Sugar and hexokinase suppress expression of PIP aquaporins and reduce leaf hydraulics that preserves leaf water potential

Abstract

Sugars affect central aspects of plant physiology, including photosynthesis, stomatal behavior and the loss of water through the stomata. Yet, the potential effects of sugars on plant aquaporins (AQPs) and water conductance have not been examined. We used database and transcriptional analyses, as well as cellular and whole-plant functional techniques to examine the link between sugar-related genes and AQPs. Database analyses revealed a high level of correlation between the expression of AQPs and that of sugar-related genes, including the Arabidopsis hexokinases 1 (AtHXK1). Increased expression of AtHXK1, as well as the addition of its primary substrate, glucose (Glc), repressed the expression of 10 AQPs from the plasma membrane-intrinsic proteins (PIP) subfamily (PIP-AQPs) and induced the expression of two stress-related PIP-AQPs. The osmotic water permeability of mesophyll protoplasts of AtHXK1-expressing plants and the leaf hydraulic conductance of those plants were significantly reduced, in line with the decreased expression of PIP-AQPs. Conversely, hxk1 mutants demonstrated a higher level of hydraulic conductance, with increased water potential in their leaves. In addition, the presence of Glc reduced leaf water potential, as compared with an osmotic control, indicating that Glc reduces the movement of water from the xylem into the mesophyll. The production of sugars entails a significant loss of water and these results suggest that sugars and AtHXK1 affect the expression of AQP genes and reduce leaf water conductance, to coordinate sugar levels with the loss of water through transpiration.

Linking water relations and hydraulics with photosynthesis

“…The apoplastic pathway via cell walls is often implicitly assumed to be the major pathway of water transport through the outside xylem (Buckley, 2015). However, the observation of aquaporin-mediated water transport in BS using aquaporin mutants means that the symplastic pathway is in fact plausible (Sade et al, 2010(Sade et al, , 2014Prado et al, 2013;Kelly et al, 2017). Other evidence for symplastic water transport comes from the diurnal rhythms in K leaf , and the dynamic response of K leaf to environmental changes including temperature and light intensity.…”

Regulatory roles of sugars in plant growth and development

“…The results indicated the role of chloroplasts in the regulation of the increase in leaf area, depending on the access to sugars [40]. The effects of sugars on plant aquaporins (and water conductance) have recently been examined; it was observed that glucose reduces the movement of water from the xylem to the mesophyll [41], which could also affect leaf growth. It has also been shown that sugars (such as, glucose and sucrose) can affect the movement of cellular organelles, including chloroplasts [42,43].…”

HEXOKINASE 1 Control of Post-Germinative Seedling Growth

“…As for SD, in LD CAA levels are relatively unchanged by light dose in wild type and gin2 . Earlier studies have reported that HXK1 transcript abundance is upregulated by glucose application ( Price et al, 2004; Yang et al, 2013; Kelly et al, 2017 ). In both our SD and LD conditions we do not observe a fluence rate dependent regulation of HXK1 transcript levels.…”