Abstract
Functional transfer RNA (tRNA) molecules are a prerequisite for protein biosynthesis. Several processing steps are required to generate the mature functional tRNA from precursor molecules. Two of the early processing steps involve cleavage at the tRNA 5' end and the tRNA 3' end. While processing at the tRNA 5' end is performed by RNase P, cleavage at the 3' end is catalyzed by the endonuclease tRNase Z. In eukaryotes, tRNase Z enzymes are found in two versions: a short form of about 250 to 300 amino acids and a long form of about 700 to 900 amino acids. All eukaryotic genomes analyzed to date encode at least one long tRNase Z protein. Of those, Arabidopsis (Arabidopsis thaliana) is the only organism that encodes four tRNase Z proteins, two short forms and two long forms. We show here that the four proteins are distributed to different subcellular compartments in the plant cell: the nucleus, the cytoplasm, the mitochondrion, and the chloroplast. One tRNase Z is present only in the cytoplasm, one protein is found exclusively in mitochondria, while the third one has dual locations: nucleus and mitochondria. None of these three tRNase Z proteins is essential. The fourth tRNase Z protein is present in chloroplasts, and deletion of its gene results in an embryo-lethal phenotype. In vitro analysis with the recombinant proteins showed that all four tRNase Z enzymes have tRNA 3' processing activity. In addition, the mitochondrial tRNase Z proteins cleave tRNA-like elements that serve as processing signals in mitochondrial mRNA maturation.
MeSH Terms
Arabidopsis/embryology,enzymology,genetics
Arabidopsis Proteins/analysis,chemistry,genetics
Cell Nucleus/enzymology
Chloroplasts/enzymology
Cytoplasm/enzymology
Endoribonucleases/analysis,chemistry,genetics
Mitochondria/enzymology
Mutation
Nucleic Acid Conformation
Phenotype
Seeds/enzymology,genetics,growth & development
Chemicals
Arabidopsis Proteins
Endoribonucleases
TRZ1 protein, Arabidopsis
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Canino Giusy
Molekulare Botanik, Universität Ulm, 89069 Ulm, Germany.
Bocian Edyta
Barbezier Nicolas
Echeverría Manuel
Forner Joachim
Binder Stefan
Marchfelder Anita
References (33)
33 references, click to expand
-
Integration of foreign sequences into the tobacco plastome via polyethylene glycol-mediated protoplast transformation.
Planta. 1996;199(2):193-201
PMID: 8680308
-
Predotar: A tool for rapidly screening proteomes for N-terminal targeting sequences.
Proteomics. 2004 Jun;4(6):1581-90
PMID: 15174128
-
In vitro processing of mitochondrial and plastid derived tRNA precursors in a plant mitochondrial extract.
Nucleic Acids Res. 1990 Mar 25;18(6):1401-6
PMID: 2326185
-
Processing of a dicistronic tRNA-snoRNA precursor: combined analysis in vitro and in vivo reveals alternate pathways and coupling to assembly of snoRNP.
Plant Physiol. 2009 Jul;150(3):1598-610
PMID: 19420328
-
GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox.
Plant Physiol. 2004 Sep;136(1):2621-32
PMID: 15375207
-
Analysis of the functional modules of the tRNA 3' endonuclease (tRNase Z).
J Biol Chem. 2005 Oct 21;280(42):35440-7
PMID: 16118225
-
Evidence that polyadenylation factor CPSF-73 is the mRNA 3' processing endonuclease.
RNA. 2004 Apr;10(4):565-73
PMID: 15037765
-
Mutations in a plastid-localized elongation factor G alter early stages of plastid development in Arabidopsis thaliana.
BMC Plant Biol. 2007 Jul 13;7:37
PMID: 17629920
-
The tRNase Z family of proteins: physiological functions, substrate specificity and structural properties.
Biol Chem. 2005 Dec;386(12):1253-64
PMID: 16336119
-
RNase P: interface of the RNA and protein worlds.
