Development of an oligosaccharide library to characterise the structural variation in glucuronoarabinoxylan in the cell walls of vegetative tissues in grasses

Tryfona, Theodora; Sorieul, Mathias; Feijao, Carolina; Stott, Katherine; Rubtsov, Denis V.; Anders, Nadine; Dupree, Paul

doi:10.1186/s13068-019-1451-6

Cited by 33 publications

(37 citation statements)

References 63 publications

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“…The hemicellulose composition of the SCW is distinct among gymnosperms, monocots, and eudicots. This suggests that, while the SCWs between these three groups of plants share common features, some unique assembly and architectural principles are at play in each of these types of SCWs (Busse-Wicher et al, 2016b ; Tryfona et al, 2019 ). The hemicellulose component of eudicot SCWs consists mainly of a single type of hemicellulose with a well-defined primary structure, i.e., glucuronoxylan (GX) (Smith et al, 2017 ).…”

Section: Introductionmentioning

confidence: 99%

Xylan Is Critical for Proper Bundling and Alignment of Cellulose Microfibrils in Plant Secondary Cell Walls

et al. 2021

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Plant biomass represents an abundant and increasingly important natural resource and it mainly consists of a number of cell types that have undergone extensive secondary cell wall (SCW) formation. These cell types are abundant in the stems of Arabidopsis, a well-studied model system for hardwood, the wood of eudicot plants. The main constituents of hardwood include cellulose, lignin, and xylan, the latter in the form of glucuronoxylan (GX). The binding of GX to cellulose in the eudicot SCW represents one of the best-understood molecular interactions within plant cell walls. The evenly spaced acetylation and 4-O-methyl glucuronic acid (MeGlcA) substitutions of the xylan polymer backbone facilitates binding in a linear two-fold screw conformation to the hydrophilic side of cellulose and signifies a high level of molecular specificity. However, the wider implications of GX–cellulose interactions for cellulose network formation and SCW architecture have remained less explored. In this study, we seek to expand our knowledge on this by characterizing the cellulose microfibril organization in three well-characterized GX mutants. The selected mutants display a range of GX deficiency from mild to severe, with findings indicating even the weakest mutant having significant perturbations of the cellulose network, as visualized by both scanning electron microscopy (SEM) and atomic force microscopy (AFM). We show by image analysis that microfibril width is increased by as much as three times in the severe mutants compared to the wild type and that the degree of directional dispersion of the fibrils is approximately doubled in all the three mutants. Further, we find that these changes correlate with both altered nanomechanical properties of the SCW, as observed by AFM, and with increases in enzymatic hydrolysis. Results from this study indicate the critical role that normal GX composition has on cellulose bundle formation and cellulose organization as a whole within the SCWs.

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Section: Introductionmentioning

confidence: 99%

Xylan Is Critical for Proper Bundling and Alignment of Cellulose Microfibrils in Plant Secondary Cell Walls

et al. 2021

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“…Little is known about the chemical nature and particularly the structural features underlying cell wall compositional shifts in response to abiotic stresses (Cesarino, 2019; Le Gall et al, 2015; Tenhaken, 2014; Zhao et al, 2019). During recent years, our understanding of cell wall biosynthesis and structure has improved profoundly, for instance, the feruloylation and p ‐coumaroylation of AX (Bartley et al, 2013; Buanafina, Fescemyer, Sharma, & Shearer, 2016; de Souza et al, 2018; de Souza et al, 2019), lignin acylation (Karlen et al, 2016; Karlen et al, 2018; Petrik et al, 2014; Wilkerson et al, 2014; Withers et al, 2012), xylan biosynthesis and structure (Anders et al, 2012; Grantham et al, 2017; Tryfona et al, 2019; Whitehead et al, 2018), and covalent interactions between lignin, xylan and cellulose (Busse‐Wicher et al, 2016; Kang et al, 2019; Simmons et al, 2016). Based on these new findings, we examined how salt stress affects the cell wall composition of maize seedlings and plants.…”

Section: Introductionmentioning

confidence: 99%

Cell wall remodeling under salt stress: Insights into changes in polysaccharides, feruloylation, lignification, and phenolic metabolism in maize

