Plant Temperature Acclimation and Growth Rely on Cytosolic Ribosome Biogenesis Factor Homologs

Beine-Golovchuk, Olga; Firmino, Alexandre Augusto Pereira; Dąbrowska, Adrianna; Schmidt, Stefanie; Erban, Alexander; Walther, Dirk; Zuther, Ellen; Hincha, Dirk K.; Kopka, Joachim

doi:10.1104/pp.17.01448

Cited by 41 publications

(133 citation statements)

References 90 publications

Supporting

Mentioning

118

Contrasting

Order By: Relevance

“…This phenomenon reverted after shift from cold to optimal 20°C. Except for slightly delayed germination, the reil1-1 mutant, similar to yeast Δreh1 , has no growth phenotype under the tested low temperature conditions (Schmidt et al, 2013; Beine-Golovchuk et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

“…Arabidopsis REIL paralogs are required specifically for plants to grow in the cold, e.g. 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).…”

Section: Introductionmentioning

confidence: 99%

“…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). The double mutation is, however, non-lethal and a valid system for the investigation of REIL functions in plants.…”

Section: Introductionmentioning

confidence: 99%

“…The double mutation is, however, non-lethal and a valid system for the investigation of REIL functions in plants. The double mutant maintains cellular integrity and acquires freezing tolerance after shifts from 20°C to 4°C or 10°C cold (Beine-Golovchuk et al, 2018). Expression of amino-terminal FLUORESCENT PROTEIN (FP)-REIL fusion proteins driven by the UBIQUITIN10 promoter rescue the mutant phenotypes (Beine-Golovchuk et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

“…The double mutant maintains cellular integrity and acquires freezing tolerance after shifts from 20°C to 4°C or 10°C cold (Beine-Golovchuk et al, 2018). 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).…”

Section: Introductionmentioning

confidence: 99%

See 4 more Smart Citations

Arabidopsis REI-LIKE proteins activate ribosome biogenesis during cold acclimation

Cheong

Beine-Golovchuk

Górka

et al. 2020

Preprint

Self Cite

View full text Add to dashboard Cite

29 30 WORD COUNT 31 18,932 32 2 TITLE 33 Arabidopsis REIL proteins activate ribosome biogenesis during cold acclimation 34 Running Title 35 REIL proteins activate ribosome biogenesis 36 Highlight of this study (summarizing sentence) (27 words) 37 REIL proteins affect paralog composition of eukaryotic ribosomes and suppress accumulation of 38 43S-preinitiation and pre-60S-maturation complexes, suggesting functions of ribosome 39 heterogeneity and biogenesis in plant cold acclimation. 40 Abstract (150 words) 41 Arabidopsis REIL proteins are cytosolic ribosomal 60S-biogenesis factors. After shift to 10°C, reil 42 mutants deplete and slowly replenish non-translating eukaryotic ribosome complexes of root 43 tissue, while tightly controlling the balance of non-translating 40S-and 60S-subunits. Reil 44 mutations compensate by hyper-accumulation of non-translating subunits at steady-state 45 temperature; after cold-shift, a KCl-sensitive 80S sub-fraction remains depleted. We infer that 46 Arabidopsis buffers fluctuating translation by pre-existing non-translating ribosomes before de 47 novo synthesis meets temperature-induced demands. Reil1 reil2 double mutants accumulate 43S-48 preinitiation and pre-60S-maturation complexes and have altered paralog composition of 49 ribosomal proteins in non-translating complexes. With few exceptions, e.g. RPL3B and RPL24C, 50 these changes are not under transcriptional control. Our study suggests requirement of de novo 51 synthesis of eukaryotic ribosomes for long-term cold acclimation, feedback control of NUC2 and 52 eIF3C2 transcription and links new proteins, AT1G03250, AT5G60530, to plant ribosome 53 biogenesis. We propose that Arabidopsis requires biosynthesis of specialized ribosomes for cold 54 acclimation. 55 Key words (6-10, in alphabetical order) 56 abiotic stress, Arabidopsis, cold acclimation, proteomics, REI-LIKE proteins, ribosome 57 biogenesis, roots, system analysis, transcriptomics 58 59 60 61The Arabidopsis thaliana Col-0 (Arabidopsis) REI1-LIKE (REIL) proteins, REIL1 62 (At4g31420) and REIL2 (At2g24500) are homologs of the yeast Rei1 (YBR267W) and the paralog 63 Reh1 (YLR387C) proteins. In yeast, both the Rei1 and Reh1 proteins function as ribosome 64 biogenesis factors that participate either in parallel or sequentially in the late ribosome biogenesis 65 step of cytoplasmic 60S ribosomal subunit maturation (Greber et al., 2012; Greber et al., 2016). 66 Aside from this function, these proteins are required to maintain growth at suboptimal or cold 67 temperatures. The ∆rei1 mutant is cold sensitive already at moderately suboptimal temperatures 68 of yeast. The ∆rei1 ∆reh1 double mutant is even more cold sensitive, while the yeast ∆reh1 69 mutation alone has no effect on growth in the cold (Iwase and Toh-e, 2004; Lebreton et al., 2006; 70 Parnell and Bass, 2009). Heterologous expression of Arabidopsis REIL1, but not of REIL2 partly 71 complements the cold sensitivity of the yeast ∆rei1 mutant (Schmidt et al., 2013). The Arabidopsis 72 REIL paralogs differ in st...

show abstract

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Arabidopsis REI-LIKE proteins activate ribosome biogenesis during cold acclimation

Cheong

Beine-Golovchuk

Górka

et al. 2020

Preprint

Self Cite

View full text Add to dashboard Cite

show abstract

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

Kong

Huang

et al. 2020

Cell Reports

View full text Add to dashboard Cite

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.

show abstract

Comparative proteomic analysis of two divergent strains provides insights into thermotolerance mechanisms of Ganoderma lingzhi

Cai

Liang

et al. 2023

Fungal Genetics and Biology

View full text Add to dashboard Cite

Plant Temperature Acclimation and Growth Rely on Cytosolic Ribosome Biogenesis Factor Homologs

Cited by 41 publications

References 90 publications

Arabidopsis REI-LIKE proteins activate ribosome biogenesis during cold acclimation

Arabidopsis REI-LIKE proteins activate ribosome biogenesis during cold acclimation

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

Comparative proteomic analysis of two divergent strains provides insights into thermotolerance mechanisms of Ganoderma lingzhi

Contact Info

Product

Resources

About