Impaired chloroplast positioning affects photosynthetic capacity and regulation of the central carbohydrate metabolism d

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ORIGINAL ARTICLE

Impaired chloroplast positioning affects photosynthetic capacity and regulation of the central carbohydrate metabolism during cold acclimation Anastasia Kitashova1   · Katja Schneider2 · Lisa Fürtauer1   · Laura Schröder1 · Tim Scheibenbogen1   · Siegfried Fürtauer1,3   · Thomas Nägele1  Received: 8 May 2020 / Accepted: 6 November 2020 / Published online: 19 November 2020 © The Author(s) 2020

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 C ­ O2 assimilation in chup1 is rather limited by biochemistry than by photochemistry. Further, coldinduced 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  Cold acclimation · Chloroplast positioning · Photosynthesis · Arabidopsis thaliana · Carbohydrate metabolism · Hexose phosphates · Hexokinase · Kinetic modelling

Introduction Tight regulation and balance of photosynthetic primary and secondary reactions are a prerequisite for efficient ­CO2 fixation, biomass accumulation and stress tolerance of higher plants. Particularly under changing environmental Electronic supplementary material  The online version of this article (https​://doi.org/10.1007/s1112​0-020-00795​-y) contains supplementary material, which is available to authorized users. * Thomas Nägele [email protected] 1



Department Biology I, Plant Evolutionary Cell Biology, LMU München, 82152 Planegg‑Martinsried, Germany

2



Department Biology I, Plant Development, LMU München, 82152 Planegg‑Martinsried, Germany

3

Fraunhofer Institute for Process Engineering and Packaging IVV, 85354 Freising, Germany



conditions, stabilization of this balance is essential for prevention of tissue damage due to cytotoxic accumulation of reactive oxygen species (ROS). Intracellular distribution of chloroplasts changes in response to changing light intensity. Chloroplast movement plays an important role in protecti