In Concert: Orchestrated Changes in Carbohydrate Homeostasis Are Critical for Plant Abiotic Stress Tolerance

Abstract

The sessile lifestyle of higher plants is accompanied by their remarkable ability to tolerate unfavorable environmental conditions. This is because, during evolution, plants developed a sophisticated repertoire of molecular and metabolic reactions to cope with changing biotic and abiotic challenges. In particular, the abiotic factors light intensity and ambient temperature are characterized by altering their amplitude within comparably short periods of time and are causative for onset of dynamic plant responses. These rapid responses in plants are also classified as 'acclimation reactions' which differ, due to their reversibility and duration, from non-reversible 'adaptation reactions'. In this review, we demonstrate the remarkable importance of stress-induced changes in carbohydrate homeostasis of plants exposed to high light or low temperatures. These changes represent a co-ordinated process comprising modifications of (i) the concentrations of selected sugars; (ii) starch turnover; (iii) intracellular sugar compartmentation; and (iv) corresponding gene expression patterns. The critical importance of these individual processes has been underlined in the recent past by the analyses of a large number of mutant plants. The outcome of these analyses raised our understanding of acclimation processes in plants per se but might even become instrumental to develop new concepts for directed breeding approaches with the aim to increase abiotic stress tolerance of crop species, which in most cases have high stress sensitivity. The latter direction of plant research is of special importance since abiotic stress stimuli strongly impact on crop productivity and are expected to become even more pronounced because of human activities which alter environmental conditions rapidly.

Vacuolar sucrose cleavage prevents limitation of cytosolic carbohydrate metabolism and stabilizes photosynthesis under abiotic stress

“…Yet, underlying biochemical and regulatory mechanisms are less clear [38]. Predominantly, this is due to diverse roles of sugars and involved enzymes in osmoregulation, cryoprotection, membrane stabilization, signalling and ROS scavenging [32,[39][40][41][42][43]. In previous studies, the sucrose biosynthesis pathway was shown to be a limiting factor in cold acclimation [33,41].…”

Metatranscriptomic and metabolite profiling reveals vertical heterogeneity within a Zygnema green algal mat from Svalbard (High Arctic)

“…The highly hydroxylated and soluble sugars may generally serve as efficient ROS quenchers and in membranes may be involved in scavenging hydroxyl radicals generated by lipid peroxidation. In response to abiotic stress factors, such as high light or low temperatures, higher plants typically accumulate the disaccharide sucrose as well as the monosaccharides glucose and fructose (Pommerrenig et al, 2018). Sugar alcohols possess more hydroxyl groups than their sugar precursors, and often accumulate in response to oxidative stress (Pommerrenig et al, 2018).…”

“…In response to abiotic stress factors, such as high light or low temperatures, higher plants typically accumulate the disaccharide sucrose as well as the monosaccharides glucose and fructose (Pommerrenig et al, 2018). Sugar alcohols possess more hydroxyl groups than their sugar precursors, and often accumulate in response to oxidative stress (Pommerrenig et al, 2018). The metabolite profile of Zygnema also indicated an accumulation of the sugar alcohols sorbitol and mannitol in the top layer of the mat, which could be a response to ROS formation.…”

“…These enzymes complement, or work in synergy with, low-molecular-weight antioxidants such as ascorbate, glutathione and tocochromanols (Kranner et al, 2010). In addition, carbohydrates and sugar alcohols may also scavenge ROS in photosynthetic organisms (Pommerrenig et al, 2018).…”

Vacuolar sucrose homeostasis is critical for development, seed properties and survival of dark phases of Arabidopsis

“…8C). Since sucrose fulfills various roles in plant development and stress response (Rolland 488 et al, 2006;Hanson and Smeekens, 2009;Teng et al, 2005) it appears likely that its 489 intracellular homeostasis must be tightly regulated (Pommerrenig et al, 2018). This 490 assumption gained direct support by the recent discovery of a chloroplast located 491 sucrose exporter pSuT, which is involved in fine control of the onset of flowering and 492 frost tolerance of Arabidopsis (Patzke et al, 2019).…”