Spatially enriched paralog rearrangements argue functionally diverse ribosomes arise during cold acclimation in arabidopsis
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https://hdl.handle.net/10037/24062Date
2021-06-07Type
Journal articleTidsskriftartikkel
Peer reviewed
Author
Martinez-Seidel, Federico; Beine‐golovchuk, Olga; Hsieh, Yin-Chen; El Eshraky, Kheloud; Gorka, Michal; Cheong, Bo-Eng; Jimenez‐posada, Erika V.; Walther, Dirk; Skirycz, Aleksandra; Roessner, Ute; Kopka, Joachim; Pereira Firmino, Alexandre AugustoAbstract
Ribosome biogenesis is essential for plants to successfully acclimate to low temperature.
Without dedicated steps supervising the 60S large subunits (LSUs) maturation in the cytosol, e.g.,
Rei-like (REIL) factors, plants fail to accumulate dry weight and fail to grow at suboptimal low
temperatures. Around REIL, the final 60S cytosolic maturation steps include proofreading and
assembly of functional ribosomal centers such as the polypeptide exit tunnel and the P-Stalk, respectively. In consequence, these ribosomal substructures and their assembly, especially during
low temperatures, might be changed and provoke the need for dedicated quality controls. To test
this, we blocked ribosome maturation during cold acclimation using two independent reil double
mutant genotypes and tested changes in their ribosomal proteomes. Additionally, we normalized
our mutant datasets using as a blank the cold responsiveness of a wild-type Arabidopsis genotype.
This allowed us to neglect any reil-specific effects that may happen due to the presence or absence
of the factor during LSU cytosolic maturation, thus allowing us to test for cold-induced changes
that happen in the early nucleolar biogenesis. As a result, we report that cold acclimation triggers a
reprogramming in the structural ribosomal proteome. The reprogramming alters the abundance of
specific RP families and/or paralogs in non-translational LSU and translational polysome fractions, a
phenomenon known as substoichiometry. Next, we tested whether the cold-substoichiometry was
spatially confined to specific regions of the complex. In terms of RP proteoforms, we report that
remodeling of ribosomes after a cold stimulus is significantly constrained to the polypeptide exit
tunnel (PET), i.e., REIL factor binding and functional site. In terms of RP transcripts, cold acclimation
induces changes in RP families or paralogs that are significantly constrained to the P-Stalk and
the ribosomal head. The three modulated substructures represent possible targets of mechanisms
that may constrain translation by controlled ribosome heterogeneity. We propose that non-random
ribosome heterogeneity controlled by specialized biogenesis mechanisms may contribute to a preferential or ultimately even rigorous selection of transcripts needed for rapid proteome shifts and
successful acclimation.
Publisher
MDPICitation
Martinez-Seidel, Beine‐golovchuk, Hsieh, El Eshraky, Gorka, Cheong, Jimenez‐posada, Walther, Skirycz, Roessner, Kopka, Pereira Firmino. Spatially enriched paralog rearrangements argue functionally diverse ribosomes arise during cold acclimation in arabidopsis. International Journal of Molecular Sciences. 2021;22(11)Metadata
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