Trends Biochem Sci. 2006 Jun;31(6):333-41
PMID: 16679018
-
An evolutionary classification of the metallo-beta-lactamase fold proteins.
In Silico Biol. 1999;1(2):69-91
PMID: 11471246
-
A transposon insertion in the Arabidopsis SSR16 gene causes an embryo-defective lethal mutation.
Plant J. 1996 Sep;10(3):479-89
PMID: 8811862
-
Expansion of the zinc metallo-hydrolase family of the beta-lactamase fold.
FEBS Lett. 2001 Aug 10;503(1):1-6
PMID: 11513844
-
5'-to-3' exoribonuclease activity in bacteria: role of RNase J1 in rRNA maturation and 5' stability of mRNA.
Cell. 2007 May 18;129(4):681-92
PMID: 17512403
-
When all's zed and done: the structure and function of RNase Z in prokaryotes.
Nat Rev Microbiol. 2007 Apr;5(4):278-86
PMID: 17363966
-
Arabidopsis genes essential for seedling viability: isolation of insertional mutants and molecular cloning.
Genetics. 2001 Dec;159(4):1765-78
PMID: 11779813
-
Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana.
Plant J. 1998 Dec;16(6):735-43
PMID: 10069079
-
Locating proteins in the cell using TargetP, SignalP and related tools.
Nat Protoc. 2007;2(4):953-71
PMID: 17446895
-
Processing of transfer RNA precursors in a wheat mitochondrial extract.
J Biol Chem. 1990 Aug 15;265(23):13782-91
PMID: 1696257
-
RNase Z in Escherichia coli plays a significant role in mRNA decay.
Mol Microbiol. 2006 May;60(3):723-37
PMID: 16629673
-
Assigning a function to a conserved group of proteins: the tRNA 3'-processing enzymes.
EMBO J. 2002 Jun 3;21(11):2769-77
PMID: 12032089
-
The steady-state level of mRNA from the Ogura cytoplasmic male sterility locus in Brassica cybrids is determined post-transcriptionally by its 3' region.
EMBO J. 1997 Aug 15;16(16):5057-68
PMID: 9305647
-
5' end maturation and RNA editing have to precede tRNA 3' processing in plant mitochondria.
Proc Natl Acad Sci U S A. 1998 Jan 6;95(1):108-13
PMID: 9419337
-
Inactivation of a glycyl-tRNA synthetase leads to an arrest in plant embryo development.
Plant Cell. 1998 Aug;10(8):1277-94
PMID: 9707529
-
Gene-expression analysis and network discovery using Genevestigator.
Trends Plant Sci. 2005 Sep;10(9):407-9
PMID: 16081312
-
tRNA transfers to the limelight.
Genes Dev. 2003 Jan 15;17(2):162-80
PMID: 12533506
-
Transgenic plants.
Cold Spring Harb Symp Quant Biol. 1985;50:433-7
PMID: 3868487
-
Maturation of the 5S rRNA 5' end is catalyzed in vitro by the endonuclease tRNase Z in the archaeon H. volcanii.
RNA. 2008 May;14(5):928-37
PMID: 18369184
-
Metallo-beta-lactamase fold within nucleic acids processing enzymes: the beta-CASP family.
Nucleic Acids Res. 2002 Aug 15;30(16):3592-601
PMID: 12177301
-
Mapping of mitochondrial mRNA termini in Arabidopsis thaliana: t-elements contribute to 5' and 3' end formation.
Nucleic Acids Res. 2007;35(11):3676-92
PMID: 17488843
-
WoLF PSORT: protein localization predictor.
Nucleic Acids Res. 2007 Jul;35(Web Server issue):W585-7
PMID: 17517783
-
Plant dicistronic tRNA-snoRNA genes: a new mode of expression of the small nucleolar RNAs processed by RNase Z.
EMBO J. 2003 Feb 3;22(3):621-32
PMID: 12554662
-
Nucleases of the metallo-beta-lactamase family and their role in DNA and RNA metabolism.
Crit Rev Biochem Mol Biol. 2007 Mar-Apr;42(2):67-93
PMID: 17453916