Plant Ribosome Biogenesis

A special issue of Plants (ISSN 2223-7747). This special issue belongs to the section "Plant Molecular Biology".

Deadline for manuscript submissions: closed (30 June 2020) | Viewed by 22356

Special Issue Editor


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Guest Editor
1. Goethe Univ Frankfurt, Dept Biosci, Mol Cell Biol Plants, D-60438 Frankfurt, Germany
2. Frankfurt Institute for Advanced Studies, Ruth-Moufang-Straße 1. 60438 Frankfurt am Main, Germany
Interests: plant molecular biology; protein homeostasis; ribosome biogenesis; membrane dynamics
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Special Issue Information

Dear Colleagues,

Nobody will argue against the importance of ribosome biogenesis. In general, ribosome maturation in bacteria and in, e.g., yeast is well described at a functional and structural level. However, we in the plant field are currently at an early but advancing state to understand the multiple dimensions of rRNA maturation in plants. Ever since the discussion of cytosolic ribosome maturation in plants started, certain distinctions to other systems have been described. This ranges from variations in the spacer regions of the rDNA for various functions, different processing orders, and intermediates of the rRNA, susceptibility of rRNA maturation to viroids and environmental stresses, and different numbers of ribosome biogenesis factors to the discovery of plant specific ribosome biogenesis factors. Moreover, recent discoveries show a high complexity of ribosome biogenesis in plants as it occurs three times in one cell—in the nucleus, mitochondria, and chloroplasts. Lately, it was, for example, suggested that mitochondrial ribosomes have an atypical structure or that a link between protein translocation and rRNA processing in chloroplasts exists. I feel the time is right to demonstrate these plant specific features in a Special Issue composed of original articles or reviews advancing the existing ones either by being complementary, more focused, and thus more detailed or by updating the models, including the new knowledge.

Thus, to enhance the visibility of the activity of the “Plant Ribosome Biogenesis Community”, a Special Issue has been organized. We aim to collect original research articles and reviews on recent topics in plant cytosolic, mitochondrial, and plastidic ribosome biogenesis, including but not limited to:

(a) Functional and structural analysis of ribosome biogenesis factors involved in maturation and transport of ribosomes in plant with, e.g., a focus in either plant-specific factors or factors with distinct features when compared to other systems;

(b) Cellular and physiological impact of ribosome biogenesis in plants with, e.g., a focus on phenotypes of rRNA processing deficient mutants and the impact on the nucleolus structure;

(c) Regulation of ribosome biogenesis by means of epigenomic control of genes involved in ribosome biogenesis, of transcriptional regulation of rRNAs, RBF-coding genes and ribosomal proteins including alternative splicing and of translational regulation of RBFs and RPs;

(d) Quality control processes during ribosome maturation in plants with respect to processes and factors involved;

(e) The regulatory function of the rDNA and intergenic region variability in ribosome biogenesis;

(f) Impact of RNAs on ribosome maturation in plants with, e.g., a focus on snoRNAs, viroids, lncRNAs;

(g) Impact of abiotic and biotic stresses on ribosome maturation and function in plants;

(h) The biogenesis of mitochondrial and plastidic ribosomes in plants. Original research, experimental as well as theoretical, both on model and crop plants is welcome.

Two remarks at the end: As the field is constantly growing, it would be very kind of you if you could pass this invitation to other interested, particularly newly-founded groups or groups that have recently turned into our field. Further, if you feel you should/could/want to provide a review article, please contact Enrico Schleiff in advance, as he is organizing the slots for the reviews.

To all of you: Have fun with premature ribosomes!

Prof. Dr. Enrico Schleiff
Guest Editor

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Keywords

  • rDNA
  • rRNA
  • snoRNA
  • lncRNAS
  • viroids
  • RNA polymerase
  • ribosome
  • ribosome biogenesis
  • ribosome biogenesis factors
  • PPR—proteins
  • nucleolus
  • nucleus
  • mitochondria
  • chloroplasts
  • quality control
  • environmental stresses
  • species-specific variations

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Published Papers (5 papers)

