Whence genes in pieces: Reconstruction of the exon-intron gene structures of the last eukaryotic common ancestor and other ancestral eukaryotes

Wiley Interdisciplinary Reviews: RNA

Volumn 4, Issue 1, 2013, Pages 93-105

  Koonin, Eugene V ^a   Csuros, Miklos ^b   Rogozin, Igor B ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; SELF SPLICING RIBOSOMAL RNA; SMALL NUCLEAR RIBONUCLEOPROTEIN; SMALL NUCLEAR RNA;

ALTERNATIVE RNA SPLICING; EUKARYOTE; EXON; GAIN OF FUNCTION MUTATION; GENE DUPLICATION; GENE EXPRESSION; GENOME; HUMAN; INTRON; LAST COMMON ANCESTOR; LOSS OF FUNCTION MUTATION; NONHUMAN; PRIORITY JOURNAL; REVIEW; SPLICEOSOME;

ALTERNATIVE SPLICING; ANIMALS; BIOLOGICAL EVOLUTION; CONSERVED SEQUENCE; EUKARYOTA; EVOLUTION, MOLECULAR; EXONS; GENOME; HUMANS; INTRONS; SPLICEOSOMES;

ANIMALIA; EUKARYOTA; INVERTEBRATA; PROTISTA; VERTEBRATA; VIRIDIPLANTAE;

EID: 84871430807     PISSN: 17577004     EISSN: 17577012     Source Type: Journal    
DOI: 10.1002/wrna.1143     Document Type: Review

References (102)

