Lipidomic profiling of Arabidopsis chloroplast protein phosphatase SLP1 mutants reveals altered diurnal lipid remodeling

TL;DR

This study shows that a chloroplast protein called SLP1 controls lipid changes in plants during day and night cycles.

Contribution

The study reveals that SLP1 regulates lipid metabolism in chloroplasts and affects lipids in other cell parts.

Findings

SLP1 influences chloroplast lipid metabolism and affects lipids in other cellular compartments.

SLP1 knockout and overexpression impact distinct glycerolipid pathways.

Oxidized lipid levels show dramatic diurnal changes in Arabidopsis.

Abstract

•Reversible protein phosphorylation is a key regulatory mechanism controlling most aspects of cell biology.•Arabidopsis thaliana possesses a dynamic lipidome that undergoes significant changes between light and dark conditions.•Chloroplast Shewanella-like protein phosphatase 1 (SLP1) plays a crucial role in regulating the metabolism of the chloroplast and its associated lipidome.•Alterations due to loss or over-expression of SLP1 in the chloroplast are transmitted to other cellular compartments, leading to altered lipids throughout the cell.

Reversible protein phosphorylation is a key regulatory mechanism controlling most aspects of cell biology.

Arabidopsis thaliana possesses a dynamic lipidome that undergoes significant changes between light and dark conditions.

Chloroplast Shewanella-like protein phosphatase 1 (SLP1) plays a crucial role in regulating the metabolism of the chloroplast and its associated lipidome.

Alterations due to loss or over-expression of SLP1 in the chloroplast are transmitted to other cellular compartments, leading to altered lipids throughout the cell.

Lipids are fundamental to the biology of all organisms, including the functioning of subcellular organelles. The plant chloroplast is the site of photosynthesis and serves as a hub of metabolic events that are dynamically regulated between the light and dark periods. The regulation of chloroplast events, like most other biological processes, is often controlled by protein phosphorylation. Here, we explored the lipidome of Arabidopsis thaliana under both light and dark conditions, examining lipid changes upon overexpression or knockout of the chloroplast-specific phosphatase Shewanella-like protein phosphatase 1 (SLP1). To date, no substrates have been identified for the phosphatase SLP1. Results indicate that Arabidopsis thaliana possesses a dynamic lipidome that undergoes significant changes between light and dark conditions, and that protein phosphorylation, in part controlled by SLP1, plays a crucial role in regulating chloroplast metabolism and its associated lipidome. Alterations due to loss or over-expression of SLP1 in the chloroplast are transmitted to other cellular compartments, leading to altered lipids throughout the cell. We report that although both SLP1 mutant lines display perturbed glycerolipid metabolism, knockout and overexpression affect distinct pathways. In the three Arabidopsis lines studied, we also identify dramatic diurnal changes in the abundance of oxidized lipids. Together, these findings establish SLP1-dependent dephosphorylation as an upstream regulator of diel lipid remodelling, linking chloroplast activity to broader cellular lipid organization.

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