Splicing of Yeast AI5beta Group I Intron Requires SUV3 to Recycle MRS1 Via Mitochondrial Degradosome-promoted Decay of Excised Intron Ribonucleoprotein (RNP)

Overview

Journal J Biol Chem

Specialty Biochemistry

Date 2010 Jan 13

PMID 20064926

Citations 13

Authors

Edward M Turk

Mark G Caprara

Affiliations

Soon will be listed here.

Abstract

Yeast Suv3p is a member of the DEXH/D box family of RNA helicases and is a critical component of the mitochondrial degradosome, which also includes a 3' --> 5' exonuclease, Dss1p. Defects in the degradosome result in accumulation of aberrant transcripts, unprocessed transcripts, and excised group I introns. In addition, defects in SUV3 result in decreased splicing of the aI5beta and bI3 group I introns. Whereas a role for Suv3p in RNA degradation is well established, the function of Suv3p in splicing of group I introns has remained elusive. It has been particularly challenging to determine if Suv3p effects group I intron splicing through RNA degradation as part of the degradosome, or has a direct role in splicing as a chaperone, because nearly all perturbations of SUV3 or DSS1 result in loss of the mitochondrial genome. Here we utilized the suv3-1 allele, which is defective in RNA metabolism and yet maintains a stable mitochondrial genome, to investigate the role of Suv3p in splicing of the aI5beta group I intron. We provide genetic evidence that Mrs1p is a limiting cofactor for aI5beta splicing, and this evidence also suggests that Suv3p activity is required to recycle the excised aI5beta ribonucleoprotein. We also show that Suv3p acts indirectly as a component of the degradosome to promote aI5beta splicing. We present a model whereby defects in Suv3p result in accumulation of stable, excised group I intron ribonucleoproteins, which result in sequestration of Mrs1p, and a concomitant reduction in splicing of aI5beta.

Citing Articles

, the conserved mitochondrial YihA GTPase family member, is required for de novo Cox1 synthesis at suboptimal temperatures in .

Verma Y, Mehra U, Pandey D, Kar J, Perez-Martinez X, Jana S Mol Biol Cell. 2021; 32(21):ar16.

PMID: 34432493 PMC: 8693954. DOI: 10.1091/mbc.E20-07-0457.

Regulates Mitochondrial Translation in Response to Metabolic Cues in Saccharomyces cerevisiae.

Kaur J, Datta K Mol Cell Biol. 2021; 41(11):e0023321.

PMID: 34398681 PMC: 8547514. DOI: 10.1128/MCB.00233-21.

Rice OsRH58, a chloroplast DEAD-box RNA helicase, improves salt or drought stress tolerance in Arabidopsis by affecting chloroplast translation.

Nawaz G, Kang H BMC Plant Biol. 2019; 19(1):17.

PMID: 30626336 PMC: 6327599. DOI: 10.1186/s12870-018-1623-8.

A Novel Function of Pet54 in Regulation of Cox1 Synthesis in Saccharomyces cerevisiae Mitochondria.

Mayorga J, Camacho-Villasana Y, Shingu-Vazquez M, Garcia-Villegas R, Zamudio-Ochoa A, Garcia-Guerrero A J Biol Chem. 2016; 291(17):9343-55.

PMID: 26929411 PMC: 4861497. DOI: 10.1074/jbc.M116.721985.

Double-stranded DNA-dependent ATPase Irc3p is directly involved in mitochondrial genome maintenance.

Sedman T, Gaidutsik I, Villemson K, Hou Y, Sedman J Nucleic Acids Res. 2014; 42(21):13214-27.

PMID: 25389272 PMC: 4245962. DOI: 10.1093/nar/gku1148.

References

Bousquet I, Dujardin G, Poyton R, SLONIMSKI P . Two group I mitochondrial introns in the cob-box and coxI genes require the same MRS1/PET157 nuclear gene product for splicing. Curr Genet. 1990; 18(2):117-24. DOI: 10.1007/BF00312599. View

de la Cruz J, Kressler D, Linder P . Unwinding RNA in Saccharomyces cerevisiae: DEAD-box proteins and related families. Trends Biochem Sci. 1999; 24(5):192-8. DOI: 10.1016/s0968-0004(99)01376-6. View

Rogowska A, Puchta O, Czarnecka A, Kaniak A, Stepien P, Golik P . Balance between transcription and RNA degradation is vital for Saccharomyces cerevisiae mitochondria: reduced transcription rescues the phenotype of deficient RNA degradation. Mol Biol Cell. 2005; 17(3):1184-93. PMC: 1382308. DOI: 10.1091/mbc.e05-08-0796. View

