Abstract

Sugars are evolutionarily conserved signaling molecules that regulate the growth and development of both unicellular and multicellular organisms. As sugar-producing photosynthetic organisms, plants utilize glucose as one of their major signaling molecules. However, the details of other sugar signaling molecules and their regulatory factors have remained elusive, due to the complexity of the metabolite and hormone interactions that control physiological and developmental programs in plants. We combined information from a gain-of-function cell-based screen and a loss-of-function reverse-genetic analysis to demonstrate that fructose acts as a signaling molecule in Arabidopsis thaliana. Fructose signaling induced seedling developmental arrest and interacted with plant stress hormone signaling in a manner similar to that of glucose. For fructose signaling responses, the plant glucose sensor HEXOKINASE1 (HXK1) was dispensable, while FRUCTOSE INSENSITIVE1 (FINS1), a putative FRUCTOSE-1,6-BISPHOSPHATASE, played a crucial role. Interestingly, FINS1 function in fructose signaling appeared to be independent of its catalytic activity in sugar metabolism. Genetic analysis further indicated that FINS1–dependent fructose signaling may act downstream of the abscisic acid pathway, in spite of the fact that HXK1–dependent glucose signaling works upstream of hormone synthesis. Our findings revealed that multiple layers of controls by fructose, glucose, and abscisic acid finely tune the plant autotrophic transition and modulate early seedling establishment after seed germination.

Highlights

  • Myriad metabolic pathways enable cells to sustain life with basic carbon and nitrogenous compounds

  • We found that fructose functions as a regulatory sugar metabolite and interacts with signaling by the plant hormones abscisic acid (ABA) and ethylene in A. thaliana

  • The fructose-dependent growth response is mediated by FRUCTOSE INSENSITIVE1 (FINS1), which encodes an ancient metabolic enzyme, putative fructose-1,6-bisphosphatase

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Summary

Introduction

Myriad metabolic pathways enable cells to sustain life with basic carbon and nitrogenous compounds. Glucose [7,8,9], sucrose [10,11,12], trehalose-6-phosphate [13], and low energy/high AMP concentrations [14,15] function as cellular signaling molecules in specific regulatory pathways that modulate plant growth and development. A recent study further demonstrated that a refined lowglucose condition can uncouple HXK1-dependent and -independent glucose signaling responses during early A. thaliana seedling establishment [9,20] In both animals and plants, the developmental roles and regulatory functions of hexoses other than glucose have remained largely unknown. Within the last few years, dietary fructose was implicated in mammalian cell signaling perturbation and metabolic syndromes such as insulin resistance, obesity, type 2 diabetes, and high blood pressure [21,22]

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