Limited Responsiveness of Chloroplast Gene Expression during Acclimation to High Light in Tobacco

Abstract

Acclimation to changing light intensities poses major challenges to plant metabolism and has been shown to involve regulatory adjustments in chloroplast gene expression. However, this regulation has not been examined at a plastid genome-wide level and for many genes, it is unknown whether their expression responds to altered light intensities. Here, we applied comparative ribosome profiling and transcriptomic experiments to analyze changes in chloroplast transcript accumulation and translation in leaves of tobacco (Nicotiana tabacum) seedlings after transfer from moderate light to physiological high light. Our time-course data revealed almost unaltered chloroplast transcript levels and only mild changes in ribosome occupancy during 2 d of high light exposure. Ribosome occupancy on the psbA mRNA (encoding the D1 reaction center protein of PSII) increased and that on the petG transcript decreased slightly after high light treatment. Transfer from moderate light to high light did not induce substantial alterations in ribosome pausing. Transfer experiments from low light to high light conditions resulted in strong PSII photoinhibition and revealed the distinct light-induced activation of psbA translation, which was further confirmed by reciprocal shift experiments. In low-light-to-highlight shift experiments, as well as reciprocal treatments, the expression of all other chloroplast genes remained virtually unaltered. Altogether, our data suggest that low light-acclimated plants upregulate the translation of a single chloroplast gene, psbA, during acclimation to high light. Our results indicate that psbA translation activation occurs already at moderate light intensities. Possible reasons for the otherwise mild effects of light intensity changes on gene expression in differentiated chloroplasts are discussed.

Secondary Structure of Chloroplast mRNAs In Vivo and In Vitro

“…In the low light conditions analyzed (see Section 4.1. ), psbA translation efficiency is expected to be low [34]. According to the annotation, psbC possesses a start codon with a very weak SD, and translation would be expected to depend on mRNA secondary structure.…”

Adapting to High Light: At a Different Time and Place?

“…The work of Schuster et al (2020) supports a model in which, even though the photosynthesis apparatus is able to rapidly adjust to high lightinduced damage, the chloroplast transcription machinery is less quick to respond. The earliest stress seems to be resolved by posttranslational and physiological processes and the hard work of the nucleus, while chloroplast genes are only called upon if the stressful situation becomes the new standard.…”

“…The work of Schuster et al (2020) published in this issue of Plant Physiology, aimed to understand to what extend tobacco (Nicotiana tabacum) seedlings alter transcription and translation of chloroplast genes during rapid adaptation to high light. As chloroplasts have an endosymbiotic origin, they have their own DNA and protein synthesis machinery.…”

“…However, it remained unknown how physiologically relevant elevations of light intensity regulate genome-wide changes in chloroplast translation. Schuster et al (2020) used tobacco plants with fully operational chloroplasts and exposed them to an ;3-fold (350-1,000 mmol m 22 s 21 ) or 20-fold (50-1,000 mmol m 22 s 21 ) increase in light intensity. Already after 2 h of high light, the decreased Fv/Fm ratio indicated photoinhibition of PSII, and after longer exposure (2 d), chlorophyll content slightly dropped.…”

The Dynamic Kaleidoscope of RNA Biology in Plants

“…The first describes a single plastid gene that requires a specific member of the mitochondria-type transcription terminator factor gene family for proper transcription termination in Arabidopsis (Xiong et al, 2020). The second article examines chloroplast transcript levels and their association with ribosomes in tobacco (Nicotiana tabacum) in response to high light (Schuster et al, 2020). These authors show that psbA, encoding the highly labile D1 reaction center protein of PSII, is the principal plastid transcript that is translationally up-regulated.…”