Lack of xyloglucan in the cell walls of the Arabidopsis xxt1/xxt2 mutant results in specific increases in homogalacturonan and glucomannan

Abstract

Mutations in both ArabidopsisXyloglucan Xylosyltransferase1 (XXT1) and Xyloglucan Xylosyltransferase2 (XXT2) result in the absence of the major hemicellulose, xyloglucan (XyG). The growth physiology, tensile strength, and cell wall compositions of etiolated hypocotyls of xxt1/xxt2 double and xxt1/xxt2/xxt5 triple mutants were characterized and compared with those of mur2 and mur3 mutations that alter the side group composition of XyG. Wild type and mur2 demonstrated normal elongation growth, whereas the xxt double and triple mutants and mur3 showed reduced elongation and cell swelling at the base of the hypocotyl at the later stages of elongation. Whereas mur3 hypocotyls had reduced tensile strength, the xxt double and triple mutants had similar tensile strengths as wild type, but reached breaking points at lower strains. Loss of XyG in hypocotyls and rosette leaf cell walls was associated with specific increases in the relative abundance of homogalacturonan and the hemicellulose glucomannan, but not arabinoxylan. The increased homogalacturonan and glucomannan abundance did not result from enhanced expression of their polymer synthases. An analysis of published transcriptomic data indicated that genes encoding some members of the expansin, xyloglucan endotransglucosylase/hydrolase, arabinogalactan-protein, and structural protein families were upregulated in the xxt mutants. We hypothesize that an as yet unknown mechanism exists by which pectin and hemicellulose abundance can be altered other than by increased rates of biosynthesis to maintain a structurally sound cell wall.

Eudicot primary cell wall glucomannan is related in synthesis, structure, and function to xyloglucan

“…Recently glucomannan has also been implicated in etiolated hypocotyl gravitropic bending, which involves asymmetric cell expansion ( Somssich et al, 2021 ). In addition, an increase in glucomannan abundance was recently observed in xxt1 xxt2 mutants ( Sowinski et al, 2022 ), which led to the suggestion that other matrix polysaccharides may compensate for a lack of XyG. Despite examples that glucomannan is important in some instances, the role for PCW glucomannan in plant growth and development, and whether that role is related to that of other hemicelluloses, remains obscure.…”

Building an extensible cell wall

“…Related points: As noted above, cell walls of the xxt1,xxt2 line were more compliant in stretching assays compared with wild-type, yet shoot growth was slightly reduced ( Park and Cosgrove, 2012a ; Xiao et al, 2016 ; Sowinski et al, 2022 ). Epidermal walls of the xxt1,xxt2 line lost their normal cross-ply structure ( Xiao et al, 2016 ) and exhibited a diminished “acid growth” response ( Xin et al, 2020 ), which is mediated by endogenous α-expansins ( Cosgrove, 2000 ).…”

“…Subtle phenotypes also occurred in the shoot apical meristem, including changes in meristem shape, microtubule patterning, and exaggerated microtubule instabilities ( Zhao et al, 2019 ). Sowinski et al (2022) documented increases in pectin and glucomannan in xxt1,xxt2 hypocotyls, but negligible changes in leaves. In evaluating xyloglucan mutants, it is difficult to disentangle direct mechanical effects of the xyloglucan deficiency from indirect or pleiotropic effects.…”

“…Because transverse microfibrils offer little resistance to axial stretching ( Zhang et al, 2021c ), the change in cellulose orientation likely accounts for the increased compliance of the walls lacking xyloglucan. An increased brittleness ( Sowinski et al, 2022 ) may also arise from altered cellulose organization. This is another example in which the facile interpretation of a wall phenotype may be misleading.…”

Gibberellin-related genes regulate dwarfing mechanism in wintersweet

“…The identified HUB genes included CpXTH23, CpCSLC12, CpGATL9 ( GAUT-Like 9 ), CpXXT2 , and CpCESA2/5 . These genes and their homologous genes are involved in cell wall formation in other plants and influence stem diameter and elongation ( Turner and Somerville, 1997 ; Burn et al, 2002 ; Cocuron et al, 2007 ; Kong et al, 2011 ; Guo et al, 2020 ; Sowinski et al, 2022 ). In rice, GA can upregulate the expression of the OsXTH8 gene, while other hormones have little effect on OsXTH8 ( Jan et al, 2004 ).…”