Margossian S, Li H, Zassenhaus H, Butow R . The DExH box protein Suv3p is a component of a yeast mitochondrial 3'-to-5' exoribonuclease that suppresses group I intron toxicity. Cell. 1996; 84(2):199-209. DOI: 10.1016/s0092-8674(00)80975-7. View

Dziembowski A, Piwowarski J, Hoser R, Minczuk M, Dmochowska A, Siep M . The yeast mitochondrial degradosome. Its composition, interplay between RNA helicase and RNase activities and the role in mitochondrial RNA metabolism. J Biol Chem. 2002; 278(3):1603-11. DOI: 10.1074/jbc.M208287200. View

Shadel G, Clayton D . Mitochondrial transcription initiation. Variation and conservation. J Biol Chem. 1993; 268(22):16083-6. View

Woodson S . Structure and assembly of group I introns. Curr Opin Struct Biol. 2005; 15(3):324-30. DOI: 10.1016/j.sbi.2005.05.007. View

Golden B, Kim H, Chase E . Crystal structure of a phage Twort group I ribozyme-product complex. Nat Struct Mol Biol. 2004; 12(1):82-9. DOI: 10.1038/nsmb868. View

Dmochowska A, Golik P, Stepien P . The novel nuclear gene DSS-1 of Saccharomyces cerevisiae is necessary for mitochondrial biogenesis. Curr Genet. 1995; 28(2):108-12. DOI: 10.1007/BF00315775. View

10.

Dmochowska A, Kalita K, Krawczyk M, Golik P, Mroczek K, Lazowska J . A human putative Suv3-like RNA helicase is conserved between Rhodobacter and all eukaryotes. Acta Biochim Pol. 1999; 46(1):155-62. View

11.

Reinders J, Zahedi R, Pfanner N, Meisinger C, Sickmann A . Toward the complete yeast mitochondrial proteome: multidimensional separation techniques for mitochondrial proteomics. J Proteome Res. 2006; 5(7):1543-54. DOI: 10.1021/pr050477f. View

12.

Perlman P, Zhu H, Butow R . The nuclear SUV3-1 mutation affects a variety of post-transcriptional processes in yeast mitochondria. Nucleic Acids Res. 1990; 18(6):1369-76. PMC: 330499. DOI: 10.1093/nar/18.6.1369. View

13.

Labbe S, Thiele D . Copper ion inducible and repressible promoter systems in yeast. Methods Enzymol. 1999; 306:145-53. DOI: 10.1016/s0076-6879(99)06010-3. View

14.

Seraphin B, Simon M, Boulet A, Faye G . Mitochondrial splicing requires a protein from a novel helicase family. Nature. 1989; 337(6202):84-7. DOI: 10.1038/337084a0. View

15.

Margossian S, Butow R . RNA turnover and the control of mitochondrial gene expression. Trends Biochem Sci. 1996; 21(10):392-6. View

16.

Hua S, Qiu M, Chan E, Zhu L, Luo Y . Minimum length of sequence homology required for in vivo cloning by homologous recombination in yeast. Plasmid. 1997; 38(2):91-6. DOI: 10.1006/plas.1997.1305. View

17.

Michel F, Westhof E . Modelling of the three-dimensional architecture of group I catalytic introns based on comparative sequence analysis. J Mol Biol. 1990; 216(3):585-610. DOI: 10.1016/0022-2836(90)90386-Z. View

18.

Mohr S, Matsuura M, Perlman P, Lambowitz A . A DEAD-box protein alone promotes group II intron splicing and reverse splicing by acting as an RNA chaperone. Proc Natl Acad Sci U S A. 2006; 103(10):3569-74. PMC: 1450124. DOI: 10.1073/pnas.0600332103. View

19.

Kaspar B, Bifano A, Caprara M . A shared RNA-binding site in the Pet54 protein is required for translational activation and group I intron splicing in yeast mitochondria. Nucleic Acids Res. 2008; 36(9):2958-68. PMC: 2396411. DOI: 10.1093/nar/gkn045. View

20.

Bassi G, Weeks K . Kinetic and thermodynamic framework for assembly of the six-component bI3 group I intron ribonucleoprotein catalyst. Biochemistry. 2003; 42(33):9980-8. DOI: 10.1021/bi0346906. View