Intron biology, focusing on group II introns, the ancestors of spliceosomal introns

Genomic Elements in Health, Disease and Evolution: Junk DNA

Volumn , Issue , 2015, Pages 195-219

  Molina Sánchez, María Dolores ^a   Nisa Martínez, Rafael ^a   García Rodríguez, Fernando M ^a   Martínez Abarca, Francisco ^a   Toro, Nicolás ^a  

^a CSIC   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84955410008     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-1-4939-3070-8_8     Document Type: Chapter

References (181)

1. Sharp PA (1991) Five easy pieces. Science 254:663
2. Martin W, Koonin EV (2006) Introns and the origin of nucleus-cytosol compartmentalization. Nature 440:41-45
3. Capy P, Vitalis R, Langin T, Higuet D, Bazin C (1996) Relationships between transposable elements based upon the integrase-transposase domains: is there a common ancestor? J Mol Evol 42:359-368
4. Simon DM, Kelchner SA, Zimmerly S (2009) A broadscale phylogenetic analysis of group II intron RNAs and intron-encoded reverse transcriptases. Mol Biol Evol 26:2795-2808
5. Doolittle WF (2014) The trouble with (group II) introns. Proc Natl Acad Sci U S A 111:6536-6537
6. Michel F, Jacquier A, Dujon B (1982) Comparison of fungal mitochondrial introns reveals extensive homologies in RNA secondary structure. Biochimie 64:867-881
7. Qin PZ, Pyle AM (1998) The architectural organization and mechanistic function of group II intron structural elements. Curr Opinion Struct Biol 8:301-308
8. Lambowitz AM, Zimmerly S (2010) Group II introns: mobile ribozymes that invade DNA. Cold Spring Harb Perspect Biol 3:a003616. doi: 10.1101/cshperspect.a003616
9. Lehmann K, Schmidt U (2003) Group II introns: structure and catalytic versatility of large natural ribozymes. Crit Rev Biochem Mol Biol 38:249-303
10. Michel F, Umesono K, Ozeki H (1989) Comparative and functional anatomy of group II catalytic introns--a review. Gene 82:5-30
11. Michel F, Ferat JL (1995) Structure and activities of group II introns. Ann Rev Biochem 64:435-461
12. Lambowitz AM, Zimmerly S (2004) Mobile group II introns. Ann Rev Genet 38:1-35
13. Marcia M, Pyle AM (2014) Principles of ion recognition in RNA: insights from the group II intron structures. RNA 20:516-527
14. Dai L, Chai D, Gu SQ, Gabel J, Noskov SY, Blocker FJ et al (2008) A three-dimensional model of a group II intron RNA and its interaction with the intron-encoded reverse transcriptase. Mol Cell 30:472-485
15. Pyle AM (2010) The tertiary structure of group II introns: implications for biological function and evolution. Crit Rev Biochem Mol Biol 45:215-232
16. Toor N, Keating KS, Fedorova O, Rajashankar K, Wang J, Pyle AM (2010) Tertiary architecture of the Oceanobacillus iheyensis group II intron. RNA 16:57-69
17. Pyle AM (2002) Metal ions in the structure and function of RNA. J Biol Inorg Chem 7:679-690
18. Toor N, Keating KS, Pyle AM (2009) Structural insights into RNA splicing. Curr Opinion Struct Biol 19:260-266
19. de Lencastre A, Hamill S, Pyle AM (2005) A single active-site region for a group II intron. Nat Struct Mol Biol 12:626-627
20. de Lencastre A, Pyle AM (2008) Three essential and conserved regions of the group II intron are proximal to the 5'-splice site. RNA 14:11-24
21. Robart AR, Seo W, Zimmerly S (2007) Insertion of group II intron retroelements after intrinsic transcriptional terminators. Proc Natl Acad Sci U S A 104:6620-6625
22. Toor N, Hausner G, Zimmerly S (2001) Coevolution of group II intron RNA structures with their intron-encoded reverser transcriptases. RNA 7:1142-1152
23. Zimmerly S, Hausner G, Wu X (2001) Phylogenetic relationships among group II intron ORFs. Nucleic Acids Res 29:1238-1250
24. Blocker FJ, Mohr G, Conlan LH, Qi L, Belfort M, Lambowitz AM (2005) Domain structure and three-dimensional model of a group II intron-encoded reverse transcriptase. RNA 11:14-28