1. Gilbert W. Why genes in pieces? Nature 1978, 271:501.
2. Jurica MS, Moore MJ. Pre-mRNA splicing: awash in a sea of proteins. Mol Cell 2003, 12: 5-14.
3. Nilsen TW. The spliceosome: the most complex macromolecular machine in the cell? Bioessays 2003, 25:1147-1149.
4. Doolittle WF. Introns-early. Nature 1978, 272: 581-581.
5. Gilbert W. The exon theory of genes. Cold Spring Harb Symp Quant Biol 1987, 52:901-905.
6. Gilbert W, Glynias M. On the ancient nature of introns. Gene 1993, 135:137-144.
7. Logsdon JM, Jr. The recent origins of spliceosomal introns revisited. Curr Opin Genet Dev 1998, 8:637-648.
8. Lynch M, Richardson AO. The evolution of spliceosomal introns. Curr Opin Genet Dev 2002, 12:701-710.
9. Stoltzfus A, Spencer DF, Zuker M, Logsdon JM, Jr, Doolittle WF. Testing the exon theory of genes: the evidence from protein structure [see comments]. Science 1994, 265:202-207.
10. Stoltzfus A, Logsdon JM, Jr, Palmer JD, Doolittle WF. Intron "sliding" and the diversity of intron positions. Proc Natl Acad Sci U S A 1997, 94:10739-10744.
11. Rogozin IB, Wolf YI, Sorokin AV, Mirkin BG, Koonin EV. Remarkable interkingdom conservation of intron positions and massive, lineage-specific intron loss and gain in eukaryotic evolution. Curr Biol 2003, 13:1512-1517.
12. Koonin EV. The origin of introns and their role in eukaryogenesis: a compromise solution to the introns-early versus introns-late debate? Biol Direct 2006, 1:22.
13. Poole AM, Jeffares DC, Penny D. The path from the RNA world. J Mol Evol 1998, 46:1-17.
14. Penny D, Hoeppner MP, Poole AM, Jeffares DC. An overview of the introns-first theory. J Mol Evol 2009, 69:527-540.
15. Nixon JE, Wang A, Morrison HG, McArthur AG, Sogin ML, Loftus BJ, Samuelson J. A spliceosomal intron in Giardia lamblia. Proc Natl Acad Sci U S A 2002, 99:3701-3705.
16. Simpson AG, MacQuarrie EK, Roger AJ. Eukaryotic evolution: early origin of canonical introns. Nature 2002, 419:270.
17. Fritz-Laylin LK, Prochnik SE, Ginger ML, Dacks JB, Carpenter ML, Field MC, Kuo A, Paredez A, Chapman J, Pham J, et al. The genome of Naegleria gruberi illuminates early eukaryotic versatility. Cell 2010, 140:631-642.
18. Lane CE, van den Heuvel K, Kozera C, Curtis BA, Parsons BJ, Bowman S, Archibald JM. Nucleomorph genome of Hemiselmis andersenii reveals complete intron loss and compaction as a driver of protein structure and function. Proc Natl Acad Sci U S A 2007, 104:19908-19913.
19. Collins L, Penny D. Complex spliceosomal organization ancestral to extant eukaryotes. Mol Biol Evol 2005, 22:1053-1066.
20. Rosbash M, Seraphin B. Who's on first? The U1 snRNP-5′ splice site interaction and splicing. Trends Biochem Sci 1991, 16:187-190.
21. Du H, Rosbash M. The U1 snRNP protein U1C recognizes the 5′ splice site in the absence of base pairing. Nature 2002, 419:86-90.
22. Carmel I, Tal S, Vig I, Ast G. Comparative analysis detects dependencies among the 5′ splice-site positions. RNA 2004, 10:828-840.
23. Umen JG, Guthrie C. A novel role for a U5 snRNP protein in 3′ splice site selection. Genes Dev 1995, 9:855-868.
24. Chiara MD, Palandjian L, Feld Kramer R, Reed R. Evidence that U5 snRNP recognizes the 3′ splice site for catalytic step II in mammals. EMBO J 1997, 16:4746-4759.
25. Dibb NJ, Newman AJ. Evidence that introns arose at proto-splice sites. EMBO J 1989, 8:2015-2021.
26. Dibb NJ. Proto-splice site model of intron origin. J Theor Biol 1991, 151:405-416.
27. Irimia M, Roy SW. Evolutionary convergence on highly-conserved 3′ intron structures in intron-poor eukaryotes and insights into the ancestral eukaryotic genome. PLoS Genet 2008, 4:e1000148.
28. Bon E, Casaregola S, Blandin G, Llorente B, Neuveglise C, Munsterkotter M, Guldener U, Mewes HW, Van Helden J, Dujon B, et al. Molecular evolution of eukaryotic genomes: hemiascomycetous yeast spliceosomal introns. Nucleic Acids Res 2003, 31:1121-1135.
