AtHSP90.5 and AtFtsH12 synergistically regulate the accumulation of photosynthesis protein complexes and chloroplast development in Arabidopsis.

The 90-kDa heat shock protein (HSP90) is a central component of the chaperone system for protein homeostasis (proteostasis). In Arabidopsis, AtHSP90.5 is the sole chloroplast-localized HSP90 family member, yet its role in chloroplast proteostasis remains poorly characterized. Here, we identify and characterize the pale green arabidopsis 5 mutant, pga5-1, which exhibits defective chloroplast development and impaired accumulation of photosynthetic protein complexes. Genetic analysis revealed that pga5-1 is a hypomorphic allele of AtHSP90.5, harboring a missense mutation (G646E) localized closely to the substrate-binding site. Biochemical studies demonstrated that AtHSP90.5 interacts with AtFtsH12, and the ATPase activity of AtHSP90.5 is essential for the oligomerization of AtFtsH12 complexes. Strikingly, the mutation of the conserved residue (E106A) for the ATPase activity of AtHSP90.5 can rescue the embryonic lethality of AtHSP90.5 null mutants, yielding albino seedlings with non-photosynthetic plastids, and partially complement pga5-1. Furthermore, we show that AtHSP90.5 associates with subunits of light-harvesting antenna complexes, including LhcB1, LhcB2, and LhcA1, and is epistatic to PGA4/cpSRP54 in regulating the accumulation of a chimeric chloroplast marker protein, LhcB2-GFP. Collectively, our findings establish a critical role for AtHSP90.5 in maintaining photosynthesis protein complexes and uncover a previously unknown functional link between AtHSP90.5 and AtFtsH12 in chloroplast protein translocation.