Overexpression of a proton‐coupled vacuolar glucose exporter impairs freezing tolerance and seed germination

Abstract

SummaryArabidopsis vacuoles harbor, besides sugar transporter of the TMT-type, an early response to dehydration like 6 (ERDL6) protein involved in glucose export into the cytosol. However, the mode of transport of ERDL6 and the plant's feedback to overexpression of its activity on essential properties such as, for example, seed germination or freezing tolerance, remain unexplored.Using patch-clamp studies on vacuoles expressing AtERDL6 we demonstrated directly that this carrier operates as a proton-driven glucose exporter.Overexpression of BvIMP, the closest sugar beet (Beta vulgaris) homolog to AtERDL6, in Arabidopsis leads surprisingly to impaired seed germination under both conditions, sugar application and low environmental temperatures, but not under standard conditions. Upon cold treatment, BvIMP overexpressor plants accumulated lower quantities of monosaccharides than the wild-type, a response in line with the reduced frost tolerance of the transgenic Arabidopsis plants, and the fact that cold temperatures inhibits BvIMP transcription in sugar beet leaves. With these findings we show that the tight control of vacuolar sugar import and export is a key requisite for cold tolerance and seed germination of plants.

Effects of cold acclimation on sugar metabolism and sugar-related gene expression in tea plant during the winter season

“…Recently, Gong et al (2015) reported that AtSUC2 and AtSUC4 were induced by cold and loss-of-function mutations resulted in hypersensitive responses to abiotic stress. Additionally, most cold-induced transporters are positively correlated with plant cold tolerance via the modulation of sugar allocation, such as MfINT-like (Sambe et al 2015), BvIMP (ERD6-like) (Klemens et al 2013b) and AtTMTs (Schulze et al 2012;Wormit et al 2006), suggesting that the up-regulated genes in the tea plant could exhibit similar functions as their homologous genes.…”

“…8b, c), but these genes might differ from the SWEET types under cold stress. Recently, Klemens et al (2013b) identified a ERD6-like transporter gene from the sugar beet and showed that its expression was inhibited by cold stress, and overexpression of ERD6 in Arabidopsis led to reduced frost tolerance. However, the ability to transport sugar in response to cold is not only dependent on mRNA abundance but on control via protein modifications, such as phosphorylation (Schulze, et al 2012).…”

Intracellular and cell-to-apoplast compartmentation of carbohydrate metabolism

“…ERDL6 was recently characterized as a novel dehydration-induced glucose exporter [68]. The Arabidopsis mutant of this transporter displayed a considerable increase in seed weight as a consequence of elevated levels of seed sugars, proteins, and lipids [68], whereas plants overexpressing this transporter were recently demonstrated to display impaired freezing tolerance and seed germination [69]. Mutants of the inositol proton transporter develop very short roots, a phenotype that could be rescued by inositol feeding and that appears to be due to a shortage of precursors for lipid or inositol phosphate signaling [70].…”

“…The precise function of most of the non-sucrose long-distance transport pathways is currently not well characterized; however, the isolation and biochemical characterization of many transport proteins have recently been documented (see for example [96,97]). Furthermore, reverse genetic experimentation has recently begun to shed light on the importance of some of these pathways [69,98], suggesting that we will shortly be able to assess their relative importance under a range of (a)biotic challenges.…”

The Malus domestica sugar transporter gene family: identifications based on genome and expression profiling related to the accumulation of fruit sugars

“…At the vacuolar membrane, the MST subfamilies, vacuolar glucose transporter (vGT), and tonoplast membrane transporter (TMT) function as sugar/H+ antiporters that load sugars into the vacuole (Wormit et al, 2006; Aluri and Büttner, 2007; Schulz et al, 2011). Proteins of the MST subfamily of ERD six-like transporters (ERD6 or ESL1) are likely involved in energy-independent sugar efflux from the vacuole (Poschet et al, 2011; Klemens et al, 2014). …”