25. Molina-Sánchez MD, Martínez-Abarca F, Toro N (2010) Structural features in the C-terminal region of the Sinorhizobium meliloti RmInt1 group II intron-encoded protein contribute to its maturase and intron DNA-insertion function. FEBS J 277:244-254
26. Toro N, Martínez-Abarca F (2013) Comprehensive phylogenetic analysis of bacterial group II intron-encoded ORFs lacking the DNA endonuclease domain reveals new varieties. PLoS One 8:e55102
27. Toro N (2003) Bacteria and Archaea Group II introns: additional mobile genetic elements in the environment. Environ Microbiol 5:143-151
28. Pyle AM, Lambowitz AM (2006) Group II introns: ribozymes that splice RNA and invade DNA. In: Getsland RF, Cech TR, Atkins JF (eds) RNA World, 3rd edn. Cold Spring Harbor Laboratory Press, New York, pp 469-505
29. Robart AR, Zimmerly S (2005) Group II intron retroelements: function and diversity. Cytogenet Genome Res 110:589-597
30. Fedorova O, Zingler N (2007) Group II introns: structure, folding and splicing mechanism. Biol Chem 388:665-678
31. Solem A, Zingler N, Pyle AM, Li-Pook-Than J (2009) Group II introns and their protein collaborators. In: Walter NG, Woodson SA, Batey RT (eds) Non-protein coding RNAs. Springer, Berlin/Heidelberg, pp 167-182
32. Toro N, Jiménez-Zurdo JI, García-Rodríguez FM (2007) Bacterial group II introns: not just splicing. FEMS Microbiol Rev 31:342-358
33. Daniels D, Michels WJ, Pyle AM (1996) Two competing pathways for self-splicing by group II introns; a quantitative analysis of in vitro reaction rates and products. J Mol Biol 256:31-49
34. Costa M, Michel F, Molina-Sanchez MD, Martinez-Abarca F, Toro N (2006) An alternative intron-exon pairing scheme implied by unexpected in vitro activities of group II intron RmInt1 from Sinorhizobium meliloti . Biochimie 88:711-717
35. Molina-Sánchez MD, Martínez-Abarca F, Toro N (2006) Excision of the Sinorhizobium meliloti group II intron RmInt1 as circles in vivo . J Biol Chem 281:28737-28744
36. Nagy V, Pirakitikulr N, Zhou KI, Chillón I, Luo J, Pyle AM (2013) Predicted group II intron lineages E and F comprise catalytically active ribozymes. RNA 19:1266-1278
37. Granlund M, Michel F, Norgren M (2001) Mutually exclusive distribution of IS1548 and GBSi1, an active group II intron identified in human isolates of group B streptococci. J Bacteriol 183:2560-2569
38. Vogel J, Börner T (2002) Lariat formation and a hydrolytic pathway in plant chloroplast group II intron splicing. EMBO J 21:3794-3803
39. Toor N, Robart AR, Christianson J, Zimmerly S (2006) Self-splicing of a group IIC intron:50 exon recognition and alternative 50 splicing events implicate the stem-loop motif of a transcriptional terminator. Nucleic Acids Res 34:6561-6573
40. Marcia M, Somarowthu S, Pyle AM (2013) Now on display: a gallery of group II intron structures at different stages of catalysis. Mob DNA 4:14
41. Kruschel D, Skilandat M, Sigel RKO (2014) NMR structure of the 5' splice site in the group IIB intron Sc.ai5γ-conformational requirements for exon-intron recognition. RNA 20:295-307
42. Peebles CL, Perlman PS, Mecklenburg KL, Petrillo ML, Tabor JH, Jarrell KA, Cheng HL (1986) A self-splicing RNA excises an intron lariat. Cell 44:213-223
43. van der Veen R, Arnberg AC, van der Horst G, Bonen L, Tabak HF, Grivell LA (1986) Excised group II introns in yeast mitochondria are lariats and can be formed by self-splicing in vitro . Cell 44:225-234
44. van der Veen R, Kwakman JH, Grivell LA (1987) Mutations at the lariat acceptor site allow self-splicing of a group II intron without lariat formation. EMBO J 6:3827-3831
45. Jarrell KA, Peebles CL, Dietrich RC, Romiti SL, Perlman PS (1988) Group II intron selfsplicing:alternative reaction conditions yield novel products. J Biol Chem 263:3432-3439
46. Podar M, Chu VT, Pyle AM, Perlman PS (1998) Group II intron splicing in vivo by first-step hydrolysis. Nature 391:915-918