29. Rogozin IB, Milanesi L. Analysis of donor splice sites in different eukaryotic organisms. J Mol Evol 1997, 45:50-59.
30. Lynch M. Intron evolution as a population-genetic process. Proc Natl Acad Sci U S A 2002, 99:6118-6123.
31. Lynch M, Conery JS. The origins of genome complexity. Science 2003, 302:1401-1404.
32. Irimia M, Penny D, Roy SW. Coevolution of genomic intron number and splice sites. Trends Genet 2007, 23:321-325.
33. Irimia M, Roy SW, Neafsey DE, Abril JF, Garcia-Fernandez J, Koonin EV. Complex selection on 5′ splice sites in intron-rich organisms. Genome Res 2009, 19:2021-2027.
34. Rogozin IB, Carmel L, Csuros M, Koonin EV. Origin and evolution of spliceosomal introns. Biol Direct 2012, 7:11.
35. Lynch M. The origins of genome archiecture. Sunderland, MA: Sinauer Associates; 2007.
36. Csuros M, Rogozin IB, Koonin EV. A detailed history of intron-rich eukaryotic ancestors inferred from a global survey of 100 complete genomes. PLoS Comput Biol 2011, 7:e1002150.
37. Aravind L, Watanabe H, Lipman DJ, Koonin EV. Lineage-specific loss and divergence of functionally linked genes in eukaryotes. Proc Natl Acad Sci U S A 2000, 97:11319-11324.
38. Akiyoshi DE, Morrison HG, Lei S, Feng X, Zhang Q, Corradi N, Mayanja H, Tumwine JK, Keeling PJ, Weiss LM, et al. Genomic survey of the non-cultivatable opportunistic human pathogen, Enterocytozoon bieneusi. PLoS Pathog 2009, 5:e1000261.
39. Lee RC, Gill EE, Roy SW, Fast NM. Constrained intron structures in a microsporidian. Mol Biol Evol 2010, 27:1979-1982.
40. Russell AG, Shutt TE, Watkins RF, Gray MW. An ancient spliceosomal intron in the ribosomal protein L7a gene (Rpl7a) of Giardia lamblia. BMC Evol Biol 2005, 5:45.
41. Parenteau J, Durand M, Morin G, Gagnon J, Lucier JF, Wellinger RJ, Chabot B, Elela SA. Introns within ribosomal protein genes regulate the production and function of yeast ribosomes. Cell 2011, 147: 320-331.
42. Logsdon JM, Jr, Tyshenko MG, Dixon C, J DJ, Walker VK, Palmer JD. Seven newly discovered intron positions in the triose-phosphate isomerase gene: evidence for the introns-late theory. Proc Natl Acad Sci U S A 1995, 92:8507-8511.
43. Rzhetsky A, Ayala FJ, Hsu LC, Chang C, Yoshida A. Exon/intron structure of aldehyde dehydrogenase genes supports the "introns-late" theory. Proc Natl Acad Sci U S A 1997, 94:6820-6825.
44. de Souza SJ, Long M, Klein RJ, Roy S, Lin S, Gilbert W. Toward a resolution of the introns early/late debate: only phase zero introns are correlated with the structure of ancient proteins. Proc Natl Acad Sci U S A 1998, 95:5094-5099.
45. Catania F, Lynch M. Where do introns come from? PLoS Biol 2008, 6:e283.
46. Fedorov A, Merican AF, Gilbert W. Large-scale comparison of intron positions among animal, plant, and fungal genes. Proc Natl Acad Sci U S A 2002, 99:16128-16133.
47. Logsdon JM, Jr, Stoltzfus A, Doolittle WF Molecular evolution: recent cases of spliceosomal intron gain? Curr Biol 1998, 8:R560-563.
48. Qiu WG, Schisler N, Stoltzfus A. The evolutionary gain of spliceosomal introns: sequence and phase preferences. Mol Biol Evol 2004, 21:1252-1263.
49. Sverdlov AV, Rogozin IB, Babenko VN, Koonin EV. Conservation versus parallel gains in intron evolution. Nucleic Acids Res 2005, 33:1741-1748.
50. Roy SW, Gilbert W. Complex early genes. Proc Natl Acad Sci U S A 2005, 102:1986-1991.
51. Rogozin IB, Sverdlov AV, Babenko VN, Koonin EV. Analysis of evolution of exon-intron structure of eukaryotic genes. Brief Bioinform 2005, 6:118-134.
52. Csuros M. Likely scenarios of intron evolution. Comp Genomics Lect Notes Comput Sci 2005, 3678:47-60.
53. Carmel L, Rogozin IB, Wolf YI, Koonin EV. An expectation-maximization algorithm for analysis of evolution of exon-intron structure of eukaryotic genes. Comp Genomics Lect Notes Comput Sci 2005, 3678:35-46.
54. Nguyen HD, Yoshihama M, Kenmochi N. New maximum likelihood estimators for eukaryotic intron evolution. PLoS Comput Biol 2005, 1:e79.
