Plant-specific ribosome biogenesis factors in Arabidopsis thaliana with essential function in rRNA processing

Abstract rRNA processing and assembly of ribosomal proteins during maturation of ribosomes involve many ribosome biogenesis factors (RBFs). Recent studies identified differences in the set of RBFs in humans and yeast, and the existence of plant-specific RBFs has been proposed as well. To identify su...

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Published inNucleic acids research Vol. 47; no. 4; pp. 1880 - 1895
Main Authors Palm, Denise, Streit, Deniz, Shanmugam, Thiruvenkadam, Weis, Benjamin L, Ruprecht, Maike, Simm, Stefan, Schleiff, Enrico
Format Journal Article
LanguageEnglish
Published England Oxford University Press 28.02.2019
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Abstract Abstract rRNA processing and assembly of ribosomal proteins during maturation of ribosomes involve many ribosome biogenesis factors (RBFs). Recent studies identified differences in the set of RBFs in humans and yeast, and the existence of plant-specific RBFs has been proposed as well. To identify such plant-specific RBFs, we characterized T-DNA insertion mutants of 15 Arabidopsis thaliana genes encoding nuclear proteins with nucleotide binding properties that are not orthologues to yeast or human RBFs. Mutants of nine genes show an altered rRNA processing ranging from inhibition of initial 35S pre-rRNA cleavage to final maturation events like the 6S pre-rRNA processing. These phenotypes led to their annotation as 'involved in rRNA processing' - IRP. The irp mutants are either lethal or show developmental and stress related phenotypes. We identified IRPs for maturation of the plant-specific precursor 5′-5.8S and one affecting the pathway with ITS2 first cleavage of the 35S pre-rRNA transcript. Moreover, we realized that 5′-5.8S processing is essential, while a mutant causing 6S accumulation shows only a weak phenotype. Thus, we demonstrate the importance of the maturation of the plant-specific precursor 5′-5.8S for plant development as well as the occurrence of an ITS2 first cleavage pathway in fast dividing tissues.
AbstractList Abstract rRNA processing and assembly of ribosomal proteins during maturation of ribosomes involve many ribosome biogenesis factors (RBFs). Recent studies identified differences in the set of RBFs in humans and yeast, and the existence of plant-specific RBFs has been proposed as well. To identify such plant-specific RBFs, we characterized T-DNA insertion mutants of 15 Arabidopsis thaliana genes encoding nuclear proteins with nucleotide binding properties that are not orthologues to yeast or human RBFs. Mutants of nine genes show an altered rRNA processing ranging from inhibition of initial 35S pre-rRNA cleavage to final maturation events like the 6S pre-rRNA processing. These phenotypes led to their annotation as 'involved in rRNA processing' - IRP. The irp mutants are either lethal or show developmental and stress related phenotypes. We identified IRPs for maturation of the plant-specific precursor 5′-5.8S and one affecting the pathway with ITS2 first cleavage of the 35S pre-rRNA transcript. Moreover, we realized that 5′-5.8S processing is essential, while a mutant causing 6S accumulation shows only a weak phenotype. Thus, we demonstrate the importance of the maturation of the plant-specific precursor 5′-5.8S for plant development as well as the occurrence of an ITS2 first cleavage pathway in fast dividing tissues.
rRNA processing and assembly of ribosomal proteins during maturation of ribosomes involve many ribosome biogenesis factors (RBFs). Recent studies identified differences in the set of RBFs in humans and yeast, and the existence of plant-specific RBFs has been proposed as well. To identify such plant-specific RBFs, we characterized T-DNA insertion mutants of 15 Arabidopsis thaliana genes encoding nuclear proteins with nucleotide binding properties that are not orthologues to yeast or human RBFs. Mutants of nine genes show an altered rRNA processing ranging from inhibition of initial 35S pre-rRNA cleavage to final maturation events like the 6S pre-rRNA processing. These phenotypes led to their annotation as ‘involved in rRNA processing’ - IRP . The irp mutants are either lethal or show developmental and stress related phenotypes. We identified IRPs for maturation of the plant-specific precursor 5′-5.8S and one affecting the pathway with ITS2 first cleavage of the 35S pre-rRNA transcript. Moreover, we realized that 5′-5.8S processing is essential, while a mutant causing 6S accumulation shows only a weak phenotype. Thus, we demonstrate the importance of the maturation of the plant-specific precursor 5′-5.8S for plant development as well as the occurrence of an ITS2 first cleavage pathway in fast dividing tissues.
