Coevolution of RNA and protein subunits in RNase P and RNase MRP, two RNA processing enzymes.

Publisher: Elsevier Inc. on behalf of American Society for Biochemistry and Molecular Biology Country of Publication: United States NLM ID: 2985121R Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1083-351X (Electronic) Linking ISSN: 00219258 NLM ISO Abbreviation: J Biol Chem Subsets: MEDLINE

Publication: 2021- : [New York, NY] : Elsevier Inc. on behalf of American Society for Biochemistry and Molecular Biology
Original Publication: Baltimore, MD : American Society for Biochemistry and Molecular Biology

Endoribonucleases*/chemistry ; Endoribonucleases*/metabolism ; Evolution, Molecular* ; Protein Subunits*/chemistry ; Protein Subunits*/metabolism ; Ribonuclease P*/chemistry ; Ribonuclease P*/metabolism ; RNA, Catalytic*/genetics ; RNA, Catalytic*/metabolism; Coenzymes ; RNA Processing, Post-Transcriptional ; RNA, Transfer/genetics ; RNA, Transfer/metabolism ; Substrate Specificity ; Eukaryota/enzymology

RNase P and RNase mitochondrial RNA processing (MRP) are ribonucleoproteins (RNPs) that consist of a catalytic RNA and a varying number of protein cofactors. RNase P is responsible for precursor tRNA maturation in all three domains of life, while RNase MRP, exclusive to eukaryotes, primarily functions in rRNA biogenesis. While eukaryotic RNase P is associated with more protein cofactors and has an RNA subunit with fewer auxiliary structural elements compared to its bacterial cousin, the double-anchor precursor tRNA recognition mechanism has remarkably been preserved during evolution. RNase MRP shares evolutionary and structural similarities with RNase P, preserving the catalytic core within the RNA moiety inherited from their common ancestor. By incorporating new protein cofactors and RNA elements, RNase MRP has established itself as a distinct RNP capable of processing ssRNA substrates. The structural information on RNase P and MRP helps build an evolutionary trajectory, depicting how emerging protein cofactors harmonize with the evolution of RNA to shape different functions for RNase P and MRP. Here, we outline the structural and functional relationship between RNase P and MRP to illustrate the coevolution of RNA and protein cofactors, a key driver for the extant, diverse RNP world.
Competing Interests: Conflict of interest The authors declare that they have no conflicts of interest with the contents of this article.
(Copyright © 2024 The Authors. Published by Elsevier Inc. All rights reserved.)

