):  
Saccharomyces Cerevisiae ◽  
Cell Death ◽  
Cell Wall ◽  
Yeast Cell ◽  
Cell Fusion ◽  
Cell Walls ◽  
Cell Wall Integrity ◽  
Fusion Genes ◽  
Cell Wall Degradation ◽  
Cell Wall Integrity Pathway

During mating, Saccharomyces cerevisiae cells must degrade the intervening cell wall to allow fusion of the partners. Because improper timing or location of cell wall degradation would cause lysis, the initiation of cell fusion must be highly regulated. Here, we find that yeast cell fusion is negatively regulated by components of the cell wall integrity (CWI) pathway. Loss of the cell wall sensor, MID2, specifically causes “mating-induced death” after pheromone exposure. Mating-induced death is suppressed by mutations in cell fusion genes ( FUS1, FUS2, RVS161, CDC42), implying that mid2Δ cells die from premature fusion without a partner. Consistent with premature fusion, mid2Δ shmoos had thinner cell walls and lysed at the shmoo tip. Normally, Cdc42p colocalizes with Fus2p to form a focus only when mating cells are in contact (prezygotes) and colocalization is required for cell fusion. However, Cdc42p was aberrantly colocalized with Fus2p to form a focus in mid2Δ shmoos. A hyperactive allele of the CWI kinase Pkc1p ( PKC1*) caused decreased cell fusion and Cdc42p localization in prezygotes. In shmoos, PKC1* increased Cdc42p localization; however, it was not colocalized with Fus2p or associated with cell death. We conclude that Mid2p and Pkc1p negatively regulate cell fusion via Cdc42p and Fus2p.

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