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Research

20 pages, 19375 KiB  
Article
Engineered Ripening-Specific Accumulation of Polyamines Spermidine and Spermine in Tomato Fruit Upregulates Clustered C/D Box snoRNA Gene Transcripts in Concert with Ribosomal RNA Biogenesis in the Red Ripe Fruit
by Vijaya Shukla, Tahira Fatima, Ravinder K. Goyal, Avtar K. Handa and Autar K. Mattoo
Plants 2020, 9(12), 1710; https://doi.org/10.3390/plants9121710 - 4 Dec 2020
Cited by 7 | Viewed by 2849
Abstract
Ripening of tomato fruit leads, in general, to a sequential decrease in the endogenous levels of polyamines spermidine (SPD) and spermine (SPM), while the trend for the diamine putrescine (PUT) levels is generally an initial decrease, followed by a substantial increase, and thereafter [...] Read more.
Ripening of tomato fruit leads, in general, to a sequential decrease in the endogenous levels of polyamines spermidine (SPD) and spermine (SPM), while the trend for the diamine putrescine (PUT) levels is generally an initial decrease, followed by a substantial increase, and thereafter reaching high levels at the red ripe fruit stage. However, genetic engineering fruit-specific expression of heterologous yeast S-adenosylmethionine (SAM) decarboxylase in tomato has been found to result in a high accumulation of SPD and SPM at the cost of PUT. This system enabled a genetic approach to determine the impact of increased endogenous levels of biogenic amines SPD and SPM in tomato (579HO transgenic line) and on the biogenesis, transcription, processing, and stability of ribosomal RNA (rRNA) genes in tomato fruit as compared with the non-transgenic 556AZ line. One major biogenetic process regulating transcription and processing of pre-mRNA complexes in the nucleus involves small nucleolar RNAs (snoRNAs). To determine the effect of high levels of SPD and SPM on these latter processes, we cloned, sequenced, and identified a box C/D snoRNA cluster in tomato, namely, SlSnoR12, SlU24a, Slz44a, and Slz132b. Similar to this snoRNA cluster housed on chromosome (Chr.) 6, two other noncoding C/D box genes, SlsnoR12.2 and SlU24b, with a 94% identity to those on Chr. 6 were found located on Chr. 3. We also found that other snoRNAs divisible into snoRNA subclusters A and B, separated by a uridine rich spacer, were decorated with other C/D box snoRNAs, namely, J10.3, Z131a/b, J10.1, and Z44a, followed by z132a, J11.3, z132b, U24, Z20, U24a, and J11. Several of these, for example, SlZ44a, Slz132b, and SlU24a share conserved sequences similar to those in Arabidopsis and rice. RNAseq analysis of high SPD/SPM transgenic tomatoes (579HO line) showed significant enrichment of RNA polymerases, ribosomal, and translational protein genes at the breaker+8 ripening stage as compared with the 556AZ control. Thus, these results indicate that SPD/SPM regulates snoRNA and rRNA expression directly or indirectly, in turn, affecting protein synthesis, metabolism, and other cellular activities in a positive manner. Full article
(This article belongs to the Special Issue Plant Ribosome Biogenesis)
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18 pages, 4885 KiB  
Article
The Existence and Localization of Nuclear snoRNAs in Arabidopsis thaliana Revisited
by Deniz Streit, Thiruvenkadam Shanmugam, Asen Garbelyanski, Stefan Simm and Enrico Schleiff
Plants 2020, 9(8), 1016; https://doi.org/10.3390/plants9081016 - 12 Aug 2020
Cited by 13 | Viewed by 3260
Abstract
Ribosome biogenesis is one cell function-defining process. It depends on efficient transcription of rDNAs in the nucleolus as well as on the cytosolic synthesis of ribosomal proteins. For newly transcribed rRNA modification and ribosomal protein assembly, so-called small nucleolar RNAs (snoRNAs) and ribosome [...] Read more.
Ribosome biogenesis is one cell function-defining process. It depends on efficient transcription of rDNAs in the nucleolus as well as on the cytosolic synthesis of ribosomal proteins. For newly transcribed rRNA modification and ribosomal protein assembly, so-called small nucleolar RNAs (snoRNAs) and ribosome biogenesis factors (RBFs) are required. For both, an inventory was established for model systems like yeast and humans. For plants, many assignments are based on predictions. Here, RNA deep sequencing after nuclei enrichment was combined with single molecule species detection by northern blot and in vivo fluorescence in situ hybridization (FISH)-based localization studies. In addition, the occurrence and abundance of selected snoRNAs in different tissues were determined. These approaches confirm the presence of most of the database-deposited snoRNAs in cell cultures, but some of them are localized in the cytosol rather than in the nucleus. Further, for the explored snoRNA examples, differences in their abundance in different tissues were observed, suggesting a tissue-specific function of some snoRNAs. Thus, based on prediction and experimental confirmation, many plant snoRNAs can be proposed, while it cannot be excluded that some of the proposed snoRNAs perform alternative functions than are involved in rRNA modification. Full article
(This article belongs to the Special Issue Plant Ribosome Biogenesis)
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29 pages, 3132 KiB  
Article
Separation and Paired Proteome Profiling of Plant Chloroplast and Cytoplasmic Ribosomes
by Alexandre Augusto Pereira Firmino, Michal Gorka, Alexander Graf, Aleksandra Skirycz, Federico Martinez-Seidel, Kerstin Zander, Joachim Kopka and Olga Beine-Golovchuk
Plants 2020, 9(7), 892; https://doi.org/10.3390/plants9070892 - 14 Jul 2020
Cited by 17 | Viewed by 6408
Abstract
