Impaired chloroplast positioning affects photosynthetic capacity and regulation of the central carbohydrate metabolism during cold acclimation

Photosynth Res. 2021 Jan;147(1):49-60. doi: 10.1007/s11120-020-00795-y. Epub 2020 Nov 19.

Abstract

Photosynthesis and carbohydrate metabolism of higher plants need to be tightly regulated to prevent tissue damage during environmental changes. The intracellular position of chloroplasts changes due to a changing light regime. Chloroplast avoidance and accumulation response under high and low light, respectively, are well known phenomena, and deficiency of chloroplast movement has been shown to result in photodamage and reduced biomass accumulation. Yet, effects of chloroplast positioning on underlying metabolic regulation are less well understood. Here, we analysed photosynthesis together with metabolites and enzyme activities of the central carbohydrate metabolism during cold acclimation of the chloroplast unusual positioning 1 (chup1) mutant of Arabidopsis thaliana. We compared cold acclimation under ambient and low light and found that maximum quantum yield of PSII was significantly lower in chup1 than in Col-0 under both conditions. Our findings indicated that net CO2 assimilation in chup1 is rather limited by biochemistry than by photochemistry. Further, cold-induced dynamics of sucrose phosphate synthase differed significantly between both genotypes. Together with a reduced rate of sucrose cycling derived from kinetic model simulations our study provides evidence for a central role of chloroplast positioning for photosynthetic and metabolic acclimation to low temperature.

Keywords: Arabidopsis thaliana; Carbohydrate metabolism; Chloroplast positioning; Cold acclimation; Hexokinase; Hexose phosphates; Kinetic modelling; Photosynthesis.

MeSH terms

  • Arabidopsis / genetics
  • Arabidopsis / physiology*
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism*
  • Carbohydrate Metabolism*
  • Chloroplast Proteins / genetics
  • Chloroplast Proteins / metabolism*
  • Cold Temperature
  • Gene Expression Regulation, Plant*
  • Microfilament Proteins / genetics
  • Microfilament Proteins / metabolism*
  • Mutation
  • Oxygen / metabolism
  • Photosynthesis* / physiology
  • Plant Leaves / physiology
  • Plant Leaves / radiation effects
  • Sucrose / metabolism*

Substances

  • Arabidopsis Proteins
  • Chloroplast Proteins
  • Microfilament Proteins
  • chloroplast unusual positioning1 protein, Arabidopsis
  • Sucrose
  • Oxygen