Function of chloroplast located sugars and the plastid envelope in acclimation to cold temperatures

Plants are permanently exposed to an immensely altering environment, including changes in ambient temperature and light intensities. Within their cells, chloroplasts sense these environmental changes and represent a central hub to coordinate cellular responses. Cold acclimation represents a complex physiological and biochemical process to guarantee vitality at lowered temperatures and to gain freezing tolerance. Since decades it is known that during cold acclimation neutral sugars, like e.g. glucose, fructose, sucrose and raffinose accumulate in the chloroplast stroma and serve as protective solutes. However, neither the exact cellular sources for these sugars, nor the chloroplastic transporters involved in sugar import and export have been identified on the molecular level.

We gained further evidence that chloroplast located sugars are involved in cold acclimation, identified a novel chloroplast located sugar transporter (named pSuT) with impact on frost tolerance and showed that stromal sugar homeostasis affects chloroplast/nucleus signal exchange. With help of an envelope proteome analysis we identified several proteins exhibiting a severely increased (e.g. the Nucleotide Transporter NTT2) or dramatically decreased abund­ance (e.g. Maltose Exporter 1 MEX1). These proteins represent novel acclimation modulators. Furthermore, we discovered a so far unknown mode of cold acclimation: some soluble proteins show a differential localization (diffloc) at the envelope membrane (either attached or released from it).

Figure: Chloroplast transporter with a role in cold-acclimation. The plastidic sugar porter pSUT exports sucrose out of the stroma during cold acclimation and affects frost tolerance as well as induction of flowering. Shortly after onset of cold temperature, the abundance of the plastidic ATP importer NTT increases while the level of the maltose exporter protein MEX1 decreases. Several soluble proteins exhibit a reversible and dynamic envelope location during warm/cold transition, named diffloc, which represents a novel type of regulation to achieve a maximal frost tolerance. Created with

Selected Publications

Pommerrenig B, Ludewig F, Cvetkovic J, Trentmann O, Klemens PAW, Neuhaus HE (2018) In concert: orchestrated changes in carbohydrate homeostasis are critical for plant abiotic stress tolerance. Plant Cell Physiol. 59, 1290-1299 doi: 10.1093/pcp/pcy037 

Patzke K, Prananingrum P, Klemens PAW, Trentmann O, Martins Rodrigues C, Keller I, Fernie AR, Geigenberger P, Bölter B, Lehmann M, Schmitz-Esser C, Pommerrenig B, Haferkamp I, Neuhaus HE (2019) The plastidic sugar transporter pSuT influences flowering and affects cold responses. Plant Physiol. 179, 569-587 doi: 10.1104/pp.18.01036

Trentmann O, Mühlhaus T, Zimmer D, Sommer FK, Schroda M, Haferkamp I, Keller I, Pommerrenig B, Neuhaus HE (2020) Identification of chloroplast envelope proteins with critical importance for cold acclimation of Arabidopsis. Plant Physiol. 182, 1239-1255 doi: 10.1104/pp.19.0094