The recent origins of spliceosomal introns revisited

Current Opinion in Genetics and Development

Volumn 8, Issue 6, 1998, Pages 637-648

  Logsdon Jr, John M ^a  

^a DALHOUSIE UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

EUKARYOTE; EVOLUTION; EXON; GENE; INTRON; MITOCHONDRION; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; PROTEIN STRUCTURE; REVIEW; SPLICEOSOME;

EUKARYOTA;

EID: 0031737389     PISSN: 0959437X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-437X(98)80031-2     Document Type: Article

References (92)

1. Palmer JD, Logsdon JM Jr. The recent origin of introns. Curr Opin Genet Dev. 1:1991;470-477.
2. Doolittle WF. Genes in pieces: were they ever together? Nature. 272:1978;581-582.
3. Darnell JE, Doolittle WF. Speculations on the early course of evolution. Proc Natl Acad Sci USA. 83:1986;1271-1275.
4. Gilbert W, Marchionni M, McKnight G. On the antiquity of introns. Cell. 46:1986;151-154.
5. Rogers JH. The role of introns in evolution. FEBS Lett. 268:1990;339-343.
6. Cavalier-Smith T. Intron phylogeny: a new hypothesis. Trends Genet. 7:1991;145-148.
7. Roger AJ, Keeling PJ, Doolittle WF. Introns, the broken transposons. Soc Gen Physiol Ser. 49:1994;27-37.
8. Sharp PA. Five easy pieces. Science. 254:1991;263.
9. Copertino DW, Hallick RB. Group II and group III introns of twintrons: potential relationships with nuclear pre-mRNA introns. Trends Biochem Sci. 18:1993;467-471.
10. Wise JA. Guides to the heart of the spliceosome. Science. 262:1993;1978-1979.
11. Cavalier-Smith T. Kingdom protozoa and its 18 phyla. Microbiol Rev. 57:1993;953-994.
12. Sogin ML. The origin of eukaryotes and evolution into major kingdoms. Bengston S. Early Life on Earth. Nobel Symposiun No. 84. 1994;181-192 Columbia University Press, New York.
13. Biderre C, Metenier G, Vivares CP. A small spliceosomal-type intron occurs in a ribosomal protein gene of the microsporidian Encephalitozoon cuniculi. Mol Biochem Parasitol. 94:1998;283-286.
14. DiMaria P, Palic B, Debrunner-Vossbrinck BA, Lapp J, Vossbrinck CR. Characterization of the highly divergent U2 RNA homolog in the microsporidian Vairimorpha necatrix. Nucleic Acids Res. 24:1996;515-522.
15. Fast NM, Roger AJ, Richardson CA, Doolittle WF. U2 and U6 snRNA genes in the microsporidian Nosema locustae: evidence for a functional spliceosome. of special interest Nucleic Acids Res. 26:1998;3202-3207 Reports the discovery of U2 and U6 spliceosomal snRNA genes from the microsporidian, Nosema. These data provided further, albeit indirect, evidence that microsporidia contain introns - a result which was verified very recently [13].
16. Edlind TD, Li J, Visvesvera GS, Vodkin MH, McLaughlin GL, Katiyar SK. Phylogenetic analysis of beta-tubulin sequences from amitochondrial protozoa. Mol Phylogenet Evol. 5:1996;359-367.
17. Keeling PJ, Doolittle WF. Alpha-tubulin from early-diverging eukaryotic lineages and the evolution of the tubulin family. Mol Biol Evol. 13:1996;1297-1305.
18. Germot A, Philippe H, Le Guyader H. Evidence for loss of mitochondria in Microsporidia from a mitochondrial-type HSP70 in Nosema locustae. Mol Biochem Parasitol. 87:1997;159-168.
19. Hirt RP, Healy B, Vossbrinck CR, Canning EU, Embley TM. A mitochondrial Hsp70 orthologue in Vairimorpha necatrix: molecular evidence that microsporidia once contained mitochondria. Curr Biol. 7:1997;995-998.
