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

J Exp Bot. 2014 Nov;65(20):5959-73. doi: 10.1093/jxb/eru335. Epub 2014 Sep 30.

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.

Keywords: Maize; diurnal cycle,; quantitative RT-PCR.; shade stress,; trehalose gene family; trehalose-6-phosphate.

MeSH terms

  • Carbohydrate Metabolism
  • Circadian Rhythm
  • Darkness
  • Gene Expression Regulation, Plant*
  • Glucosyltransferases / genetics
  • Glucosyltransferases / metabolism
  • Multigene Family
  • Phosphoric Monoester Hydrolases / genetics
  • Phosphoric Monoester Hydrolases / metabolism
  • Plant Proteins / genetics*
  • Plant Proteins / metabolism
  • Plants, Genetically Modified
  • Protein Serine-Threonine Kinases
  • Seedlings / genetics
  • Seedlings / physiology
  • Seedlings / radiation effects
  • Starch / metabolism
  • Sucrose / metabolism
  • Sugar Phosphates / metabolism
  • Trehalose / analogs & derivatives
  • Trehalose / metabolism
  • Zea mays / genetics
  • Zea mays / physiology*
  • Zea mays / radiation effects

Substances

  • Plant Proteins
  • Sugar Phosphates
  • trehalose-6-phosphate
  • Sucrose
  • Starch
  • Trehalose
  • Glucosyltransferases
  • trehalose-6-phosphate synthase
  • SNF1-related protein kinases
  • Protein Serine-Threonine Kinases
  • trehalose-phosphatase
  • Phosphoric Monoester Hydrolases