47. Chin K, Pyle AM (1995) Branch-point attack in group II introns is a highly reversible transesterification, providing a potential proofreading mechanism for 5'-splice site selection. RNA 1:391-406
48. Chu VT, Liu Q, Podar M, Perlman PS, Pyle AM (1998) More than one way to splice an RNA:branching without a bulge and splicing without branching in group II introns. RNA 4:1186-1202
49. Murray HL, Mikheeva S, Coljee VW, Turczyk BM, Donahue WF, Bar-Shalom A, Jarrel KA (2001) Excision of group II introns as circles. Mol Cell 8:201-211
50. Li-Pook-Than J, Bonen L (2006) Multiple physical forms of excised group II intron RNAs in wheat mitochondria. Nucleic Acids Res 34:2782-2790
51. Chee GJ, Takami H (2011) Alternative splicing by participation of the group II intron ORF in extremely halotolerant and alkaliphilic Oceanobacillus iheyensis . Microbes Environ 26:54-60
52. Molina-Sánchez MD, Barrientos-Durán A, Toro N (2011) Relevance of the branch point adenosine, coordination loop, and 3' exon binding site for in vivo excision of the Sinorhizobium meliloti group II intron RmInt1. J Biol Chem 286:21154-21163
53. Dalby SJ, Bonen L (2013) Impact of low temperature on splicing of atypical group II introns in wheat mitochondria. Mitochondrion 13:647-655
54. Barrientos-Durán A, Chillón I, Martínez-Abarca F, Toro N (2011) Exon sequence requirements for excision in vivo of the bacterial group II intron RmInt1. BMC Mol Biol 12:24. doi: 10.1186/1471-2199-12-24
55. Costa M, Michel F, Westhof E (2000) A three-dimensional perspective on exon binding by a group II self-splicing intron. EMBO J 19:5007-5018
56. Hamill S, Pyle AM (2006) The receptor for branch-site docking within a group II intron active site. Mol Cell 23:831-840
57. Su L, Qin P, Michels W, Pyle A (2001) Guiding ribozyme cleavage through motif recognition:the mechanism of cleavage site selection by a group II intron ribozyme. J Mol Biol 306:665-668
58. Bonen L (2008) Cis - and trans -splicing of group II introns in plant mitochondria. Mitochondrion 8:26-34
59. Glanz S, Kück U (2009) Trans -splicing of organelle introns - a detour to continuous RNAs. Bioessays 31:921-934
60. Copertino DW, Hallick RB (1993) Group II and group III introns of twintrons: potential relationship with nuclear pre-mRNA introns. Trends Biochem Sci 18:467-471
61. Jenkins K, Hong L, Hallick R (1995) Alternative splicing of the Euglena gracilis chloroplast roa A transcript. RNA 1:624-633
62. Robart AR, Montgomery NK, Smith KL, Zimmerly S (2004) Principles of 3' splice site selection and alternative splicing for an unusual group II intron from Bacillus anthracis . RNA 10:854-862
63. Costa M, Michel F, Toro N (2006) Potential for alternative intron-exon pairings in group II intron RmInt1 from Sinorhizobium meliloti and its relatives. RNA 12:338-341
64. McNeil BA, Simon DM, Zimmerly S (2014) Alternative splicing of a group II intron in a surface layer protein gene in Clostridium tetani . Nucleic Acids Res 42:1959-1969
65. Brown GG, Colas des Francs-Small C, Ostersetzer-Biran O (2014) Group II intron splicing factors in plant mitochondria. Front Plant Sci 5:35. doi: 10.3389/fpls.2014.00035
66. Matsuura M, Saldanha R, Ma H, Wank H, Yang J, Mohr G et al (1997) A bacterial group II intron encoding reverse transcriptase, maturase, and DNA endonuclease activities: biochemi- cal demonstration of maturase activity and insertion of new genetic information within the intron. Genes Dev 11:2910-2924
67. Saldanha R, Chen B, Wank H, Matsuura M, Edwards J, Lambowitz AM (1999) RNA and protein catalysis in group II intron splicing and mobility reactions using purified components. Biochemistry 38:9069-9083
68. Cui X, Matsuura M, Wang Q, Ma H, Lambowitz AM (2004) A group II intron-encoded maturase functions preferentially in cis and requires both the reverse transcriptase and X domains to promote RNA splicing. J Mol Biol 340:211-231
