Ride to cell wall: Arabidopsis XTH11, XTH29 and XTH33 exhibit different secretion pathways and responses to heat and drought stress. (7th June 2021)

• Record Type: Journal Article
• Authors: De Caroli, Monica; Manno, Elisa; Piro, Gabriella; Lenucci, Marcello S.
• Is Part Of: Plant journal. Volume 107:Number 2(2021)
• Page Start: 448
• Page End: 466
• Publication Date: 2021-06-07
• Subjects: XTH -- UPS -- EXPO -- cell wall trafficking -- heat stress -- drought stress -- Arabidopsis thaliana; Plant molecular biology -- Periodicals; Plant cells and tissues -- Periodicals; Botany -- Periodicals; 580
• DOI: 10.1111/tpj.15301
• Languages: English
• ISSNs: 0960-7412

Abstract

Summary: The xyloglucan endotransglucosylase/hydrolases (XTHs) are enzymes involved in cell wall assembly and growth regulation, cleaving and re‐joining hemicellulose chains in the xyloglucan–cellulose network. Here, in a homologous system, we compare the secretion patterns of XTH11, XTH33 and XTH29, three members of the Arabidopsis thaliana XTH family, selected for the presence (XTH11 and XTH33) or absence (XTH29) of a signal peptide, and the presence of a transmembrane domain (XTH33). We show that XTH11 and XTH33 reached, respectively, the cell wall and plasma membrane through a conventional protein secretion (CPS) pathway, whereas XTH29 moves towards the apoplast following an unconventional protein secretion (UPS) mediated by exocyst‐positive organelles (EXPOs). All XTHs share a common C‐terminal functional domain (XET‐C) that, for XTH29 and a restricted number of other XTHs (27, 28 and 30), continues with an extraterminal region (ETR) of 45 amino acids. We suggest that this region is necessary for the correct cell wall targeting of XTH29, as the ETR‐truncated protein never reaches its final destination and is not recruited by EXPOs. Furthermore, quantitative real‐time polymerase chain reaction analyses performed on 4‐week‐old Arabidopsis seedlings exposed to drought and heat stress suggest a different involvement of the three XTH s in cell wall remodeling under abiotic stress, evidencing stress‐, organ‐ and time‐dependent variations in the expression levels. Significantly, XTH29, codifying the only XTH that follows a UPS pathway, is highly upregulated with respect to XTH11 and XTH33, which code for CPS‐secreted proteins. Significance Statement: The cellular distribution of three xyloglucan endotransglucosylase/hydrolases (XTHs) was monitored comparatively while expressing respective fluorescent constructs in Arabidopsis cotyledons. We show that XTH11 and XTH33 follow conventional protein secretion towards cell wall and plasma membrane, respectively, whereas XTH29, the only XTH predicted to lack a signal peptide, is secreted into the wall via exocyst‐positive organelle‐mediated unconventional protein secretion (UPS). Significantly, XTH29, poorly expressed in physiological conditions, demonstrates upregulation under drought and high temperature conditions, suggesting a specific possible role for UPS‐secreted XTH29 in stress responses.