The Chloroplast RNA binding protein CP31A shows cold-dependent RNA association and mediates cold-resistance via its acidic domain

Chloroplast gene expression is characterized by a multitude of post-transcriptional events as well as long-lived mRNAs. Given that the chloroplast is responsible for expressing core components of the photosynthetic apparatus, it is not surprising that the accumulation and processing of chloroplast RNA is heavily affected by various external and internal cues, including light and temperature changes. A multitude of nuclear-encoded RNA-binding proteins (RBPs) are known to be required for chloroplast RNA metabolism, but we do not yet know how chloroplast RBPs convert abiotic signals into gene expression changes. Previous studies showed that chloroplast ribonucleoprotein 31A (CP31A) is required for the stabilization of multiple chloroplast mRNAs in the cold, and that the phosphorylation of CP31A at various residues within its N-terminal acidic domain (AD) can alter its affinity for RNA in vitro. Here, we demonstrate that CP31A shows increased affinity for a large number of chloroplast RNAs in vivo. Loss of CP31A leads to cold sensitivity, and cold-dependent RNA binding and cold resistance both depend on the AD of CP31A. Together, our analysis establishes the AD of CP31A as a key mediator of cold acclimation of the chloroplast transcriptome.