rRNA processing and assembly of ribosomal proteins during maturation of ribosomes involve many ribosome biogenesis factors (RBFs). Recent studies identified differences in the set of RBFs in humans and yeast, and the existence of plant-specific RBFs has been proposed as well. To identify such plant-specific RBFs, we characterized T-DNA insertion mutants of 15 Arabidopsis thaliana genes encoding nuclear proteins with nucleotide binding properties that are not orthologues to yeast or human RBFs. Mutants of nine genes show an altered rRNA processing ranging from inhibition of initial 35S pre-rRNA cleavage to final maturation events like the 6S pre-rRNA processing. These phenotypes led to their annotation as 'involved in rRNA processing' - IRP. The irp mutants are either lethal or show developmental and stress related phenotypes. We identified IRPs for maturation of the plant-specific precursor 5'-5.8S and one affecting the pathway with ITS2 first cleavage of the 35S pre-rRNA transcript. Moreover, we realized that 5'-5.8S processing is essential, while a mutant causing 6S accumulation shows only a weak phenotype. Thus, we demonstrate the importance of the maturation of the plant-specific precursor 5'-5.8S for plant development as well as the occurrence of an ITS2 first cleavage pathway in fast dividing tissues.
Author Shanmugam, Thiruvenkadam
Simm, Stefan
Palm, Denise
Schleiff, Enrico
Weis, Benjamin L
Streit, Deniz
Ruprecht, Maike
AuthorAffiliation 1 Institute for Molecular Biosciences, Goethe University Frankfurt, Max von Laue Str. 9, D-60438 Frankfurt, Germany
2 Frankfurt Institute for Advanced Studies, D-60438 Frankfurt, Germany
3 Buchmann Institute for Molecular Life Sciences, Goethe University Frankfurt, D-60438 Frankfurt, Germany
AuthorAffiliation_xml – name: 1 Institute for Molecular Biosciences, Goethe University Frankfurt, Max von Laue Str. 9, D-60438 Frankfurt, Germany
– name: 2 Frankfurt Institute for Advanced Studies, D-60438 Frankfurt, Germany
– name: 3 Buchmann Institute for Molecular Life Sciences, Goethe University Frankfurt, D-60438 Frankfurt, Germany
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  orcidid: 0000-0002-0518-3489
  surname: Schleiff
  fullname: Schleiff, Enrico
  email: schleiff@bio.uni-frankfurt.de
  organization: Institute for Molecular Biosciences, Goethe University Frankfurt, Max von Laue Str. 9, D-60438 Frankfurt, Germany
BackLink https://www.ncbi.nlm.nih.gov/pubmed/30576513$$D View this record in MEDLINE/PubMed
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Snippet Abstract rRNA processing and assembly of ribosomal proteins during maturation of ribosomes involve many ribosome biogenesis factors (RBFs). Recent studies...
rRNA processing and assembly of ribosomal proteins during maturation of ribosomes involve many ribosome biogenesis factors (RBFs). Recent studies identified...
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StartPage 1880
SubjectTerms Arabidopsis - genetics
Arabidopsis Proteins - genetics
DNA, Bacterial - genetics
Gene Expression Regulation, Plant - genetics
Molecular Biology
Nuclear Proteins - genetics
Ribosomal Proteins - genetics
Ribosomes - genetics
RNA Precursors - genetics
RNA Processing, Post-Transcriptional - genetics
RNA, Ribosomal - genetics
Title Plant-specific ribosome biogenesis factors in Arabidopsis thaliana with essential function in rRNA processing
URI https://www.ncbi.nlm.nih.gov/pubmed/30576513
https://search.proquest.com/docview/2159985349
https://pubmed.ncbi.nlm.nih.gov/PMC6393314
Volume 47
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