STCH4/REIL2 Confers Cold Stress Tolerance in Arabidopsis by Promoting rRNA Processing and CBF Protein Translation

Abstract

Graphical Abstract Highlights d STCH4 maintains rRNA processing under low temperatures d STCH4 promotes CBF translation under low temperatures d Overexpression of STCH4 enhances cold stress tolerance d STCH4 may be required for ribosome remodeling under low temperatures SUMMARYPlants respond to cold stress by inducing the expression of transcription factors that regulate downstream genes to confer tolerance to freezing. We screened an Arabidopsis transfer DNA (T-DNA) insertion library and identified a cold-hypersensitive mutant, which we named stch4 (sensitive to chilling 4). STCH4/ REIL2 encodes a ribosomal biogenesis factor that is upregulated upon cold stress. Overexpression of STCH4 confers chilling and freezing tolerance in Arabidopsis. The stch4 mutation reduces CBF protein levels and thus delayed the induction of C-repeatbinding factor (CBF) regulon genes. Ribosomal RNA processing is reduced in stch4 mutants, especially under cold stress. STCH4 associates with multiple ribosomal proteins, and these interactions are modulated by cold stress. These results suggest that the ribosome is a regulatory node for cold stress responses and that STCH4 promotes an altered ribosomal composition and functions in low temperatures to facilitate the translation of proteins important for plant growth and survival under cold stress.

Arabidopsis REI-LIKE proteins activate ribosome biogenesis during cold acclimation

“…at 4°C or at 10°C, but not for growth at optimized 20°C temperature (Schmidt et al, 2013; Beine-Golovchuk et al, 2018). In agreement with these findings, identical T-DNA insertion mutants of reil2 were recently discovered in a screen for chilling sensitive Arabidopsis mutants (Yu et al 2020), namely reil2.1/ stch4-2 (GK_166C10) and reil2.2/ stch4-1 (SALK_040068). The reil1-1 reil2-1 double mutant has a more severe cold phenotype and all but stops development after germination at 10°C prior to the emergence of the first rosette leaf (Schmidt et al, 2013; Beine-Golovchuk et al, 2018).…”

“…Conserved functions of the Arabidopsis REIL proteins and new functions that evolved on the path towards multicellular embryophyte plants became apparent (Beine-Golovchuk et al, 2018). As was expected in analogy to yeast, FP-REIL1 and FP-REIL2 fusion proteins localize to the cytosol (Beine-Golovchuk et al, 2018; Yu et al, 2020) and the REIL1 protein appears to interact with ribosome complexes containing the 60S large ribosome subunit (LSU). Based on immunoprecipitation-mass spectrometry, REIL2 associates with the eukaryotic ribosome (Yu et al, 2020).…”

“…As was expected in analogy to yeast, FP-REIL1 and FP-REIL2 fusion proteins localize to the cytosol (Beine-Golovchuk et al, 2018; Yu et al, 2020) and the REIL1 protein appears to interact with ribosome complexes containing the 60S large ribosome subunit (LSU). Based on immunoprecipitation-mass spectrometry, REIL2 associates with the eukaryotic ribosome (Yu et al, 2020). Our current study locates REIL2 to the non-translating 60S fraction of Col-0 wild type.…”

“…Expression of amino-terminal FLUORESCENT PROTEIN (FP)-REIL fusion proteins driven by the UBIQUITIN10 promoter rescue the mutant phenotypes (Beine-Golovchuk et al, 2018). The two allelic reil2-1 and reil2-2 mutants are both growth retarded and form small spoon-shaped leaves at 10°C (Schmidt et al, 2013; Yu et al, 2020). This phenomenon reverted after shift from cold to optimal 20°C.…”

“…Ectopic overexpression of REIL2 under control of the 35S promoter conveyed enhanced chilling and freezing tolerance under mixotrophic in vitro conditions, i.e. in the presence half-strength Murashige and Skoog (MS) medium (Yu et al, 2020).…”