55. Carmel L, Wolf YI, Rogozin IB, Koonin EV. Three distinct modes of intron dynamics in the evolution of eukaryotes. Genome Res 2007, 17:1034-1044.
56. Csuros M, Holey JA, Rogozin IB. In search of lost introns. Bioinformatics 2007, 23:i87-96.
57. Csuros M. Malin: maximum likelihood analysis of intron evolution in eukaryotes. Bioinformatics 2008, 24:1538-1539.
58. Sullivan JC, Reitzel AM, Finnerty JR. A high percentage of introns in human genes were present early in animal evolution: evidence from the basal metazoan Nematostella vectensis. Genome Inform 2006, 17:219-229.
59. Raible F, Tessmar-Raible K, Osoegawa K, Wincker P, Jubin C, Balavoine G, Ferrier D, Benes V, de Jong P, Weissenbach J, et al. Vertebrate-type intron-rich genes in the marine annelid Platynereis dumerilii. Science 2005, 310:1325-1326.
60. Csuros M, Rogozin IB, Koonin EV. Extremely intron-rich genes in the alveolate ancestors inferred with a flexible maximum-likelihood approach. Mol Biol Evol 2008, 25:903-911.
61. Martin W, Rujan T, Richly E, Hansen A, Cornelsen S, Lins T, Leister D, Stoebe B, Hasegawa M, Penny D. Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus. Proc Natl Acad Sci U S A 2002, 99:12246-12251.
62. Basu MK, Rogozin IB, Deusch O, Dagan T, Martin W, Koonin EV. Evolutionary dynamics of introns in plastid-derived genes in plants: saturation nearly reached but slow intron gain continues. Mol Biol Evol 2008, 25:111-119.
63. Ahmadinejad N, Dagan T, Gruenheit N, Martin W, Gabaldon T. Evolution of spliceosomal introns following endosymbiotic gene transfer. BMC Evol Biol 2010, 10:57.
64. Danchin EG. What Nematode genomes tell us about the importance of horizontal gene transfers in the evolutionary history of animals. Mob Genet Elements 2011, 1:269-273.
65. Haegeman A, Jones JT, Danchin EG. Horizontal gene transfer in nematodes: a catalyst for plant parasitism? Mol Plant Microbe Interact 2011, 24:879-887.
66. Mayer WE, Schuster LN, Bartelmes G, Dieterich C, Sommer RJ. Horizontal gene transfer of microbial cellulases into nematode genomes is associated with functional assimilation and gene turnover. BMC Evol Biol 2011, 11:13.
67. Danchin EG, Rosso MN, Vieira P, de Almeida-Engler J, Coutinho PM, Henrissat B, Abad P. Multiple lateral gene transfers and duplications have promoted plant parasitism ability in nematodes. Proc Natl Acad Sci U S A 2010, 107:17651-17656.
68. Black DL. Protein diversity from alternative splicing: a challenge for bioinformatics and post-genome biology. Cell 2000, 103:367-370.
69. Kriventseva EV, Koch I, Apweiler R, Vingron M, Bork P, Gelfand MS, Sunyaev S. Increase of functional diversity by alternative splicing. Trends Genet 2003, 19:124-128.
70. Resch A, Xing Y, Modrek B, Gorlick M, Riley R, Lee C. Assessing the impact of alternative splicing on domain interactions in the human proteome. J Proteome Res 2004, 3:76-83.
71. Keren H, Lev-Maor G, Ast G. Alternative splicing and evolution: diversification, exon definition and function. Nat Rev Genet 2010, 11:345-355.
72. Brett D, Hanke J, Lehmann G, Haase S, Delbruck S, Krueger S, Reich J, Bork P. EST comparison indicates 38% of human mRNAs contain possible alternative splice forms. FEBS Lett 2000, 474:83-86.
73. Croft L, Schandorff S, Clark F, Burrage K, Arctander P, Mattick JS. ISIS, the intron information system, reveals the high frequency of alternative splicing in the human genome. Nat Genet 2000, 24:340-341.
74. Modrek B, Resch A, Grasso C, Lee C. Genome-wide detection of alternative splicing in expressed sequences of human genes. Nucleic Acids Res 2001, 29:2850-2859.
75. Pan Q, Shai O, Lee LJ, Frey BJ, Blencowe BJ. Deep surveying of alternative splicing complexity in the human transcriptome by high-throughput sequencing. Nat Genet 2008, 40:1413-1415.
76. Filichkin SA, Priest HD, Givan SA, Shen R, Bryant DW, Fox SE, Wong WK, Mockler TC. Genome-wide mapping of alternative splicing in Arabidopsis thaliana. Genome Res, 20:45-58.