20. Hirt RP, Logsdon JM Jr, Healy B, Dorey M, Doolittle WF, Embley TM. Microsporidia are related to fungi: evidence from the largest subunit of RNA polymerase II and other proteins. Proc Natl Acad Sci USA. 1998;. in press.
21. Palmer JD, Delwiche CF. Second-hand chloroplasts and the case of the disappearing nucleus. Proc Natl Acad Sci USA. 93:1996;7432-7435.
22. Baldauf SL, Doolittle WF. Origin and evolution of the slime molds (Mycetozoa). Proc Natl Acad Sci USA. 94:1997;12007-12012.
23. Peyretaillade E, Biderre C, Peyret P, Duffieux F, Metenier G, Gouy M, Michot B, Vivares CP. Microsporidian Encephalitozoon cuniculi, a unicellular eukaryote with an unusual chromosomal dispersion of ribosomal genes and a LSU rRNA reduced to the universal core. Nucleic Acids Res. 26:1998;3513-3520.
24. Keeling PJ, McFadden GI. Origins of microsporidia. Trends Microbiol. 6:1998;19-23.
25. Nilsen TW. trans-splicing: an update. Mol Biochem Parasitol. 73:1995;1-6.
26. Lucke S, Klockner T, Palfi Z, Boshart M, Bindereif A. Trans mRNA splicing in trypanosomes: cloning and analysis of a PRP8-homologous gene from Trypanosoma brucei provides evidence for a U5-analogous RNP. EMBO J. 16:1997;4433-4440.
27. Bonen L. Trans-splicing of pre-mRNA in plants, animals, and protists. FASEB J. 7:1993;40-46.
28. Hashimoto T, Nakamura Y, Kamaishi T, Hasegawa M. Early evolution of eukaryotes inferred from protein phylogenies of translation elongation factors 1α and 2. Arch Protiskend. 148:1997;287-295.
29. Henze K, Badr A, Wettern M, Cerff R, Martin W. A nuclear gene of eubacterial origin in Euglena gracilis reflects cryptic endosymbioses during protist evolution. Proc Natl Acad Sci USA. 92:1995;9122-9126.
30. Niu XH, Hartshorne T, He XY, Agabian N. Characterization of putative small nuclear RNAs from Giardia lamblia. Mol Biochem Parasitol. 66:1994;49-57.
31. Smith MW, Aley SB, Sogin M, Gillin D, Evans GA. Sequence survey of the Giardia lamblia genome. Mol Biochem Parasitol. 1998;. in press.
32. Stiller JW, Hall BD. The origin of red algae: implications for plastid evolution. Proc Natl Acad Sci USA. 94:1997;4520-4525.
33. Hilario E, Gogarten JP. The prokaryote-to-eukaryote transition reflected in the evolution of the V/F/A-ATPase catalytic and proteolipid subunits. J Mol Evol. 46:1998;703-715.
34. Leipe DD, Gunderson JH, Nerad TA, Sogin ML. Small subunit ribosomal RNA of Hexamita inflata and the quest for the first branch in the eukaryotic tree. Mol Biochem Parasitol. 59:1993;41-48.
35. Shih MC, Heinrich P, Goodman HM. Intron existence predated the divergence of eukaryotes and prokaryotes. Science. 242:1988;1164-1166.
36. Liaud MF, Zhang DX, Cerff R. Differential intron loss and endosymbiotic transfer of chloroplast glyceraldehyde-3-phosphate dehydrogenase genes to the nucleus. Proc Natl Acad Sci USA. 87:1990;8918-8922.
37. Kersanach R, Brinkmann H, Llaud M, Zhang D, Martin W, Cerff R. Five identical intron positions in ancient duplicated genes of eubacterial origin. Nature. 367:1994;387-389.