69. Nisa-Martínez R, Jiménez-Zurdo JI, Martínez-Abarca F, Muñoz-Adelantado E, Toro N (2007) Dispersion of the RmInt1 group II intron in the Sinorhizobium meliloti genome upon acquisition by conjugative transfer. Nucleic Acids Res 35:214-222
70. Wahleithner JA, MacFarlane JL, Wolstenholme DR (1990) A sequence encoding a maturaserelated protein in a group II intron of a plant mitochondrial nad 1 gene. Proc Natl Acad Sci U S A 87:548-552. doi: 10.1073/pnas.87.2.548
71. Zoschke R, Nakamura M, Liere K, Sugiura M, Börner T, Schmitz-Linneweber C (2010) An organellar maturase associates with multiple group II introns. Proc Natl Acad Sci U S A 107:3245-3250. doi: 10.1073/pnas.0909400107
72. Nakagawa N, Sakurai N (2006) A mutation in At - nMat1a , which encodes a nuclear gene having high similarity to group II intron maturase, causes impaired splicing of mitochondrial nad 4 transcript and altered carbon metabolism in Arabidopsis thaliana . Plant Cell Physiol 47:772-783. doi: 10.1093/pcp/pcj051
73. Keren I, Bezawork-Geleta A, Kolton M, Maayan I, Belausov E, Levy M et al (2009) AtnMat2, a nuclear-encoded maturase required for splicing of group-II introns in Arabidopsis mitochondria. RNA 15:2299-2311. doi: 10.1261/rna.1776409
74. Cohen S, Zmudjak M, Colas des Francs-Small C, Malik S, Shaya F, Keren I et al (2014) nMAT4, a maturase factor required for nad 1 pre-mRNA processing and maturation, is essential for holocomplex I biogenesis in Arabidopsis mitochondria. Plant J 78:253-268
75. Guo W, Mower J (2013) Evolution of plant mitochondrial intron-encoded maturases: frequent lineage-specific loss and recurrent intracellular transfer to the nucleus. J Mol Evol 77:43-54. doi: 10.1007/s00239-013-9579-7
76. de Longevialle AF, Small ID, Lurin C (2010) Nuclearly encoded splicing factors implicated in RNA splicing in higher plant organelles. Mol Plant 3:691-705. doi: 10.1093/mp/ssq025
77. Huang HR, Rowe CE, Mohr S, Jiang Y, Lambowitz AM, Perlman PS (2005) The splicing of yeast mitochondrial group I and group II introns requires a DEAD-box protein with RNA chaperone function. Proc Natl Acad Sci U S A 102:163-168
78. Halls C, Mohr S, del Campo M, Yang Q, Jankowsky E, Lambowitz AM (2007) Involvement of DEAD-box proteins in group I and group II intron splicing: biochemical characterization of Mss116p, ATP hydrolysis-dependent and -independent mechanisms, and general RNA chaperone activity. J Mol Biol 365:835-855
79. del Campo M, Mohr S, Jiang Y, Jia H, Jankowsky E, Lambowitz AM (2009) Unwinding by local strand separation is critical for the function of DEAD-box proteins as RNA chaperones. J Mol Biol 389:674-693
80. Köhler D, Schmidt-Gattung S, Binder S (2010) The DEAD-box protein PMH2 is required for efficient group II intron splicing in mitochondria of Arabidopsis thaliana . Plant Mol Biol 72:459-467. doi: 10.1007/s11103-009-9584-9
81. Jacobs J, Glanz S, Bunse-Graβmann A, Kruse O, Kück U (2010) RNA trans -splicing: identification of components of a putative chloroplast spliceosome. Eur J Cell Biol 89:932-939
82. Jacobs J, Marx C, Kock V, Reifschneider O, Fränzel B, Krisp C et al (2013) Identification of a chloroplast ribonucleoprotein complex containing trans -splicing factors, intron RNA, and novel components. Mol Cell Proteomics 12:1912-1925. doi: 10.1074/mcp.M112.026583
83. Enyeart PJ, Mohr G, Ellington AD, Lambowitz AM (2014) Biotechnological applications of mobile group II introns and their reverse transcriptases: gene targeting, RNA-seq, and noncoding RNA analysis. Mob DNA 5:2. doi: 10.1186/1759-8753-5-2
84. Skelly PJ, Hardy CM, Clark-Walker GD (1991) A mobile group II intron of a naturally occurring rearranged mitochondrial genome in Kluyveromyces lactis . Curr Genet 20:115-120
85. Lazowska J, Meunier B, Macadre C (1994) Homing of a group II intron in yeast mitochondrial DNA is accompanied by unidirectional co-conversion of upstream-located markers. EMBO J 13:4963-4972
