Master regulators in plant glucose signaling networks

Abstract

The daily life of photosynthetic plants revolves around sugar production, transport, storage and utilization, and the complex sugar metabolic and signaling networks integrate internal regulators and environmental cues to govern and sustain plant growth and survival. Although diverse sugar signals have emerged as pivotal regulators from embryogenesis to senescence, glucose is the most ancient and conserved regulatory signal that controls gene and protein expression, cell-cycle progression, central and secondary metabolism, as well as growth and developmental programs. Glucose signals are perceived and transduced by two principal mechanisms: direct sensing through glucose sensors and indirect sensing via a variety of energy and metabolite sensors. This review focuses on the comparative and functional analyses of three glucose-modulated master regulators in Arabidopsis thaliana, the hexokinase1 (HXK1) glucose sensor, the energy sensor kinases KIN10/KIN11 inactivated by glucose, and the glucose-activated target of rapamycin (TOR) kinase. These regulators are evolutionarily conserved, but have evolved universal and unique regulatory wiring and functions in plants and animals. They form protein complexes with multiple partners as regulators or effectors to serve distinct functions in different subcellular locales and organs, and play integrative and complementary roles from cellular signaling and metabolism to development in the plant glucose signaling networks.

Effects of glucose and gibberellic acid on glucosinolate content and antioxidant properties of Chinese kale sprouts

“…The glucosinolate content varies depending on genetic and environmental factors, and is modulated by external signals such as sugar (Miao et al, 2013) and phytohormones (Yuan et al, 2009;Sun et al, 2012;Wang et al, 2012;Guo et al, 2013a;2013b;Huseby et al, 2013;Kim et al, 2013;Zang et al, 2015). Glucose is not only the basal carbon and energy source but also a signaling molecule having regulatory effects throughout the life cycle of plant (Sheen, 2014). Our previous studies showed that glucose dramatically increases glucosinolate content in both Arabidopsis and crop brassicas (Wei et al, 2011;Guo et al, 2013c;Miao et al, 2013).…”

Plant respiration under low oxygen

“…For instance, studies on the enzymatic functionality of glycolysis have determined the importance of phosphoglucomutase (PGM) in starch formation processes in both heterotrophic (root and seed) and autotrophic tissues as well as the role of hexokinases (HXK) and other enzymes such as the glucose signaling network (Sheen, 2014). Regarding the TCA cycle, some progress has been made in understanding how alternative pathways involving γ-aminobutyric acid (GABA) and the glyoxylate cycle operate, with special attention given to changes in the optimal conditions, in order to show the high level of plasticity in the response of the TCA cycle to environmental changes (Sweetlove et al, 2010).…”

Sugar-induced plant growth is dependent on brassinosteroids

“…1,2 Glucose (Glc) and sucrose (Suc), 2 kinds of metabolic sugars that are widely present in plants, have been recognized as pivotal integrating regulatory molecules that control gene expression related to plant metabolism, stress responses, and other growth and development related processes including seed germination, floral transition, fruit ripening, embryogenesis, and senescence. [2][3][4] While little is known to the signaling mechanisms of Suc, part of the signal transduction pathways of Glc in plants has been established, which include 3 distinct pathways: HEXOKINASE1 (HXK1)-dependent pathway, HXK1-independent pathway, and glycolysis-dependent pathway that utilizes the SUCROSE NONFERMENTING RELATED KINASE1 (SnRK1)/TARGET OF RAPAMYCIN (TOR) pathway. 5 Discovery of unique and global repression of photosynthetic genes by Glc in Arabidopsis led to identification of HXK1 as the first plant Glc sensor, which mediates Glc repression or promotion of gene transcription and plant growth.…”

“…6,7 Later on, diverse isoforms of HXK and HXK-like (HXL) genes were found in the genomes of many plants, including rice, maize, tomato, tobacco and Arabidopsis, which suggests that plants have evolved a complex mode of Glc signaling to support various growth strategies and architectures dictated by sugar availability. 4,7 Suc is the major transport sugar in higher plants and could also initiate signaling pathways leading to changes of gene expression and physiological adaptation, but a Suc sensor has not be identified. 8 Brassinosteroids (BRs) are a class of polyhydroxylated sterol derivatives that regulate diverse developmental and physiological processes, including seed germination, seedling photomorphogenesis, stomata differentiation, organ boundary formation, flowering, male fertility, and even responses to biotic and abiotic stresses.…”

“…10,12,14,15 Sugars repress plant growth in the light, whereas they promote growth in the dark, indicating that the sugar regulation of growth is mediated through different pathways in the light and dark. 4,[15][16][17][18][19] In Arabidopsis, Phytochrome-Interacting Factors (PIFs) and the plant hormone gibberellin (GA) have been shown to play important roles in sugar-induced hypocotyl elongation under both dark and short photoperiod conditions. [17][18][19] In a recent study, we found that sugar-induced hypocotyl elongation and the expression of genes important for cell elongation in Arabidopsis seedlings could be significantly repressed by the treatment with brassinazole (BRZ), a biosynthetic inhibitor of BRs, suggesting that BR is important for sugar regulation of plant growth in darkness.…”