38. Stoltzfus A. Origin of introns - early or late. Nature. 369:1994;526-527.
39. Logsdon JM Jr, Palmer JD. Origin of introns - early or late? Nature. 369:1994;526.
40. Cho G, Doolittle RF. Intron distribution in ancient paralogs supports random insertion and not random loss. of outstanding interest J Mol Evol. 44:1997;573-584 An important and insightful analysis of introns in ten gene family pairs that diverged prior to the LCA ('ancient paralogs'). The authors compare probability models of random intron gain and loss to explain the coincidence of intron positions in these paralogs. They conclude that random insertion explains the patterns significantly better than intron loss, even when allowing for intron 'sliding'.
41. Dibb NJ, Newman AJ. Evidence that introns arose at proto-splice sites. EMBO J. 8:1989;2015-2021.
42. Hankeln T, Friedl H, Ebersberger I, Martin J, Schmidt ER. A variable intron distribution in globin genes of Chironomus: evidence for recent intron gain. of outstanding interest Gene. 205:1997;151-160 A report of recently inserted introns in globin genes from chironomid midges. The authors compared three paralogous globin genes from each of 16 species (with most of the genes sequenced themselves), these paralogs having diverged well before the Chironomous species divergences. Exclusive to the Chironomous thummi species-group, they found that all three of the globin paralogs contain a uniquely positioned intron. This intron was apparently gained three separate times following the divergence of Chironomous species groups. The fact the intron sequences in the three paralogs are demonstrably homologous suggests that the intron - after having initially been gained - was moved between paralogs by a gene conversion-like mechanism. Interestingly, the authors identify another recently gained intron in one paralog in the Chironomous melanotus species group; this intron, although shared in position with plants, is a clear case of parallel insertion.
43. Straus D, Gilbert W. Genetic engineering in the Precambrian: structure of the chicken triosephosphate isomerase gene. Mol Cell Biol. 5:1985;3497-3506.
44. Tittiger CS, Walker VK. A novel intron site in the triosephosphate isomerase gene from the mosquito, Culex tarsalis. Nature. 361:1992;470-472.
45. Doolittle WF, Stoltzfus A. Genes-in-pieces revisited. Nature. 361:1993;403.
46. Gilbert W, Glynias M. On the ancient nature of introns. Gene. 135:1993;137-144.
47. Stoltzfus A, Spencer DF, Zuker M, Logsdon JM Jr, Doolittle WF. Testing the exon theory of genes: the evidence from protein structure. Science. 265:1994;202-207.
48. Logsdon JM Jr, Tyshenko MG, Dixon C, D-Jafari J, 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 USA. 92:1995;8507-8511.
49. Kwiatowski J, Krawczyk M, Kornacki M, Bailey K, Ayala FJ. Evidence against the exon theory of genes derived from the triose-phosphate isomerase gene. Proc Natl Acad Sci USA. 92:1995;8503-8506.
50. Tyshenko MG, Walker VK. Towards a reconciliation of the introns early or late views: triosephosphate isomerase genes from insects. Biochim Biophys Acta. 1353:1997;131-136.
51. Keeling PJ, Doolittle WF. Evidence that eukaryotic triosephosphate isomerase is of alpha-proteobacterial origin. of special interest Proc Natl Acad Sci USA. 94:1997;1270-1275 Provides compelling phylogenetic results indicating that triose-phosphate isomerase (TPI) in eukaryotes is eubacterial in origin. Specifically, the authors show an α-proteobacterial affinity of TPI and thus a possible mitochondrial origin. This gene has been key to the intron evolution debate, and its eubacterial origin makes IE scenarios of intron loss increasingly difficult.
52. de Souza SJ, Long M, Gilbert W. Introns and gene evolution. of special interest Genes Cells. 1:1996;493-505 A remarkably argumentative review strongly favoring the IE view.
53. Gilbert W, de Souza SJ, Long M. Origin of genes. of special interest Proc Natl Acad Sci USA. 94:1997;7698-7703 A forceful 'review' from the main current proponents of the IE theory. This paper mainly re-iterates previous analyses of intron phase and protein structure correlations but also includes some updates of these studies.
