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Ribosome biogenesis in plants reqRibosome biogenesis in plants requires the nuclear envelope and mitochondria localized OPENER complexuires the nuclear envelope and mitochondria localized OPENER complex

ABSTRACT: Eukaryotic ribosome biogenesis proceeds from nucleolus to cytosol assisted by various assembly factors. The process is evolutionarily conserved across eukaryotes but differences between kingdoms are emerging. Here, we describe how the OPENER (OPNR) protein complex is required for 60S ribosome assembly in the model plant Arabidopsis thaliana. The complex was observed on both nuclear envelope and mitochondria, and contains OPNR, OPENER ASSOCIATED PROTEIN 1 (OAP1), OAP2, Cell Division Cycle 48 D (CDC48D) and Calmodulin-interacting protein 111 (CIP111). Depletion of the OPNR complex components resulted in reproductive lethality and cytoplasmic retention of assembly factors on 60S ribosomes. Subsequent biochemical analyses and structural modelling suggested that OPNR, OAP1 and OAP2 form a claw-like trimer which grabs the ribosome assembly factor RPL24C on the pre-60S ribosome. Our results reveal previously unrecognised subcellular complexity of ribosome biogenesis in plants, and point to mitochondria association as a feature to ensure sufficient translational capacity.

INSTRUMENT(S):

ORGANISM(S): Arabidopsis Thaliana (mouse-ear Cress)

TISSUE(S): Cell Culture

SUBMITTER: Shaochun Zhu

LAB HEAD: Totte Niittylä

PROVIDER: PXD057599 | Pride | 2025-07-24

REPOSITORIES: Pride

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			Action	DRS
	S00090_Exploris01_SZ_TurboID_CK1.raw	Raw
	S00090_Exploris01_SZ_TurboID_CK2.raw	Raw
	S00090_Exploris01_SZ_TurboID_OAPI_VT1.raw	Raw
	S00090_Exploris01_SZ_TurboID_OAPI_VT2.raw	Raw
	S00090_Exploris01_SZ_TurboID_OPNR_VT1.raw	Raw

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Project description:The REIL proteins are required for late ribosomal biogenesis and accumulation of the 60S large ribosome subunit in mature leaves of Arabidopsis thaliana upon acclimation to low temperature. To validate these functions in roots, we conducted a multi-level system analysis targeted at understanding defects and compensations responses of reil mutants before acclimation to low temperature and following temperature shift. Hydroponic root tissue enabled analysis of eukaryotic ribosome complexes with negligible interference of organelle ribosomes. Hydroponic cultivation attenuated the growth defect of reil mutants at low temperature and provided new insights into the primary functions of Arabidopsis REIL proteins. Arabidopsis tightly controls the balance of non-translating 40S and 60S subunits. Reil mutants initially deplete both non-translating subunits upon shift to 10°C and subsequently replenish these pools slowly. Reil mutations compensate the 60S biosynthesis defect by increased baseline levels of non-translating 40S and 60S subunits and depletion of a likely non-translating, KCl-sensitive 80S sub-fraction in the cold. We infer that Arabidopsis buffers fluctuating translation demands following temperature cues by activating non-translating ribosome fractions before de novo synthesis meets temperature-induced demands. Reil1 reil2 double mutants accumulate 43S-preinitiation complexes and pre-60S-maturation complexes and affect the paralog composition of non-translating ribosome fractions. With few exceptions, e.g. RPL3B and RPL24C, these changes were not under transcriptional control. Our study suggests requirement of de novo synthesis of eukaryotic ribosomes for long-term cold acclimation. Double mutant analysis indicates feedback control of REIL-mediated 60S maturation on NUC2 and eIF3C2 transcription and implies functions of two so far non-described proteins in late plant ribosome biogenesis. We propose that Arabidopsis requires biosynthesis of specialized ribosomes for successful cold acclimation.

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Ribosome biogenesis in plants reqRibosome biogenesis in plants requires the nuclear envelope and mitochondria localized OPENER complexuires the nuclear envelope and mitochondria localized OPENER complex

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