86. Moran JV, Zimmerly S, Eskes R, Kennell JC, Lambowitz AM, Butow RA, Perlman PS (1995) Mobile group II introns of yeast mitochondrial DNA are novel site-specific retroelements. Mol Cell Biol 15:2828-2838
87. Mueller MW, Allmaier M, Eskes R, Schweyen RJ (1993) Transposition of group II intron aI1 in yeast and invasion of mitochondrial genes at new locations. Nature 366:174-176
88. Cousineau B, Lawrence S, Smith D, Belfort M (2000) Retrotransposition of a bacterial group II intron. Nature 404:1018-1021 (Erratum: Nature 2001;414:84)
89. Muñoz E, Villadas PJ, Toro N (2001) Ectopic transposition of a group II intron in natural bacterial populations. Mol Microbiol 41:645-652
90. Cousineau B, Smith D, Lawrence-Cavanagh S, Mueller JE, Yang J, Mills D et al (1998) Retrohoming of a bacterial group II intron: mobility via complete reverse splicing, independent of homologous DNA recombination. Cell 94:451-462
91. Martínez-Abarca F, Barrientos-Durán A, Fernández-López M, Toro N (2004) The RmInt1 group II intron has two different retrohoming pathways for mobility using predominantly the nascent lagging strand at DNA replication forks for priming. Nucleic Acids Res 32:2880-2888
92. Lambowitz AM, Mohr G, Zimmerly S (2005) Group II intron homing endonucleases: ribonucleoprotein complexes with programmable target specificity. In: Belfort M, Stoddard BL, Wood DW, Derbyshire V (eds) Homing endonucleases and inteins. Springer, Heidelberg, pp 121-145
93. Zimmerly S, Guo H, Perlman PS, Lambowitz AM (1995) Group II intron mobility occurs by target DNA-primed reverse transcription. Cell 82:545-554
94. Zimmerly S, Guo H, Eskes R, Yang J, Perlman PS, Lambowitz AM (1995) A group II intron RNA is a catalytic component of a DNA endonuclease involved in intron mobility. Cell 83:529-538
95. Yang J, Zimmerly S, Perlman PS, Lambowitz AM (1996) Efficient integration of an intron RNA into double-stranded DNA by reverse splicing. Nature 381:332-335
96. Eskes R, Yang J, Lambowitz AM, Perlman PS (1997) Mobility of yeast mitochondrial group II introns: engineering a new site specificity and retrohoming via full reverse splicing. Cell 88:865-874
97. Mills DA, Manias DA, McKay LL, Dunny GM (1997) Homing of a group II intron from Lactococcus lactis subsp. lactis ML3. J Bacteriol 179:6107-6111
98. Belfort M, Derbyshire V, Parker MM, Cousineau B, Lambowitz AM (2002) Mobile introns:pathways and proteins. In: Craig NL, Gragie R, Gellert M, Lambowitz AM (eds) Mobile DNA II. ASM Press, Washington, DC, pp 761-781
99. Mohr G, Smith D, Belfort M, Lambowitz AM (2000) Rules for DNA target-site recognition by a lactococcal group II intron enable retargeting of the intron to specific DNA sequences. Genes Dev 14:559-573
100. Singh NN, Lambowitz AM (2001) Interaction of a group II intron ribonucleoprotein endonuclease with its DNA target site investigated by DNA footprinting and modification interference. J Mol Biol 309:361-386
101. Singh RN, Saldanha RJ, D'Souza LM, Lambowitz AM (2002) Binding of a group II intronencoded reverse transcriptase/maturase to its high-affinity intron RNA binding site involves sequence-specific recognition and autoregulates translation. J Mol Biol 318:287-303
102. Yang J, Mohr G, Perlman PS, Lambowitz AM (1998) Group II intron mobility in yeast mitochondria:target DNA-primed reverse transcription activity of aI1 and reverse splicing into DNA transposition sites in vitro . J Mol Biol 282:505-523
103. Guo H, Zimmerly S, Perlman PS, Lambowitz AM (1997) Group II intron endonucleases use both RNA and protein subunits for recognition of specific sequences in double-stranded DNA. EMBO J 16:6835-6848
104. Jiménez-Zurdo JI, García-Rodríguez FM, Barrientos-Durán A, Toro N (2003) DNA target site requirements for homing in vivo of a bacterial group II intron encoding a protein lacking the DNA endonuclease domain. J Mol Biol 326:413-423
105. Zhuang F, Karberg M, Perutka J, Lambowitz AM (2009) EcI5, a group IIB intron with high retrohoming frequency: DNA target site recognition and use in gene targeting. RNA 15:432-449
