Chloroplast translation in Marchantia and its regulation by light

Barkan lab, University of Oregon.Translation of the chloroplast psbA mRNA in angiosperms is dynamically regulated by light. psbA translation initiation is triggered by the light-induced damage of its gene product, the D1 reaction center protein of photosystem II (PSII). This regulatory circuit tunes the rate of D1 synthesis to D1 photodamage, providing nascent D1 as needed for PSII repair. Several proteins that have been implicated in chlorophyll/D1 transactions during PSII assembly and repair are involved in this regulation. To address whether the light-induced chlorophyll synthesis that is characteristic of angiosperms is relevant to the regulatory mechanism, we examined the effects of light-dark shifts on chloroplast mRNA ribosome occupancies in the liverwort Marchantia polymorpha, which synthesizes chlorophyll in both the dark and the light. As in angiosperms, ribosome occupancy on psbA mRNA decreased rapidly upon shifting plants to the dark, was rapidly restored upon a transfer back to the light, and ribosome occupancy on other chloroplast mRNAs did not change substantively during this light shift regime. This behavior was similar in a Marchantia mutant defective in the chloroplast chlB gene, required for the synthesis of chlorophyll in the dark. These findings show that patterns of light-regulated chloroplast translation are conserved among vascular and non-vascular plants, and suggest that light-induced chlorophyll synthesis is not relevant to light-regulated psbA translation. Additionally, our data support synthetic biology approaches in Marchantia by providing a plastome-wide view of translational efficiency and translational output.

俄勒冈大学巴坎实验室。被子植物中叶绿体psbA mRNA的翻译过程受光的动态调控。psbA的翻译起始由其基因产物——光系统II（PSII）的D1反应中心蛋白——的光诱导损伤所触发。该调控环路可将D1的合成速率与D1的光损伤程度相匹配，为光系统II的修复过程按需提供新生D1蛋白。多项在光系统II组装与修复过程中参与叶绿素/D1互作的蛋白，也参与了该调控过程。
为探究作为被子植物典型特征的光诱导叶绿素合成是否与该调控机制相关，本研究以地钱（Marchantia polymorpha）为对象，检测了光暗转换对其叶绿体mRNA核糖体占用率的影响；地钱可在黑暗与光照条件下均合成叶绿素。
与被子植物的情况一致，将地钱转移至黑暗环境后，psbA mRNA上的核糖体占用率迅速下降；重新转移至光照环境后，该占用率又快速恢复；而在此光暗转换处理过程中，其他叶绿体mRNA的核糖体占用率未发生显著变化。
对于叶绿体chlB基因缺陷的地钱突变体而言，该现象同样存在——chlB基因是黑暗条件下叶绿素合成所必需的。
上述研究结果表明，光调控的叶绿体翻译模式在维管植物与非维管植物中均保守存在，同时提示光诱导叶绿素合成与光调控的psbA翻译过程并无关联。
此外，本研究通过提供全质体组范围的翻译效率与翻译产出数据，为地钱的合成生物学研究提供了支持。