Light-inducedpsbAtranslation in plants is triggered by photosystem II damage via an assembly-linked autoregulatory circuit

Abstract

The D1 reaction center protein of Photosystem II (PSII) is subject to light-induced damage.Degradation of damaged D1 and its replacement by nascent D1 are at the heart of a PSII repair cycle, without which photosynthesis is inhibited. In mature plant chloroplasts, light stimulates the recruitment of ribosomes specifically to psbA mRNA to provide nascent D1 for PSII repair, and also triggers a global increase in translation elongation rate. The light-induced signals that initiate these responses are unclear. We present action spectrum and genetic data indicating that the light-induced recruitment of ribosomes to psbA mRNA is triggered by D1 photodamage, whereas the global stimulation of translation elongation is triggered by photosynthetic electron transport. Furthermore, mutants lacking HCF136, which mediates an early step in D1 assembly, exhibit constitutively high psbA ribosome occupancy in the dark, and differ in this way from mutants lacking PSII for other reasons. These results, together with the recent elucidation of a thylakoid membrane complex that functions in PSII assembly, PSII repair and psbA translation, suggest an autoregulatory mechanism in which the light-induced degradation of D1 relieves repressive interactions between D1 and translational activators in the complex. We suggest that the presence of D1 in this complex coordinates D1 synthesis with the need for nascent D1 during both PSII biogenesis and PSII repair in plant chloroplasts. Significance StatementPhotosystem II (PSII) harbors the water-splitting activity underlying oxygenic photosynthesis.The PSII reaction center protein D1 is subject to photodamage and must be replaced with nascent D1 to maintain photosynthetic activity. How new D1 synthesis is coordinated with D1 damage has been a long-standing question. Our results clarify the nature of the light-induced signal that activates D1 synthesis for PSII repair in plants, and suggest an autoregulatory mechanism in which degradation of damaged D1 relieves a repressive interaction between D1 and translational activators in a complex that functions in PSII assembly and repair. This proposed mechanism comprises a responsive switch that couples D1 synthesis to need for D1 during PSII biogenesis and repair.

Ribosome profiling elucidates differential gene expression in bundle sheath and mesophyll cells in maize

“…Ribo-seq and RNA-seq data were processed as described previously (Chotewutmontri and Barkan, 2020) with minor modifications. In brief, adapter sequences were trimmed using cutadapt (Martin, 2011).…”

The state of oligomerization of Rubisco controls the rate of LSU translation inChlamydomonas reinhardtii

“…The presence of a D1-HCF244-OHP1/2 assembly intermediate was linked to the inhibition of D1 synthesis in the dark, relieved in the photorepair process. This assembly intermediate has been suggested to act as a repressor complex which may physically interact with D1 HCF73 translational activator to mediate D1 repression in the dark (Chotewutmontri and Barkan, 2020).…”

“…Cytochrome b 6 f and ATP-synthase, undergo translation regulatory processes, known as CES processes, sensing their assembly state in C. reinhardtii chloroplasts (Kuras and Wollman, 1994;Choquet et al, 1998;Wostrikoff et al, 2004;Minai et al, 2006;Drapier et al, 2007) as well as in higher plant chloroplasts (Levey et al, 2014;Chotewutmontri and Barkan, 2020): the rate of translation of a subset of chloroplast-encoded subunits was shown to depend on the presence of their assembly partners. Accordingly, earlier observations of Chlamydomonas RBCS knockout mutants showed that LSU synthesis is strongly decreased (Khrebtukova and Spreitzer, 1996).…”