Localisation and substrate specificities of transglycanases in charophyte algae relate to development and morphology.

Jenny Russinova,Klaus Herburger,Louise M Ryan,Zoë A Popper,Andreas Holzinger

doi:10.1242/jcs.203208

Abstract

ABSTRACTCell wall-modifying enzymes have been previously investigated in charophyte green algae (CGA) in cultures of uniform age, giving limited insight into their roles. Therefore, we investigated the in situ localisation and specificity of enzymes acting on hemicelluloses in CGA genera of different morphologies and developmental stages. In vivo transglycosylation between xyloglucan and an endogenous donor in filamentous Klebsormidium and Zygnema was observed in longitudinal cell walls of young (1 month) but not old cells (1 year), suggesting that it has a role in cell growth. By contrast, in parenchymatous Chara, transglycanase action occurred in all cell planes. In Klebsormidium and Zygnema, the location of enzyme action mainly occurred in regions where xyloglucans and mannans, and to a lesser extent mixed-linkage β-glucan (MLG), were present, indicating predominantly xyloglucan:xyloglucan endotransglucosylase (XET) activity. Novel transglycosylation activities between xyloglucan and xylan, and xyloglucan and galactomannan were identified in vitro in both genera. Our results show that several cell wall-modifying enzymes are present in CGA, and that differences in morphology and cell age are related to enzyme localisation and specificity. This indicates an evolutionary significance of cell wall modifications, as similar changes are known in their immediate descendants, the land plants. This article has an associated First Person interview with the first author of the paper.

Highlights

IntroductionIt has been shown recently that flexible cell walls mediated by desiccationinduced callose deposition in Klebsormidium (Herburger and Holzinger, 2015) or the specific occurrence of pectic substances in the macroalgae Ulva compressa (Holzinger et al, 2015) coincide with elevated desiccation tolerance in aero-terrestrial or intertidal habitats, respectively
Age-dependent cell wall thickening correlates with higher proportion of pectins or hemicelluloses To test whether increasing cell age (1 month compared to 1 year) changes the cell wall composition of Klebsormidium and Zygnema S, the alcohol-insoluble residue (AIR) of algal filaments was fractionated (Fig. 1) and analysed
Increasing cell age increased the total hemicellulose content of Klebsormidium. This suggests that age-dependent cell wall thickening in Zygnema is characterized by an increase in the pectin content, while in Klebsormidium cell walls are thickened by deposition of hemicelluloses

Summary

Introduction

It has been shown recently that flexible cell walls mediated by desiccationinduced callose deposition in Klebsormidium (Herburger and Holzinger, 2015) or the specific occurrence of pectic substances in the macroalgae Ulva compressa (Holzinger et al, 2015) coincide with elevated desiccation tolerance in aero-terrestrial or intertidal habitats, respectively. This suggests that modulating the cell wall architecture and composition in response to abiotic stress was crucial for the survival of algal colonizers of terrestrial habitats. The cell walls of various CGA have been explored over the past decades, there are many remaining questions regarding the localisation and metabolism of specific wall components

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