54. Mattick JS. Introns: evolution and function. Curr Opin Genet Dev. 4:1994;823-831.
55. Weber K, Kabsch W. Intron positions in actin genes seem unrelated to the secondary structure of the protein. EMBO J. 13:1994;1280-1286.
56. de Souza SJ, Long M, Schoenbach L, Roy SW, Gilbert W. Intron positions correlate with module boundaries in ancient proteins. Proc Natl Acad Sci USA. 93:1996;14632-14636. [Published connection appears in Proc Natl Acad Sci USA 1997, 18:1603].
57. 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. of outstanding interest Proc Natl Acad Sci USA. 95:1998;5094-5099 An update and integration of previous findings on intron phase and protein structure. With a larger database of proteins and intron positions, the authors now examine the relationship between these two results after confirming each with the new data. They find that most of the statistical excess observed for protein correlation is provided by phase zero introns and it is largely the non-vertebrate introns that contribute to the signal. The authors suggest that these results could provide resolution between the IE and IL theories by allowing for both ancient (mostly phase zero) introns as well as later intron gain (in all three phases). They argue that "about 35%" of introns in ancient proteins are themselves ancient, the rest having been inserted.
58. Long M, Rosenberg C, Gilbert W. Intron phase correlations and the evolution of the intron/exon structure of genes. Proc Natl Acad Sci USA. 92:1995;12495-12499.
59. Tomita M, Shimizu N, Brutlag DL. Introns and reading frames: correlation between splicing sites and their codon positions. Mol Biol Evol. 13:1996;1219-1223.
60. Patthy L. Modular exchange principles in proteins. Curr Opin Struct Biol. 1:1991;351-361.
61. Patthy L. Exon shuffling and other ways of module exchange. Matrix Biol. 15:1996;301-310. (discussion 311-302.).
62. Fedorov A, Fedorova L, Starshenko V, Filatov V, Griggor'ev E. Influence of exon duplication on intron and exon phase distribution. of special interest J Mol Evol. 46:1998;263-271 Demonstrates that exon duplication, arguably a special case of exon shuffling, contributes significantly to observed non-randomness in intron phases. The authors claim that such influences were not taken into account by Long et al. [58]. Nonetheless, such duplicated exons could not account for all observed phase correlations, which they estimate to comprise 6% of the human genome.
63. Berget SM. Exon recognition in vertebrate splicing. J Biol Chem. 270:1995;2411-2414.
64. Hurst LD, McVean GT. A difficult phase for introns-early. Curr Biol. 6:1996;533-536.
65. Stoltzfus A, Logsdon JM Jr, Palmer JD, Doolittle WF. Intron 'sliding' and the diversity of intron positions. of outstanding interest Proc Natl Acad Sci USA. 94:1997;10739-10744 Is intron 'sliding' a reasonable explanation for observed differences in intron positions? This report asks this question in an even-handed way, largely avoiding the IE vs. IL debate itself. In considering a number of possible indications of intron sliding, no strong evidence for such a process could be found. It was, thus, concluded that sliding could not contribute significantly to the diversity of intron positions. Nonetheless, these results can only be viewed in strong-support of the IL theory.
66. Jellie AM, Tate WP, Trotman CNA. Evolutionary history of introns in a multidomain globin gene. J Mol Evol. 42:1996;641-647.
67. Rzhetsky A, Ayala FJ, Hsu LC, Chang C, Yoshida A. Exon/intron structure of aldehyde dehydrogenase genes supports the 'introns-late' theory. of outstanding interest Proc Natl Acad Sci USA. 94:1997;6820-6825 A careful comparison of IE and IL models using a maximum likelihood analysis of intron positions. Starting from a resolved phylogenetic tree of the aldehyde dehydrogenase gene family, comprising nine completely sequenced genes in humans, scenarios of intron gain, loss and/or sliding were compared. An IE model which allowed both intron loss and sliding was preferred, but only allowing sliding rates that were very high. The authors suggest that the inferred rate of sliding (higher than the intron deletion rate) would be so unreasonable that any possible correlation between protein and gene would be obscured, leading to an internal contradiction of the IE theory in the absence of the sliding assumption, the IL models of intron gain fared best.