106. Mohr G, Ghanem E, Lambowitz AM (2010) Mechanisms used for genomic proliferation by thermophilic group II introns. PLoS Biol 8:e1000391. doi: 10.1371/journal.pbio.1000391
107. Rodríguez-Martínez JM, Nordmann P, Poirel L (2012) Group IIC intron with an unusual target of integration in Enterobacter cloacae . J Bacteriol 194:150-160. doi: 10.1128/ JB.05786-11
108. Eskes R, Liu L, Ma H, Chao MY, Dickson L, Lambowitz AM, Perlman PS (2000) Multiple homing pathways used by yeast mitochondrial group II introns. Mol Cell Biol 20:8432-8446
109. Aizawa Y, Xiang Q, Lambowitz AM, Pyle AM (2003) The pathway of DNA recognition and RNA integration by a group II intron retrotransposon. Mol Cell 11:795-805
110. Guo H, Karberg M, Long M, Jones JP 3rd, Sullenger B, Lambowitz AM (2000) Group II introns designed to insert into therapeutically relevant DNA target sites in human cells. Science 289:452-457
111. Karberg M, Guo H, Zhong J, Coon R, Perutka J, Lambowitz AM (2001) Group II introns as controllable gene targeting vectors for genetic manipulation of bacteria. Nat Biotechnol 19:1162-1167
112. Muñoz-Adelantado E, San Filippo J, Martínez-Abarca F, García-Rodríguez FM, Lambowitz AM, Toro N (2003) Mobility of the Sinorhizobium meliloti group II intron RmInt1 occurs by reverse splicing into DNA, but requires an unknown reverse transcriptase priming mechanism. J Mol Biol 327:931-943
113. Zhong J, Lambowitz AM (2003) Group II intron mobility using nascent strands at DNA replication forks to prime reverse transcription. EMBO J 22:4555-4565
114. Ichiyanagi K, Beauregard A, Lawrence S, Smith D, Cousineau B, Belfort M (2002) Multiple pathways for the Ll.LtrB group II intron include reverse splicing into DNA targets. Mol Microbiol 46:1259-1271
115. Schäfer B, Gan L, Perlman PS (2003) Reverse transcriptase an reverse splicing activities encoded by the mobile group II intron COB I1 of fission yeast mitochondrial DNA. J Mol Biol 329:191-206
116. Centron D, Roy PH (2002) Presence of a group II intron in a multiresistant Serratia marcescens strain that harbors three integrons and a novel gene fusion. Antimicrob Agents Chemother 46:1402-1409
117. Dai L, Zimmerly S (2002) Compilation and analysis of group II intron insertions in bacterial genomes: evidence for retroelement behavior. Nucleic Acids Res 30:1091-1102
118. Léon G, Roy PH (2009) Group IIC intron mobility into attC sites involves a bulged DNA stem-loop motif. RNA 15:1543-1553
119. Dème E, Nolte A, Jacquier A (1999) Unexpected metal ion requirements specific for catalysis of the branching reaction in a group II intron. Biochemistry 38:3157-3167
120. Mohr S, Matsuura M, Perlman PS, Lambowitz AM (2006) 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 103:3569-3574
121. Gordon PM, Fong R, Piccirilli JA (2007) A second divalent metal ion in the group II intron reaction center. Chem Biol 14:607-612
122. Roitzsch M, Pyle AM (2009) The linear form of a group II intron catalyzes efficient autocatalytic reverse splicing, establishing a potential for mobility. RNA 15:473-482
123. Zhuang F, Mastroianni M, White TB, Lambowitz AM (2009) Linear group II intron RNAs can retrohome in eukaryotes and may use nonhomologous end-joining for cDNA ligation. Proc Natl Acad Sci U S A 106:18189-18194
124. White TB, Lambowitz AM (2012) The retrohoming of linear group II intron RNAs in Drosophila melanogaster occurs by both DNA ligase 4-dependent and -independent mechanisms. PLoS Genet 8:e1002534. doi: 10.1371/journal.pgen.1002534
125. Bowater R, Doherty AJ (2006) Making ends meet: repairing breaks in bacterial DNA by nonhomologous end-joining. PLoS Genet 2:e8. doi: 10.1371/journal.pgen.0020008
126. Martínez-Abarca F, Toro N (2000) RecA-independent ectopic transposition in vivo of a bacterial group II intron. Nucleic Acids Res 28:4397-4402