Oliveira

Mota

Salatta

et al. 2020

Plant Cell & Environment

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Although cell wall polymers play important roles in the tolerance of plants to abiotic stress, the effects of salinity on cell wall composition and metabolism in grasses remain largely unexplored. Here, we conducted an in-depth study of changes in cell wall composition and phenolic metabolism induced upon salinity in maize seedlings and plants. Cell wall characterization revealed that salt stress modulated the deposition of cellulose, matrix polysaccharides and lignin in seedling roots, plant roots and stems. The extraction and analysis of arabinoxylans by size-exclusion chromatography, 2D-NMR spectroscopy and carbohydrate gel electrophoresis showed a reduction of arabinoxylan content in salt-stressed roots. Saponification and mild acid hydrolysis revealed that salinity also reduced the feruloylation of arabinoxylans in roots of seedlings and plants. Determination of lignin content and composition by nitrobenzene oxidation and 2D-NMR confirmed the increased incorporation of syringyl units in lignin of maize roots. Salt stress also induced the expression of genes and the activity of enzymes enrolled in phenylpropanoid biosynthesis. The UHPLC-MS-based metabolite profiling confirmed the modulation of phenolic profiling by salinity and the accumulation of ferulate and its derivatives 3-and 4-O-feruloyl

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“…To investigate the biochemical basis for stunting and premature death in the BdGT43B2 CRISPR mutants, polysaccharide analysis by carbohydrate electrophoresis (PACE) (Goubet et al., 2002) was employed (Figure 4). Hydrolysis of eGFP CRISPR control AIR released mainly Xyl, XD 2,3 XX (Xyl [Beta1,2 Xyl‐alpha1,3‐Araf‐]Xyl‐Xyl‐Xyl), XA 3 XX (Xyl [alpha1,3‐Araf‐]Xyl‐Xyl‐Xyl) (Tryfona et al., 2019) and some further uncharacterized oligosaccharides. Notably, the hydrolysis of both BdGT43B2 CRISPR line AIR (41A and 165B) showed a clear decrease in the intensity of all bands, indicating the mutants contained reduced amounts of digestible xylan.…”

Section: Resultsmentioning

confidence: 99%

BdGT43B2 functions in xylan biosynthesis and is essential for seedling survival in Brachypodium distachyon

et al. 2020

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Xylan is the predominant hemicellulose in the primary cell walls of grasses, but its synthesis and interactions with other wall polysaccharides are complex and incompletely understood. To probe xylan biosynthesis, we generated CRISPR/Cas9 knockout and amiRNA knockdown lines of BdGT43B2, an ortholog of the wheat TaGT43-4 xylan synthase scaffolding protein in the IRX14 clade, in Brachypodium distachyon.Knockout of BdGT43B2 caused stunting and premature death in Brachypodium seedlings. Immunofluorescence labeling of xylans was greatly reduced in homozygous knockout BdGT43B2 mutants, whereas cellulose labeling was unchanged or slightly increased. Biochemical analysis showed reductions in digestible xylan in knockout mutant walls, and cell size was smaller in knockout leaves. BdGT43B2 knockdown plants appeared morphologically normal as adults, but showed slight reductions in seedling growth and small decreases in xylose content in isolated cell walls. Immunofluorescence labeling of xylan and cellulose staining was both reduced inBdGT43B2 knockdown plants. Together, these data indicate that BdGT43B2 functions in the synthesis of a form of xylan that is required for seedling growth and survival in Brachypodium distachyon. K E Y W O R D S artificial microRNA (amiRNA), Brachypodium distachyon, CRISPR/Cas9, glycosyl transferase, polysaccharide analysis by carbohydrate electrophoresis, xylanBrachypodium distacyhon is a useful model species for the analysis of grass cell walls because it is diploid, has a small stature and an 8-10 week seed-to-seed life cycle, has a sequenced genome, and is relatively easy to transform (Vogel et al., 2010). The composition of its cell walls has been characterized (Rancour, Marita, & Hatfield, 2012). Phylogenetic analysis of Brachypodium distachyon GT43 members shows that there are eight members in Clade A and two members in Clade B (Whitehead et al., 2018). RNAi knockdown of one these GT43 genes, Bradi5g24290, results in modestly reduced

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Development of an oligosaccharide library to characterise the structural variation in glucuronoarabinoxylan in the cell walls of vegetative tissues in grasses

Cited by 33 publications

References 63 publications

Xylan Is Critical for Proper Bundling and Alignment of Cellulose Microfibrils in Plant Secondary Cell Walls

Xylan Is Critical for Proper Bundling and Alignment of Cellulose Microfibrils in Plant Secondary Cell Walls

Cell wall remodeling under salt stress: Insights into changes in polysaccharides, feruloylation, lignification, and phenolic metabolism in maize

BdGT43B2 functions in xylan biosynthesis and is essential for seedling survival in Brachypodium distachyon

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