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The D1 subunit of photosystem II (PSII) is subject to light-induced damage. In plants, D1 photodamage activates translation of chloroplastpsbAmRNA encoding D1, providing D1 for PSII repair. Three D1 assembly factors have been implicated in the regulatory mechanism: HCF244 and RBD1 activatepsbAtranslation, whereas HCF136 repressespsbAtranslation in the dark. To clarify the regulatory circuit, we analyzedpsbAribosome occupancy in dark-adapted and illuminatedrbd1andrbd1;hcf136double mutants in Arabidopsis and in Zm-hcf244and Zm-hcf244;Zm-hcf136double mutants in maize. The results show that RBD1 is required for light-inducedpsbAtranslation but has only a small effect onpsbAribosome occupancy in the dark. RBD1 is not required forpsbAtranslation when HCF136 is absent, indicating that RBD1 activatespsbAtranslation in the light by inhibiting HCF136’s repressive effect. By contrast, HCF244 is required to recruit ribosomes topsbAmRNA in light, dark, and in the absence of HCF136. We demonstrate further that HCF244 is not required for the translational activator HCF173 to bind thepsbA5’UTR. These results show that RBD1 is central to the perception of the D1 photodamage that triggers D1 synthesis and that it activatespsbAtranslation by relieving repression by an HCF136-dependent assembly intermediate. HCF244 activates downstream of those events without impacting HCF173’s binding topsbAmRNA. The results implicate a feature of nascent D1 that is affected by both HCF136 and RBD1 as the signal that reports D1 photodamage to regulatepsbAtranslation rate as needed for PSII repair.
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This content will become publicly available on September 1, 2026
Effects of light on chloroplast translation in Marchantia polymorpha are similar to those in angiosperms and are not influenced by light‐independent chlorophyll synthesis
SUMMARY Translation of the chloroplastpsbAmRNA in angiosperms is activated by photodamage of its gene product, the D1 subunit of photosystem II (PSII), providing nascent D1 for PSII repair. The involvement of chlorophyll in the regulatory mechanism has been suggested due to the regulatory roles of proteins proposed to mediate chlorophyll/D1 transactions and the fact that chlorophyll is synthesized only in the light in angiosperms. We used ribosome profiling and RNA‐seq to address whether the effects of light on chloroplast translation are conserved in the liverwort Marchantia (Marchantia polymorpha), which synthesizes chlorophyll in both the dark and the light. As in angiosperms, ribosome occupancy onpsbAmRNA decreased rapidly upon shifting plants to the dark and was rapidly restored upon a transfer back to the light, whereas ribosome occupancy on other chloroplast mRNAs changed very little. The results were similar in aMarchantiamutant unable to synthesize chlorophyll in the dark. Those results, in conjunction with pulse‐labeling data, suggest that light elicits a plastome‐wide activation of translation elongation and a specific increase inpsbAtranslation initiation inMarchantia, as in angiosperms. These findings show that light regulates chloroplast translation similarly in vascular and non‐vascular plants, and that constitutive chlorophyll synthesis does not affect light‐regulatedpsbAtranslation initiation. Additionally, the translational outputs of chloroplast genes are similar inMarchantiaand angiosperms but result from differing contributions of mRNA abundance and translational efficiencies. This adds to the evidence that chloroplast mRNA abundance and translational efficiencies co‐evolve under selection to maintain protein outputs.
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- PAR ID:
- 10651557
- Publisher / Repository:
- Society for Experimental Biology and John Wiley & Sons Ltd.,
- Date Published:
- Journal Name:
- The Plant Journal
- Volume:
- 123
- Issue:
- 5
- ISSN:
- 0960-7412
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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