68. Logsdon JM, Stoltzfus A, Doolittle WF. Recent cases of spliceosomal intron gain? of outstanding interest Curr Biol. 8:1998;R560-R563 This commentary lays out the problems of finding and clearly documenting recent spliceosomal intron gains. Three reports identifying possible cases of intron gain are examined in detail, and one is called into question. In the bona fide cases, intron gain was determined to have occurred at proto-splice site motifs, indicating the importance of this sequence in the mechanism(s) of spliceosomal intron insertion.
69. Giroux MJ, Clancy M, Baier J, Ingham L, McCarty D, Hannah LC. De novo synthesis of an intron by the maize transposable element Dissociation. Proc Natl Acad Sci USA. 91:1994;12150-12154.
70. Purugganan M, Wessler S. The splicing of transposable elements and their role in intron evolution. Genetica. 86:1992;295-303.
71. of outstanding interest Tarrio R, Rodriguez-Trelles F, Ayala FJ. New Drosophila introns originate by duplication. of special interest Proc Natl Acad Sci USA. 95:1998;1658-1662 A clear example of recent spliceosomal intron gains along with possible identification of their source. Three newly-inserted introns were identified in the xanthine dehydrogenase (Xdh) genes of dipteran insects. Evidence is presented that the source of these new introns is another intron, conserved in position, in the Xdh gene. Unfortunately, homology between the 'source' Xdh intron and the new introns, all of which were very AT-rich, could not be verified independently [68].
72. O'Neill RJ, Brennan FE, Delbridge ML, Crozier RH, Graves JA. De novo insertion of an intron into the mammalian sex determining gene, SRY. Proc Natl Acad Sci USA. 95:1998;1653-1657.
73. Frugoli JA, McPeek MA, Thomas TL, McClung CR. Intron loss and gain during evolution of the catalase gene family in angiosperms. of outstanding interest Genetics. 149:1998;355-365 A clear analysis of intron evolution in the catalase gene family of angiosperms. Catalase gene structures were determined from both Arabidopsis and Hordeum and compared to available sequences from databases. Eight intron positions are present in angiosperm catalase genes, one of which is uniquely present in Oryza, making it a likely recent intron gain. By mapping intron positions on a catalase gene phylogeny, a reasonable model for intron gain and loss was inferred. One case of multiple, non-independent loss of the five adjacent introns could be identified and is attributed to cDNA-mediated recombination.
74. Fedorov A, Suboch G, Bujakov M, Fedorova L. Analysis of nonuniformity in intron phase distribution. Nucleic Acids Res. 20:1992;2553-2557.
75. Long M, de Souza SJ, Rosenberg C, Gilbert W. Relationship between 'proto-splice sites' and intron phases: evidence from dicodon analysis. of outstanding interest Proc Natl Acad Sci USA. 95:1998;219-223 Can observed biases in the distribution of intron phases be explained by similar biases in presumed sites of intron insertion? Using a sizable database of gene sequences from the 'model' eukaryotic species, this question was addressed. The authors determined the distribution of intron phases in each organism and compared these to the distribution of phases occupied by inferred proto-splice sites. The authors demonstrate that the phase distributions from inferred proto-splice sites do not match the observed phases. Yet, it is clear that both sets of data have the same directional tendency, a result the authors do not consider. Although these results might indicate that phase correlations are the result of insertional bias(es), they are instead taken to support the IE view that intronphase distributions are caused by exon shuffling.
76. Madhani HD, Guthrie C. A novel base-pairing interaction between U2 and U6 snRNAs suggests a mechanism for the catalytic activation of the spliceosome. Cell. 71:1992;803-817.
77. Padgett RA, Podar M, Boulanger SC, Perlman PS. The stereochemical course of group II intron self-splicing. Science. 266:1994;1685-1688.