Trends Genet. 2017 Sep;33(9):594-603. (PMID: 28697848)
RNA. 2006 May;12(5):699-706. (PMID: 16540690)
J Biol Chem. 1988 Jan 15;263(2):652-7. (PMID: 2447080)
Science. 1996 Apr 12;272(5259):268-70. (PMID: 8602511)
Nucleic Acids Res. 2005 Aug 08;33(14):4485-95. (PMID: 16087735)
Nucleic Acids Res. 2012 May;40(10):4666-80. (PMID: 22298511)
RNA. 2010 Sep;16(9):1725-47. (PMID: 20627997)
Trends Biochem Sci. 2006 Jun;31(6):333-41. (PMID: 16679018)
Biochemistry. 1984 Dec 18;23(26):6327-34. (PMID: 6085007)
Science. 2004 Oct 1;306(5693):104-7. (PMID: 15459389)
Cell. 1983 Dec;35(3 Pt 2):849-57. (PMID: 6197186)
Cell. 2018 Nov 15;175(5):1393-1404.e11. (PMID: 30454648)
Proc Natl Acad Sci U S A. 2010 Dec 28;107(52):22493-8. (PMID: 21135215)
RNA. 2002 Mar;8(3):296-306. (PMID: 12003490)
Trends Biochem Sci. 2022 Nov;47(11):965-977. (PMID: 35725940)
RNA. 2015 Sep;21(9):1591-605. (PMID: 26135751)
RNA. 2011 Feb;17(2):356-64. (PMID: 21173200)
J Biol Chem. 2012 Oct 26;287(44):37089-97. (PMID: 22977255)
Nat Commun. 2022 Aug 31;13(1):5120. (PMID: 36045135)
RNA. 2018 Jan;24(1):1-5. (PMID: 28971852)
Crit Rev Biochem Mol Biol. 2006 Mar-Apr;41(2):77-102. (PMID: 16595295)
Biochemistry. 1998 Feb 24;37(8):2393-400. (PMID: 9485387)
Annu Rev Biophys. 2013;42:537-57. (PMID: 23654306)
EMBO J. 1990 Jun;9(6):1929-37. (PMID: 2347311)
RNA. 2007 Oct;13(10):1648-55. (PMID: 17717080)
J Biol Chem. 2005 Mar 25;280(12):11352-60. (PMID: 15637077)
Nature. 2010 Dec 9;468(7325):784-9. (PMID: 21076397)
J Cell Biol. 2006 Apr 10;173(1):35-45. (PMID: 16585272)
J Cell Biochem. 2009 Dec 15;108(6):1244-51. (PMID: 19844921)
RNA. 2001 Feb;7(2):220-32. (PMID: 11233979)
Proc Natl Acad Sci U S A. 1993 Jul 15;90(14):6498-502. (PMID: 8341661)
IUBMB Life. 2012 Jun;64(6):521-8. (PMID: 22605678)
Cell. 2016 May 19;165(5):1171-1181. (PMID: 27156450)
Nat Struct Biol. 2000 Oct;7(10):827-8. (PMID: 11017184)
J Biol Chem. 1988 Feb 15;263(5):2447-51. (PMID: 3276688)
Genes Dev. 2017 Jan 1;31(1):59-71. (PMID: 28115465)
Proc Natl Acad Sci U S A. 1994 Jan 18;91(2):659-63. (PMID: 8290578)
BMC Genomics. 2011 Nov 06;12:550. (PMID: 22053856)
Nucleic Acids Res. 2007;35(11):3519-24. (PMID: 17483522)
Mol Cell Biol. 2004 Feb;24(3):945-53. (PMID: 14729943)
EMBO J. 2010 Feb 17;29(4):761-9. (PMID: 20075859)
PLoS One. 2014 Nov 17;9(11):e112488. (PMID: 25401760)
Nucleic Acids Res. 2010 Dec;38(22):7885-94. (PMID: 20716516)
Nat Commun. 2022 Feb 3;13(1):649. (PMID: 35115551)
Science. 1984 Jan 20;223(4633):285-6. (PMID: 6199841)
Science. 2020 Aug 7;369(6504):656-663. (PMID: 32586950)
Cell. 1990 Aug 10;62(3):407-9. (PMID: 1696176)
RNA. 1996 Jun;2(6):551-63. (PMID: 8718684)
Trends Biochem Sci. 1995 Feb;20(2):78-82. (PMID: 7701567)
RNA. 2009 Jul;15(7):1407-16. (PMID: 19465684)
Nat Commun. 2020 Jul 10;11(1):3474. (PMID: 32651392)
Genes Dev. 1994 Nov 1;8(21):2617-28. (PMID: 7958920)
Trends Biochem Sci. 2020 Oct;45(10):825-828. (PMID: 32891515)
Nature. 2003 Feb 13;421(6924):760-4. (PMID: 12610630)
Nature. 2005 Sep 22;437(7058):584-7. (PMID: 16113684)
J Biol Chem. 2020 Feb 21;295(8):2313-2323. (PMID: 31953324)
Nat Commun. 2019 Jun 13;10(1):2617. (PMID: 31197137)
Proc Natl Acad Sci U S A. 2005 Sep 20;102(38):13392-7. (PMID: 16157868)
Curr Opin Struct Biol. 2002 Jun;12(3):289-95. (PMID: 12127446)
Cell. 2001 Jan 26;104(2):195-203. (PMID: 11207361)
RNA. 2006 Aug;12(8):1463-7. (PMID: 16822954)
Genes Dev. 1994 Jun 15;8(12):1423-33. (PMID: 7926742)
J Mol Biol. 1992 Jul 20;226(2):399-409. (PMID: 1379304)
EMBO J. 1987 Feb;6(2):409-17. (PMID: 3582365)
Nucleic Acids Res. 1996 Apr 1;24(7):1252-9. (PMID: 8614627)
Mol Biosyst. 2007 Sep;3(9):604-7. (PMID: 17700860)
Science. 2018 Nov 9;362(6415):. (PMID: 30262633)
Nucleic Acids Res. 1992 Feb 11;20(3):425-32. (PMID: 1371349)
RNA. 2006 Jul;12(7):1373-82. (PMID: 16723659)
Nucleic Acids Res. 2022 Aug 12;50(14):8154-8167. (PMID: 35848927)
Wiley Interdiscip Rev RNA. 2010 Jul-Aug;1(1):102-16. (PMID: 21956908)
Int J Mol Sci. 2021 Sep 24;22(19):. (PMID: 34638646)
J Am Chem Soc. 2017 Dec 6;139(48):17457-17463. (PMID: 29116782)
Trends Biochem Sci. 2021 Dec;46(12):976-991. (PMID: 34511335)
J Biol Chem. 2021 Sep;297(3):101028. (PMID: 34339732)
Genes Dev. 1998 Jun 1;12(11):1678-90. (PMID: 9620854)
J Mol Biol. 2010 Jul 2;400(1):38-51. (PMID: 20434461)
J Cell Biol. 1999 Aug 9;146(3):559-72. (PMID: 10444065)
J Struct Biol. 2021 Jun;213(2):107704. (PMID: 33571640)
RNA Biol. 2009 Jul-Aug;6(3):208-20. (PMID: 19395864)
Elife. 2021 Jun 28;10:. (PMID: 34180399)
Science. 1989 Sep 22;245(4924):1377-80. (PMID: 2476849)
RNA. 2006 Jun;12(6):1023-37. (PMID: 16618965)
EMBO J. 1996 Sep 2;15(17):4723-33. (PMID: 8887563)
Cell Res. 2007 Mar;17(3):219-26. (PMID: 17189938)
Genes Dev. 1997 Mar 1;11(5):582-92. (PMID: 9119223)

Keywords: RNase MRP; RNase P; coevolution; cryo-EM; ribonucleoprotein

0 (Coenzymes)
EC 3.1.- (Endoribonucleases)
EC 3.1.- (mitochondrial RNA-processing endoribonuclease)
0 (Protein Subunits)
EC 3.1.26.5 (Ribonuclease P)
0 (RNA, Catalytic)
9014-25-9 (RNA, Transfer)

Date Created: 20240209 Date Completed: 20240403 Latest Revision: 20240504

20240504

PMC10966300

10.1016/j.jbc.2024.105729

38336296