Chloroplast translational regulation uncovers nonessential photosynthesis genes as key players in plant cold acclimation

Abstract

Plants evolved efficient multifaceted acclimation strategies to cope with low temperatures. Chloroplasts respond to temperature stimuli and participate in temperature sensing and acclimation. However, very little is known about the involvement of chloroplast genes and their expression in plant chilling tolerance. Here we systematically investigated cold acclimation in tobacco seedlings over two days of exposure to low temperatures by examining responses in chloroplast genome copy number, transcript accumulation and translation, photosynthesis, cell physiology and metabolism. Our time-resolved genome-wide investigation of chloroplast gene expression revealed substantial cold-induced translational regulation at both the initiation and elongation levels, in the virtual absence of changes at the transcript level. These cold-triggered dynamics in chloroplast translation are widely distinct from previously described high light-induced effects. Analysis of the gene set responding significantly to the cold stimulus suggested nonessential plastid-encoded subunits of photosynthetic protein complexes as novel players in plant cold acclimation. Functional characterization of one of these cold-responsive chloroplast genes by reverse genetics demonstrated that the encoded protein, the small cytochrome b6f complex subunit PetL, crucially contributes to photosynthetic cold acclimation. Together, our results uncover an important, previously underappreciated role of chloroplast translational regulation in plant cold acclimation.

Comparative analysis of physiological variations and genetic architecture for cold stress response in soybean germplasm

“…Cold stress signaling above freezing temperature triggered various physiological processes to ameliorate the deleterious effects on plant cellular organs, referred to as cold or chilling acclimation. Among the immediate physiological response, cold stress reduced the chlorophyll fluorescence trait (maximum quantum efficiency of PSII) (Fv/Fm) in the dark-adapted state and impaired the photosynthesis process (Gao et al, 2022). Similarly, we observed a significant reduction in Fv/Fm under cold stress conditions from 0.105 to 0.790 compared to control conditions from 0.719 to 0.883 (Figure 1B).…”

“…Similarly, cold or freezing tolerant poplar maintained higher qL and Fv/Fm by protecting the photosystem (He et al, 2019). In previous studies, comparative RNA-seq analysis showed upregulation of several photosynthetic genes in response to cold in tobacco and M. × giganteus (Spence et al, 2014;Gao et al, 2022). The chloroplast is the primary biosynthesis place of defense-related hormones (Bwalya et al, 2022); therefore, we determined whether photosynthesis genes are involved in cold defense in soybean.…”

“…Similarly, in a previous study, in response to freezing stress, transgenic Populus euphratica overexpressing PeSTZ1 maintained higher photosynthetic activity (Fv/Fm) by dissipating more excessive light energy which imparts them higher freezing tolerance compared with wild type (He et al, 2019). These results indicate that the maximum quantum efficiency of PSII in the dark-adapted state (Fv/Fm) could be an essential parameter for screening the cold tolerant germplasm (Gao et al, 2022). Different studies reported that cold stress led to cold injury to plants' organs, including leaves which were directly facing the environmental anomalies and exhibited the cold effects directly.…”

“…Due to unexpected weather conditions, cold stress at the seedling stage caused irreplaceable production loss of soybean in prominent growing areas (Cheng et al, 2010). Generally, in plants, cold stress results in low germination rates, growth retardation, tissue injures, physiological changes, such as antioxidant metabolism activation and metabolic perturbation, and reduced photosynthetic efficiency (Mehrotra et al, 2020;Gao et al, 2022).…”

Chloroplast proteostasis: A story of birth, life, and death

“…Chloroplast protein synthesis undergoes fast and global reorganization during heat acclimation in the green alga Chlamydomonas and the seed plant tobacco ( Trösch et al., 2022 ). Recently, translational regulation of chloroplasts was shown to play an important role in plant responses to chilling stress ( Gao et al., 2022 ). Mutations in chloroplast translation initiation factor FUG1 ( IF2 ) and ribosomal proteins reduce chilling tolerance in Arabidopsis and tobacco ( Rogalski et al., 2008 ; Marino et al., 2019 ).…”