A histone demethylase is involved in regulating the transcription factor PSR1 for carbon storage in Chlamydomonas

Abstract

Histone modifications are widespread in microalgae, a group of photoautotrophs capable of transforming CO₂ to diverse bio-products. However, the functional roles of histone modifying enzymes for carbon metabolism remain largely unexplored. Here, we unveiled the involvement of a JmjC domain-containing histone demethylase (CrHDM1), a previously uncharacterized epigenetic regulator, in carbon metabolism by modulating a transcription factor in the model alga Chlamydomonas reinhardtii (thereafter Chlamydomonas). CrHDM1 disruption resulted in increased carbohydrate levels including starch yet attenuated protein and lipid levels in Chlamydomonas, which were restored by genetic complementation with the CrHDM1 gene. Phosphorus Responsive Regulator1 (PSR1), a transcription factor involved in starch storage regulation, was transcriptionally upregulated by CrHDM1 disruption, along with the upregulation of starch synthesis genes. PSR1 knockout in the crhdm1 mutant impaired the CrHDM1 disruption-associated starch increase. CrHDM1, localized in the nucleus, was demonstrated to specifically demethylate H3K4me2 in vitro. Besides, chromatin immunoprecipitation-quantitative PCR experiments showed that the H3K4me2 level at the PSR1 promoter, which positively correlated with PSR1 transcript level, was negatively regulated by CrHDM1. Collectively, our findings uncover a newly discovered epigenetic regulator–transcription factor module involved in starch storage and provide valuable insights into the epigenetic regulation of carbon metabolism in Chlamydomonas.