127. Dickson L, Huang HR, Liu L, Matsuura M, Lambowitz AM, Perlman PS (2001) Retrotransposition of a yeast group II intron occurs by reverse splicing directly into ectopic DNA sites. Proc Natl Acad Sci U S A 98:13207-13212
128. Ichiyanagi K, Beauregard A, Belfort M (2003) A bacterial group II intron favors retrotransposition into plasmid targets. Proc Natl Acad Sci U S A 100:15742-15747
129. Coros CJ, Landthaler M, Piazza CL, Beauregard A, Esposito D, Perutka J (2005) Retrotransposition strategies of the Lactococcus lactis Ll.LtrB group II intron are dictated by host identity and cellular environment. Mol Microbiol 56:509-524
130. Beauregard A, Chalamcharla VR, Piazza CL, Belfort M, Coros CJ (2006) Bipolar localization of the group II intron Ll.LtrB is maintained in Escherichia coli deficient in nucleoid condensation, chromosome partitioning and DNA replication. Mol Microbiol 62:709-722
131. Smith D, Zhong J, Matsuura M, Lambowitz AM, Belfort M (2005) Recruitment of host functions suggests a repair pathway for late steps in group II intron retrohoming. Genes Dev 19:2477-2487
132. Coros CJ, Piazza CL, Chalamcharla VR, Belfort M (2008) A mutant screen reveals RNase E as a silencer of group II intron retromobility in Escherichia coli . RNA 14:2634-2644
133. Beauregard A, Curcio MJ, Belfort M (2008) The take and give between retrotransposable elements and their hosts. Ann Rev Genet 42:587-617
134. Zhao J, Niu W, Marcotte E, Lambowitz A (2008) Group II intron protein localization and insertion sites are affected by polyphosphate. PLoS Biol 6:e150. doi: 10.1371/journal. pbio.0060150
135. Coros CJ, Piazza CL, Chalamcharla VR, Smith D, Belfort M (2009) Global regulators orchestrate group II intron retromobility. Mol Cell 34:250-256
136. Edgell DR, Chalamcharla VR, Belfort M (2011) Learning to live together: mutualism between self-splicing introns and host genomes. BMC Biol 9:22. doi: 10.1186/1741-7007-9-22
137. Yao J, Truong DM, Lambowitz AM (2013) Genetic and biochemical assays reveal a key role for replication restart proteins in group II intron retrohoming. PLoS Genet 9:e1003469. doi: 10.1371/journal.pgen.1003469
138. Perutka J, Wang W, Goerlitz D, Lambowitz AM (2004) Use of computer-designed group II introns to disrupt Escherichia coli DExH/D-box protein and DNA helicase genes. J Mol Biol 336:421-439
139. García-Rodríguez FM, Barrientos-Durán A, Díaz-Prado V, Fernández-López M, Toro N (2011) Use of RmInt1, a group IIB intron lacking the intron-encoded protein endonuclease domain, in gene targeting. Appl Environ Microbiol 77:854-861. doi: 10.1128/ AEM.02319-10
140. Mohr G, Hong W, Zhang J, Cui GZ, Yang Y, Cui Q et al (2013) A targetron system for gene targeting in thermophiles and its application in Clostridium thermocellum . PLoS One 8:e69032. doi: 10.1371/journal.pone.0069032
141. García-Rodríguez FM, Hernández-Gutiérrez T, Díaz-Prado V, Toro N (2014) Use of the computer- retargeted group II intron RmInt1 of Sinorhizobium meliloti for gene targeting. RNA Biol 11:391-401
142. Yao J, Lambowitz AM (2007) Gene targeting in gram-negative bacteria by use of a mobile group II intron ("targetron") expressed from a broad-host-range vector. Appl Environ Microbiol 73:2735-2743
143. Park JM, Jang YS, Kim TY, Lee SY (2010) Development of a gene knockout system for Ralstonia eutropha H16 based on the broad-host-range vector expressing a mobile group II intron. FEMS Microbiol Lett 309:193-200
144. Yao J, Zhong J, Fang Y, Geisinger E, Novick RP, Lambowitz AM (2006) Use of targetrons to disrupt essential and nonessential genes in Staphylococcus aureus reveals temperature sensitivity of Ll.LtrB group II intron splicing. RNA 12:1271-1281
145. Heap JT, Pennington OJ, Cartman ST, Carter GP, Minton NP (2007) The ClosTron: a universal gene knock-out system for the genus Clostridium . J Microbiol Methods 70:452-464
146. Rodriguez SA, Yu JJ, Davis G, Arulanandam BP, Klose KE (2008) Targeted inactivation of Francisella tularensis genes by group II introns. Appl Environ Microbiol 74:2619-2626
