Glucose and ethylene signal transduction crosstalk revealed by an Arabidopsis glucose-insensitive mutant

Abstract

Glucose is an essential signaling molecule that controls plant development and gene expression through largely unknown mechanisms. To initiate the dissection of the glucose signal transduction pathway in plants by using a genetic approach, we have identified an Arabidopsis mutant, gin1 (glucose-insensitive), in which glucose repression of cotyledon greening and expansion, shoot development, f loral transition, and gene expression is impaired. Genetic analysis indicates that GIN1 acts downstream of the sensor hexokinase in the glucose signaling pathway. Surprisingly, gin1 insensitivity to glucose repression of cotyledon and shoot development is phenocopied by ethylene precursor treatment of wild-type plants or by constitutive ethylene biosynthesis and constitutive ethylene signaling mutants. In contrast, the ethylene insensitive mutant etr1-1 exhibits glucose hypersensitivity. Epistasis analysis places GIN1 downstream of the ethylene receptor, ETR1, and defines a new branch of ethylene signaling pathway that is uncoupled from the triple response induced by ethylene. The isolation and characterization of gin1 reveal an unexpected convergence between the glucose and the ethylene signal transduction pathways. GIN1 may function to balance the control of plant development in response to metabolic and hormonal stimuli that act antagonistically.Glucose has profound effects on gene expression, metabolism, and development in microorganisms, animals, and plants (1-9). Although the glucose signal transduction pathways are well characterized in unicellular microorganisms, relatively little is known about the molecular basis of glucose responses in multicellular eukaryotes. In higher plants, glucose has been implicated to be the primary sugar signal that controls many aspects of plant development, including germination, hypocotyl elongation, cotyledon greening and expansion, primary and lateral root growth, true leaf development, floral transition, and the onset of senescence. At the molecular level, the expression of a broad spectrum of genes is either repressed or induced by glucose (4-9). Recently, hexokinase (HXK), the enzyme that catalyzes the phosphorylation of hexose sugars at the first step of the glycolytic pathway, has been shown to be the glucose sensor in plants (9-12). Studies in transgenic Arabidopsis plants with elevated or reduced Arabidopsis thaliana HXK levels or with a heterologous yeast HXK provide supporting evidence that HXK is a bifunctional enzyme with catalytic and regulatory activities, and glucose signaling may be uncoupled from glucose metabolism in plants (12). However, the downstream components in the glucose-signaling pathway are mostly unknown. Although interactions between sugar and light or hormonal signaling pathways have been suggested (13-23), the mechanisms underlying the crosstalk between glucose and other signaling pathways remain obscure.We report here the phenotypic, molecular, and genetic analyses of a recessive Arabidopsis mutant (glucose-insensitive, gin1) that is defective...

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