Opposing action of photosystem II assembly factors RBD1 and HCF136 underlies light-regulatedpsbAtranslation in plant chloroplasts

ABSTRACT The D1 reaction center protein of photosystem II (PSII) is subject to light-induced damage. In plants, D1 photodamage activates translation of the chloroplast psbA mRNA encoding D1, providing D1 for PSII repair. Genetic data have implicated three D1 assembly factors in the regulatory mechanism: HCF244 and RBD1 activate psbA translation whereas HCF136 represses psbA translation in the dark. To clarify the regulatory circuit, we analyzed psbA ribosome occupancy in dark-adapted and illuminated rbd1 and hcf136;rbd1 double mutants in Arabidopsis, and in Zm- hcf244 and Zm- hcf136; Zm- hcf244 double mutants in maize. The results show that RBD1 is required for the light-induced recruitment of ribosomes to psbA mRNA but has little effect on psbA ribosome occupancy in the dark. Furthermore, RBD1 is dispensable for psbA translation when HCF136 is absent, indicating that RBD1 activates psbA translation indirectly, by inhibiting HCF136’s repressive effect. By contrast, HCF244 is required to recruit ribosomes to psbA mRNA in light, dark, and in the absence of HCF136. These results demonstrate that the step in D1 assembly that is mediated by RBD1 is central to the perception of the D1 photodamage that triggers D1 synthesis, that RBD1 activates psbA translation in the light by relieving the repressive effect of an HCF136-dependent assembly intermediate, and that HCF244 acts independently of these events to activate psbA translation. The results implicate a feature of nascent D1 that is affected by both HCF136 and RBD1 as the signal that reports D1 photodamage to regulate psbA translation rate as needed for PSII repair. Significance Statement The D1 subunit of photosystem II (PSII) is damaged by light and must be replaced with nascent D1 to maintain photosynthesis. In plants, D1 photodamage triggers D1 synthesis by activating translation of chloroplast psbA mRNA encoding D1. Our results demonstrate that an antagonistic interplay between two photosystem II assembly factors, HCF136 and RBD1, is at the core of the signal transduction process that senses light-induced D1 damage to regulate psbA translation. These findings implicate a feature of nascent D1 that is affected by both HCF136 and RBD1 as the signal that reports D1 photodamage to tune psbA translation as needed for PSII repair. The results elucidate an assembly-coupled translational rheostat that maintains photosynthesis in the face of PSII photodamage.