The trehalose pathway in maize: conservation and gene regulation in response to the diurnal cycle and extended darkness.

Clémence Henry,L Mark Lagrimini,Mark Stitt,Alec Kollman,Regina Feil,Brian M Waters,Allison Siekman,Samuel W Bledsoe

doi:10.1093/jxb/eru335

Abstract

Energy resources in plants are managed in continuously changing environments, such as changes occurring during the day/night cycle. Shading is an environmental disruption that decreases photosynthesis, compromises energy status, and impacts on crop productivity. The trehalose pathway plays a central but not well-defined role in maintaining energy balance. Here, we characterized the maize trehalose pathway genes and deciphered the impacts of the diurnal cycle and disruption of the day/night cycle on trehalose pathway gene expression and sugar metabolism. The maize genome encodes 14 trehalose-6-phosphate synthase (TPS) genes, 11 trehalose-6-phosphate phosphatase (TPP) genes, and one trehalase gene. Transcript abundance of most of these genes was impacted by the day/night cycle and extended dark stress, as were sucrose, hexose sugars, starch, and trehalose-6-phosphate (T6P) levels. After extended darkness, T6P levels inversely followed class II TPS and sucrose non-fermenting-related protein kinase 1 (SnRK1) target gene expression. Most significantly, T6P no longer tracked sucrose levels after extended darkness. These results showed: (i) conservation of the trehalose pathway in maize; (ii) that sucrose, hexose, starch, T6P, and TPS/TPP transcripts respond to the diurnal cycle; and(iii) that extended darkness disrupts the correlation between T6P and sucrose/hexose pools and affects SnRK1 target gene expression. A model for the role of the trehalose pathway in sensing of sucrose and energy status in maize seedlings is proposed.

Highlights

A central feature of plant metabolism is the photosynthetic conversion of light energy into stored chemical energy
T6P no longer tracked sucrose levels after extended darkness. These results showed: (i) conservation of the trehalose pathway in maize; (ii) that sucrose, hexose, starch, T6P, and trehalose-6-phosphate synthase (TPS)/trehalose-6-phosphate phosphatase (TPP) transcripts respond to the diurnal cycle; and(iii) that extended darkness disrupts the correlation between T6P and sucrose/hexose pools and affects sucrose non-fermenting-related protein kinase 1 (SnRK1) target gene expression
We identified 14, 11, and one genes predicted to encode for TPS, TPP, and TRE maize enzymes, respectively from maize genome databases

Summary

Introduction

A central feature of plant metabolism is the photosynthetic conversion of light energy into stored chemical energy. As light energy wanes at dusk and throughout the night, the plant transitions from a net producer of sugars to a net consumer. The plant utilizes stored carbohydrates as a source of carbon skeletons and chemical energy (Baena-González et al, 2007; Stitt and Zeeman, 2012). Like Arabidopsis, the vast majority of the stored carbohydrate is in the form of starch (Gibon et al, 2009; Sulpice et al, 2010, 2014), but in other plants, sugars including hexoses and sucrose can play a role in maintaining energy balance throughout the transition between light and dark. Trehalose [α-d-glucopyranosyl-(1→1)-α-d-glucopyranoside] is an important osmotic protectant in bacteria, fungi, and insects where it accumulates to high concentrations

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