The interplay of post-translational protein modifications in Arabidopsis leaves during photosynthesis induction

Diurnal dark to light transition causes profound physiological changes in plant metabolism. These changes require distinct modes of regulation as a unique feature of photosynthetic lifestyle. The activities of several key metabolic enzymes are regulated by light-dependent post-translational modifications (PTM) and have been studied at depth at the level of individual proteins. In contrast, a global picture of the light-dependent PTMome dynamics is lacking, leaving the response of a large proportion of cellular function undefined. Here, we investigated the light-dependent metabolome and proteome changes in Arabidopsis rosettes in a time resolved manner to dissect their kinetic interplay, focusing on phosphorylation, lysine acetylation, and cysteine-based redox switches. Of over 24 000 PTM sites that were detected, more than 1700 were changed during the transition from dark to light. While the first changes, as measured 5 min after onset of illumination, occurred mainly in the chloroplasts, PTM changes at proteins in other compartments coincided with the full activation of the Calvin-Benson cycle and the synthesis of sugars at later timepoints. Our data reveal connections between metabolism and PTM-based regulation throughout the cell. The comprehensive multiome profiling analysis provides unique insight into the extent by which photosynthesis reprograms global cell function and adds a powerful resource for the dissection of diverse cellular processes in the context of photosynthetic function.

Automated summary

The transition from dark to light in the diurnal cycle causes significant physiological changes in plant metabolism, which require specific modes of regulation. While the activities of key metabolic enzymes regulated by light-dependent post-translational modifications (PTMs) have been extensively studied at the protein level, a comprehensive understanding of the global dynamics of light-dependent PTMs is lacking. In this study, we investigated the changes in the metabolome and proteome in Arabidopsis rosettes in response to light in a time-dependent manner, focusing on phosphorylation, lysine acetylation, and cysteine-based redox switches. Our findings revealed that over 1700 out of more than 24,000 detected PTM sites were altered during the transition from dark to light, with different compartments showing distinct PTM changes at different timepoints.