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.

Keywords: energy sensor kinase; glucose signaling networks; hexokinase; target of rapamycin kinase.

Fig. 1

Arabidopsis glucose-signaling networks. Glucose is generated from the photosynthetic or storage source and transported as sucrose or glucose to the sink tissues and organs to promote cell proliferation, elongation, expansion, and to maintain energy and metabolic homeostasis. The regulatory mechanisms and functions of three master regulators, HXK1, KIN10/11 and TOR, modulated by glucose signals are shown. The glucose signaling networks are intertwined with the signaling pathways controlled by environmental light, nutrients, stresses and microbes, as well as internal hormones, peptides and clock. Red stars mark the action sites of glucose signaling. Glc, glucose; HXK, hexokinase; HKLs, hexokinase-like; KIN, Arabidopsis protein kinase; QC, quiescent center; TOR, target of rapamycin.

Fig. 2

Glucose-TOR-E2Fa signaling regulates the G1 to S transition and promotes cell cycle initiation in meristems. TOR kinase activated by photosynthesis-derived glucose directly phosphorylates E2Fa transcription factor, which leads to the transcriptional activation of S1-phase genes involved in DNA replication in root meristems. The e2fa mutant shows defects in glucose-activated G1-S phase transition and rapid root growth. The glucose-TOR signaling pathway occurs in most cells in the root meristem and is distinct from the conventional pathway mediated by plant growth hormones or cell-specific transcription factors, which activate the expression of CYCD. Elevated CYCD activates CDK, which phosphorylates the RBR suppressor to release E2Fa. CYCD, cyclinD; CDK, cyclin-activated protein kinase; EdU, 5-ethyle-2’-deoxyuridine; RAM, root apical meristem; RBR: retinoblastoma-related; SAM, shoot apical meristem.