Dissecting the roles of osmolyte accumulation during stress

TLDR

Plants accumulate organic osmolytes under environmental stresses that cause cellular dehydration, and while this accumulation is thought to mediate osmotic adjustment and protect subcellular structures, evidence is largely correlative and may also involve metabolic benefits and signaling pathways such as hexose and redox signaling. The study aims to reassess whether synthesis of proline and glycine betaine buffers cellular redox potential and thereby contributes to stress tolerance. The authors investigate this by examining transgenic plants engineered to produce trehalose, fructans, or mannitol, focusing on disturbances in hexose sensing and altered photoassimilate allocation between root and shoot tissues that may underlie observed stress‑tolerant phenotypes. Transgenic accumulation of proline, mannitol, fructans, trehalose, glycine betaine, or ononitol yields only marginal improvements in salt and/or drought tolerance, suggesting that absolute osmolyte concentrations are unlikely to mediate osmotic adjustment.

Abstract

Many plants accumulate organic osmolytes in response to the imposition of environmental stresses that cause cellular dehydration. Although an adaptive role for these compounds in mediating osmotic adjustment and protecting subcellular structure has become a central dogma in stress physiology, the evidence in favour of this hypothesis is largely correlative. Transgenic plants engineered to accumulate proline, mannitol, fructans, trehalose, glycine betaine or ononitol exhibit marginal improvements in salt and/or drought tolerance. While these studies do not dismiss causative relationships between osmolyte levels and stress tolerance, the absolute osmolyte concentrations in these plants are unlikely to mediate osmotic adjustment. Metabolic benefits of osmolyte accumulation may augment the classically accepted roles of these compounds. In re‐assessing the functional significance of compatible solute accumulation, it is suggested that proline and glycine betaine synthesis may buffer cellular redox potential. Disturbances in hexose sensing in transgenic plants engineered to produce trehalose, fructans or mannitol may be an important contributory factor to the stress‐tolerant phenotypes observed. Associated effects on photoassimilate allocation between root and shoot tissues may also be involved. Whether or not osmolyte transport between subcellular compartments or different organs represents a bottleneck that limits stress tolerance at the whole‐plant level is presently unclear. None the less, if osmolyte metabolism impinges on hexose or redox signalling, then it may be important in long‐range signal transmission throughout the plant.