77. Lu T, Lu G, Fan D, Zhu C, Li W, Zhao Q, Feng Q, Zhao Y, Guo Y, Huang X, et al. Function annotation of the rice transcriptome at single-nucleotide resolution by RNA-seq. Genome Res, 20:1238-1249.
78. Severing EI, van Dijk AD, van Ham RC. Assessing the contribution of alternative splicing to proteome diversity in Arabidopsis thaliana using proteomics data. BMC Plant Biol 2011, 11:82.
79. Artamonova, II, Gelfand MS. Comparative genomics and evolution of alternative splicing: the pessimists' science. Chem Rev 2007, 107:3407-3430.
80. Kim E, Goren A, Ast G. Alternative splicing: current perspectives. Bioessays 2008, 30:38-47.
81. Irimia M, Rukov JL, Penny D, Roy SW. Functional and evolutionary analysis of alternatively spliced genes is consistent with an early eukaryotic origin of alternative splicing. BMC Evol Biol 2007, 7:188.
82. Ast G. How did alternative splicing evolve? Nat Rev Genet 2004, 5:773-782.
83. Jackson IJ. A reappraisal of non-consensus mRNA splice sites. Nucleic Acids Res 1991, 19:3795-3798.
84. Hall SL, Padgett RA. Conserved sequences in a class of rare eukaryotic nuclear introns with non-consensus splice sites. J Mol Biol 1994, 239:357-365.
85. Dietrich RC, Incorvaia R, Padgett RA. Terminal intron dinucleotide sequences do not distinguish between U2- and U12-dependent introns. Mol Cell 1997, 1:151-160.
86. Burge CB, Padgett RA, Sharp PA. Evolutionary fates and origins of U12-type introns. Mol Cell 1998, 2:773-785.
87. Russell AG, Charette JM, Spencer DF, Gray MW. An early evolutionary origin for the minor spliceosome. Nature 2006, 443:863-866.
88. Davila Lopez M, Rosenblad MA, Samuelsson T. Computational screen for spliceosomal RNA genes aids in defining the phylogenetic distribution of major and minor spliceosomal components. Nucleic Acids Res 2008, 36:3001-3010.
89. Lin CF, Mount SM, Jarmolowski A, Makalowski W. Evolutionary dynamics of U12-type spliceosomal introns. BMC Evol Biol 2010, 10:47.
90. Patel AA, McCarthy M, Steitz JA. The splicing of U12-type introns can be a rate-limiting step in gene expression. Embo J 2002, 21:3804-3815.
91. Patel AA, Steitz JA. Splicing double: insights from the second spliceosome. Nat Rev Mol Cell Biol 2003, 4:960-970.
92. Basu MK, Makalowski W, Rogozin IB, Koonin EV. U12 intron positions are more strongly conserved between animals and plants than U2 intron positions. Biol Direct 2008, 3:19.
93. Basu MK, Rogozin IB, Koonin EV. Primordial spliceosomal introns were probably U2-type. Trends Genet 2008, 24:525-528.
94. Sverdlov AV, Csuros M, Rogozin IB, Koonin EV. A glimpse of a putative pre-intron phase of eukaryotic evolution. Trends Genet 2007, 23:105-108.
95. Babenko VN, Rogozin IB, Mekhedov SL, Koonin EV. Prevalence of intron gain over intron loss in the evolution of paralogous gene families. Nucleic Acids Res 2004, 32:3724-3733.
96. Makarova KS, Wolf YI, Mekhedov SL, Mirkin BG, Koonin EV. Ancestral paralogs and pseudoparalogs and their role in the emergence of the eukaryotic cell. Nucleic Acids Res 2005, 33:4626-4638.
97. Yoshihama M, Nguyen HD, Kenmochi N. Intron dynamics in ribosomal protein genes. PLoS ONE 2007, 2:e141.
98. Cho G, Doolittle RF. Intron distribution in ancient paralogs supports random insertion and not random loss [published erratum appears in J Mol Evol 1997 Aug;45(2):206]. J Mol Evol 1997, 44:573-584.
99. Martin W, Koonin EV. Introns and the origin of nucleus-cytosol compartmentalization. Nature 2006, 440:41-45.
100. Koonin EV. Intron-dominated genomes of early ancestors of eukaryotes. J Hered 2009, 100:618-623.
101. Lambowitz AM, Zimmerly S. Group II introns: mobile ribozymes that invade DNA. Cold Spring Harb Perspect Biol 2010, 3:a003616.
102. Keating KS, Toor N, Perlman PS, Pyle AM. A structural analysis of the group II intron active site and implications for the spliceosome. Rna 2010, 16: 1-9.