Conventional preparation methods of plant ribosomes fail to resolve non-translating chloroplast or cytoplasmic ribosome subunits from translating fractions. We established preparation of these ribosome complexes from Arabidopsis thaliana leaf, root, and seed tissues by optimized sucrose density gradient centrifugation of protease protected plant [...] Read more.
Conventional preparation methods of plant ribosomes fail to resolve non-translating chloroplast or cytoplasmic ribosome subunits from translating fractions. We established preparation of these ribosome complexes from Arabidopsis thaliana leaf, root, and seed tissues by optimized sucrose density gradient centrifugation of protease protected plant extracts. The method co-purified non-translating 30S and 40S ribosome subunits separated non-translating 50S from 60S subunits, and resolved assembled monosomes from low oligomeric polysomes. Combining ribosome fractionation with microfluidic rRNA analysis and proteomics, we characterized the rRNA and ribosomal protein (RP) composition. The identity of cytoplasmic and chloroplast ribosome complexes and the presence of ribosome biogenesis factors in the 60S-80S sedimentation interval were verified. In vivo cross-linking of leaf tissue stabilized ribosome biogenesis complexes, but induced polysome run-off. Omitting cross-linking, the established paired fractionation and proteome analysis monitored relative abundances of plant chloroplast and cytoplasmic ribosome fractions and enabled analysis of RP composition and ribosome associated proteins including transiently associated biogenesis factors. Full article
(This article belongs to the Special Issue Plant Ribosome Biogenesis)
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16 pages, 3324 KiB  
Article
Ethylene is Involved in Symptom Development and Ribosomal Stress of Tomato Plants upon Citrus Exocortis Viroid Infection
by Francisco Vázquez Prol, M. Pilar López-Gresa, Ismael Rodrigo, José María Bellés and Purificación Lisón
Plants 2020, 9(5), 582; https://doi.org/10.3390/plants9050582 - 2 May 2020
Cited by 8 | Viewed by 4616
Abstract
Citrus exocortis viroid (CEVd) is known to cause different symptoms in citrus trees, and its mechanism of infection has been studied in tomato as an experimental host, producing ribosomal stress on these plants. Some of the symptoms caused by CEVd in tomato plants [...] Read more.
Citrus exocortis viroid (CEVd) is known to cause different symptoms in citrus trees, and its mechanism of infection has been studied in tomato as an experimental host, producing ribosomal stress on these plants. Some of the symptoms caused by CEVd in tomato plants resemble those produced by the phytohormone ethylene. The present study is focused on elucidating the relationship between CEVd infection and ethylene on disease development. To this purpose, the ethylene insensitive Never ripe (Nr) tomato mutants were infected with CEVd, and several aspects such as susceptibility to infection, defensive response, ethylene biosynthesis and ribosomal stress were studied. Phenotypic characterization revealed higher susceptibility to CEVd in these mutants, which correlated with higher expression levels of both defense and ethylene biosynthesis genes, as well as the ribosomal stress marker SlNAC082. In addition, Northern blotting revealed compromised ribosome biogenesis in all CEVd infected plants, particularly in Nr mutants. Our results indicate a higher ethylene biosynthesis in Nr mutants and suggest an important role of this phytohormone in disease development and ribosomal stress caused by viroid infection. Full article
(This article belongs to the Special Issue Plant Ribosome Biogenesis)
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22 pages, 3595 KiB  
Article
The bRPS6-Family Protein RFC3 Prevents Interference by the Splicing Factor CFM3b during Plastid rRNA Biogenesis in Arabidopsis thaliana
by Yumi Nagashima, Katsutomo Ohshiro, Akiyasu Iwase, Miyuki T. Nakata, Shugo Maekawa and Gorou Horiguchi
Plants 2020, 9(3), 328; https://doi.org/10.3390/plants9030328 - 4 Mar 2020
Cited by 4 | Viewed by 4137
Abstract
Plastid ribosome biogenesis is important for plant growth and development. REGULATOR OF FATTY ACID COMPOSITION3 (RFC3) is a member of the bacterial ribosomal protein S6 family and is important for lateral root development. rfc3-2 dramatically reduces the plastid rRNA level and produces lateral [...] Read more.
Plastid ribosome biogenesis is important for plant growth and development. REGULATOR OF FATTY ACID COMPOSITION3 (RFC3) is a member of the bacterial ribosomal protein S6 family and is important for lateral root development. rfc3-2 dramatically reduces the plastid rRNA level and produces lateral roots that lack stem cells. In this study, we isolated a suppressor of rfc three2 (sprt2) mutant that enabled recovery of most rfc3 mutant phenotypes, including abnormal primary and lateral root development and reduced plastid rRNA level. Northern blotting showed that immature and mature plastid rRNA levels were reduced, with the exception of an early 23S rRNA intermediate, in rfc3-2 mutants. These changes were recovered in rfc3-2 sprt2-1 mutants, but a second defect in the processing of 16S rRNA appeared in this line. The results suggest that rfc3 mutants may be defective in at least two steps of plastid rRNA processing, one of which is specifically affected by the sprt2-1 mutation. sprt2-1 mutants had a mutation in CRM FAMILY MEMBER 3b (CFM3b), which encodes a plastid-localized splicing factor. A bimolecular fluorescence complementation (BiFC) assay suggested that RFC3 and SPRT2/CFM3b interact with each other in plastids. These results suggest that RFC3 suppresses the nonspecific action of SPRT2/CFM3b and improves the accuracy of plastid rRNA processing. Full article
(This article belongs to the Special Issue Plant Ribosome Biogenesis)
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