78. Gaur RK, McLaughlin LW, Green MR. Functional group substitutions of the branchpoint adenosine in a nuclear pre-mRNA and a group II intron. RNA. 3:1997;861-869.
79. Hetzer M, Wurzer G, Schweyen RJ, Mueller MW. Trans-activation of group II intron splicing by nuclear U5 snRNA. of outstanding interest Nature. 386:1997;417-420 An exciting experimental confirmation of the relationship between group II introns and the spliceosome. In an in vitro study of group II intron splicing, the ID3 subdomain - thought to be analogous to U5 snRNA - was deleted; this caused a significant reduction in the second step of splicing. The activity was restored by adding a U5 snRNA fragment in trans, thus providing further support for a group II 'introns in pieces' view of the spliceosome.
80. Keeling PJ. A kingdom's progress: Archezoa and the origin of eukaryotes. Bioessays. 20:1998;87-95.
81. Ferat JL, Michel F. Group II self-splicing introns in bacteria. Nature. 364:1994;358-361.
82. Michel F, Ferat JL. Structure and activities of group II introns. Annu Rev Biochem. 64:1995;435-461.
83. Mullany P, Pallen M, Wilks M, Stephen JR, Tabaqchali S. A group II intron in a conjugative transposon from the gram-positive bacterium, Clostridium difficile. Gene. 174:1996;145-150.
84. Mills DA, Manias DA, McKay LL, Dunny GM. Homing of a group II intron from Lactococcus lactis subsp. lactis ML3. J Bacteriol. 179:1997;6107-6111.
85. Yeo CC, Tham JM, Yap MW, Poh CL. Group II intron from Pseudomonas alcaligenes NCIB 9867 (P25X): entrapment in plasmid RP4 and sequence analysis. Microbiology. 143:1997;2833-2840.
86. Martinez-Abarca F, Zekri S, Toro N. Characterization and splicing in vivo of a Sinorhizobium meliloti group II intron associated with particular insertion sequences of the IS630-Tc1/IS3 retroposon superfamily. Mol Microbiol. 28:1998;1295-1306.
87. Roger AJ, Doolittle WF. Why introns-in-pieces? Nature. 364:1993;289-290.
88. Cousineau B, Smith D, Lawrence-Cavanagh S, Mueller JE, Yang J, Mills D, Manias D, Dunny G, Lambowitz AM, Belfort M. Retrohoming of a bacterial group II intron: mobility via complete reverse splicing, independent of homologous DNA. of special interest Cell. 94:1998;451-462 Demonstrates that the mobility of a group II intron in Lactococcus lactis - and the same intron placed in E. coli - occurs by the reversal of self-splicing. Evidence favoring intron insertion via reverse splicing include relaxed flanking exon sequence requirements, absence of marker co-conversion and independence of RecA function. This provides strong evidence for the veracity of group II reverse-splicing as a mechanism for intron insertion.
89. Doolittle WF. You are what you eat: a gene transfer ratchet could account for bacterial genes in eukaryotic nuclear genomes. Trends Genet. 14:1998;307-311.
90. Eskes R, Yang J, Lambowitz AM, Perlman PS. Mobility of yeast mitochondrial group II introns: engineering a new site specificity and retrohoming via full reverse splicing. Cell. 88:1997;865-874.
91. Takahashi Y, Tani T, Ohshima Y. Spliceosomal introns in conserved sequences of U1 and U5 small nuclear RNA genes in yeast Rhodotorula hasegawae. J Biochem (Tokyo). 120:1996;677-683.
92. Trotman CN. Introns-early: slipping lately? of special interest Trends Genet. 14:1998;132-134 A recent review starting from a decidedly IE perspective with its main focus on intron evolution in globins. After summarizing recent papers, most of which clearly support the IL theory, the author suggests that IE and IL views are not mutually exclusive. He claims that with introns being gained and lost, "truly primoridal introns" would be very difficult to identify.