Ribosome Biogenesis in Plants: From Functional 45S Ribosomal DNA Organization to Ribosome Assembly Factors

Sáez‐Vasquez, Julio; Delseny, Michel

doi:10.1105/tpc.18.00874

Cited by 130 publications

(144 citation statements)

References 269 publications

(399 reference statements)

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“…Durut and co-authors (2014) conclude that NUC2 might bind nucleosomes to induce and/or maintain a repressive rDNA chromatin state. Building on the hypothesis that NUC2 may act as a repressor (Sáez-Vásquez and Delseny, 2019), we may naively interpret our observation of deregulated NUC2 expression as indication of feedback repression of the primary step of rRNA transcription in response to blocked 60S maturation. However, studies on reil2 single paralog mutants suggest that the control of rRNA transcription may be negligible compared to feed back control of rRNA processing exerted downstream of the 35S rRNA precursor (Yu et al, 2020).…”

Section: Discussionmentioning

confidence: 83%

“…NUC1 and NUC2 nucleolins have antagonistic roles in rRNA gene expression. Both are required for plant growth (Sáez-Vásquez and Delseny, 2019). Similar to eIF3C2 and eIF3G2 , the reil double mutants constitutively activate NUC2 expression whereas NUC1 expression mirrored cytosolic RP gene expression.…”

Section: Resultsmentioning

confidence: 99%

“…NUC2 and NUC1 act as histone chaperons early in eukaryotic ribosome biogenesis. The nucleolins control rDNA variant expression by modulation of 45S rRNA transcription and/ or processing (Durut et al, 2014; Sáez-Vásquez and Delseny, 2019). NUC2 expression is high in the root apical meristem, similar to our still enigmatic finding of reil dependent PISTILLATA deregulation in roots.…”

Section: Discussionmentioning

confidence: 99%

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Arabidopsis REI-LIKE proteins activate ribosome biogenesis during cold acclimation

Cheong

Beine-Golovchuk

Górka

et al. 2020

Preprint

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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...

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Section: Discussionmentioning

confidence: 83%

Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

See 1 more Smart Citation

Arabidopsis REI-LIKE proteins activate ribosome biogenesis during cold acclimation

Cheong

Beine-Golovchuk

Górka

et al. 2020

Preprint

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“…Mutations in genes encoding ribosomal proteins are also identified as modifiers in as2 or as1 [ 2 , 53 , 54 , 55 , 56 , 57 , 58 ]. In addition, mutations in genes encoding nucleolar proteins, such as RNA HELICASE10 ( RH10 ), NUCLEOLIN1 ( NUC1 ), ROOT INITIATION DEFECTIVE2 ( RID2 ), and APUM23 are involved in ribosome biosynthesis, and enhance the phenotypes of as2 and as1 [ 59 , 60 , 61 , 62 , 63 ]. Mutations in HDT1 and HDT2 for nucleolar histone deacetylases (HDACs), which localize to the nucleolus, also act as modifiers of the as2 and as1 phenotypes [ 35 ].…”

Section: Modifier Mutations That Enhance Defects Of As2 mentioning

confidence: 99%

Roles of ASYMMETRIC LEAVES2 (AS2) and Nucleolar Proteins in the Adaxial–Abaxial Polarity Specification at the Perinucleolar Region in Arabidopsis

Iwakawa

Takahashi

Machida

et al. 2020

IJMS

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Leaves of Arabidopsis develop from a shoot apical meristem grow along three (proximal–distal, adaxial–abaxial, and medial–lateral) axes and form a flat symmetric architecture. ASYMMETRIC LEAVES2 (AS2), a key regulator for leaf adaxial–abaxial partitioning, encodes a plant-specific nuclear protein and directly represses the abaxial-determining gene ETTIN/AUXIN RESPONSE FACTOR3 (ETT/ARF3). How AS2 could act as a critical regulator, however, has yet to be demonstrated, although it might play an epigenetic role. Here, we summarize the current understandings of the genetic, molecular, and cellular functions of AS2. A characteristic genetic feature of AS2 is the presence of a number of (about 60) modifier genes, mutations of which enhance the leaf abnormalities of as2. Although genes for proteins that are involved in diverse cellular processes are known as modifiers, it has recently become clear that many modifier proteins, such as NUCLEOLIN1 (NUC1) and RNA HELICASE10 (RH10), are localized in the nucleolus. Some modifiers including ribosomal proteins are also members of the small subunit processome (SSUP). In addition, AS2 forms perinucleolar bodies partially colocalizing with chromocenters that include the condensed inactive 45S ribosomal RNA genes. AS2 participates in maintaining CpG methylation in specific exons of ETT/ARF3. NUC1 and RH10 genes are also involved in maintaining the CpG methylation levels and repressing ETT/ARF3 transcript levels. AS2 and nucleolus-localizing modifiers might cooperatively repress ETT/ARF3 to develop symmetric flat leaves. These results raise the possibility of a nucleolus-related epigenetic repression system operating for developmental genes unique to plants and predict that AS2 could be a molecule with novel functions that cannot be explained by the conventional concept of transcription factors.

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“…As in other organisms, the number and quality of plant ribosomes must be regulated for proper translation and homeostasis [52,53]. While ribosome synthesis and assembly is relatively well studied [53][54][55][56][57], little is known about the turnover of mature ribosomes at the end of their useful life. As in other organisms, mature plant ribosomes can be degraded to facilitate recycling of building blocks such as nucleotides and amino acids for use in primary metabolism to either maintain cell homeostasis or in response to stress.…”

Section: Degradation Of Ribosomes In Plantsmentioning

confidence: 99%

The Ins and Outs of Autophagic Ribosome Turnover

Kazibwe

Liu

MacIntosh

et al. 2019

Cells

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Ribosomes are essential for protein synthesis in all organisms and their biogenesis and number are tightly controlled to maintain homeostasis in changing environmental conditions. While ribosome assembly and quality control mechanisms have been extensively studied, our understanding of ribosome degradation is limited. In yeast or animal cells, ribosomes are degraded after transfer into the vacuole or lysosome by ribophagy or nonselective autophagy, and ribosomal RNA can also be transferred directly across the lysosomal membrane by RNautophagy. In plants, ribosomal RNA is degraded by the vacuolar T2 ribonuclease RNS2 after transport by autophagy-related mechanisms, although it is unknown if a selective ribophagy pathway exists in plants. In this review, we describe mechanisms of turnover of ribosomal components in animals and yeast, and, then, discuss potential pathways for degradation of ribosomal RNA and protein within the vacuole in plants.

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Ribosome Biogenesis in Plants: From Functional 45S Ribosomal DNA Organization to Ribosome Assembly Factors

Cited by 130 publications

References 269 publications

Arabidopsis REI-LIKE proteins activate ribosome biogenesis during cold acclimation

Arabidopsis REI-LIKE proteins activate ribosome biogenesis during cold acclimation

Roles of ASYMMETRIC LEAVES2 (AS2) and Nucleolar Proteins in the Adaxial–Abaxial Polarity Specification at the Perinucleolar Region in Arabidopsis

The Ins and Outs of Autophagic Ribosome Turnover

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