147. Zhong J, Karberg M, Lambowitz AM (2003) Targeted and random bacterial gene disruption using a group II intron (tagetron) vector containing a retrotransposition-activated selectable marker. Nucleic Acids Res 31:1656-1664
148. Malhotra M, Srivastava S (2008) An ipdC gene knock-out of Azospirillum brasilense strain SM and its implications on indole-3-acetic acid biosynthesis and plant growth promotion. Antonie Van Leeuwenhoek 93:425-433
149. Akhtar P, Hkan SA (2012) Two independent replicons can support replication of the anthrax toxin-encoding plasmid pXO1 of Bacillus anthracis . Plasmid 67:111-117
150. Cheng C, Nair AD, Indukuri W, Gong S, Felsheim RF, Jaworski D et al (2013) Targeted and random mutagenesis of Ehrlichia chaffeensis for the identification of genes required for in vivo infection. PLoS Pathog 9:e1003171. doi: 10.1371/journal.ppat.1003171
151. Frazier CL, San Filippo J, Lambowitz AM, Mills DA (2003) Genetic manipulation of Lactococcus lactis by using targeted group II introns: generation of stable insertions without selection. Appl Environ Microbiol 69:1121-1128
152. Alonzo F 3rd, Port GC, Cao M, Freitag NE (2009) The postranslocation chaperone PrsA2 contributes to multiple facets of Listeria monocytogenes pathogenesis. Infect Immun 77:3077-3085
153. Zarschler K, Janesch B, Zayni S, Schäffer C, Messner P (2009) Construction of a gene knockout system for application in Paenibacillus alvei CCM 2051 T, exemplified by the S-layer glycan biosynthesis initiation enzyme WsfP. Appl Environ Microbiol 75:3077-3085
154. Steen JA, Steen JA, Harrison P, Seemann T, Wilkie I, Harper M, Adler B, Boyce JD (2010) Fis is essential for capsule production in Pasteurella multocida and regulates expression of other important virulence factors. PLoS Pathog 6:e1000750. doi: 10.1371/journal.ppat.1000750
155. Pearson MM, Mobley HL (2007) The type III secretion system of Proteus mirabilis HI4320 does not contribute to virulence in the mouse model of ascending urinary tract infection. J Med Microbiol 56:1277-1283
156. Enyeart PJ, Chirieleison SM, Dao MN, Perutka J, Quandt EM, Yao J et al (2013) Generalized bacterial genome editing using mobile group II introns and Cre-lox. Mol Syst Biol 9:685. doi: 10.1038/msb.2013.41
157. Smith CL, Weiss BL, Aksoy S, Runyen-Janecky LJ (2013) Characterization of the achromobactin iron acquisition operon in Sodalis glossinidius . Appl Environ Microbiol 79:2872-2881
158. Kumar S, Smith KP, Floyd JL, Varela MF (2011) Cloning and molecular analysis of a mannitol operon of phosphoenolpyruvate-dependent phosphotransferase (PTS) type from Vibrio cholerae O395. Arch Microbiol 193:201-208
159. Palonen E, Lindstrom M, Karttunen R, Somervuo P, Korkeala H (2011) Expression of signal transduction system encoding genes of Yersinia pseudotuberculosis IP32953 at 28°C and 3°C. PLoS One 6:e25063. doi: 10.1371/journal.pone.0025063
160. Jones JP III, Kierlin MN, Coon RB, Perutka J, Lambowitz AM, Sullenger BA (2005) Retargeting mobile group II introns to repair mutant genes. Mol Ther 11:687-694
161. Rawsthorne H, Turner KN, Mills DA (2006) Multicopy integration of heterologous genes, using the lactococal group II intron targeted to bacterial insertion sequences. Appl Environ Microbiol 72:6088-6093
162. Plante I, Cousineau B (2006) Restriction for gene insertion within the Lactococcus lactis Ll.LtrB group II intron. RNA 12:1980-1992
163. Mastroianni M, Watanabe K, Whit TB, Zhuang F, Vernon J, Matsuura M, Wallingford J, Lambowitz AM (2008) Group II intron-based gene targeting reactions in eukaryotes. PLoS One 3:e3121. doi: 10.1371/journal.pone.0003121
164. Grabowski PJ, Seiler SA, Sharp PA (1985) A multicomponent complex is involved in the splicing of messenger RNA precursors. Cell 42:345-353
165. Cech TK (1986) The generality of self-splicing RNA: relationship to nuclear mRNA splicing. Cell 44:207-210
166. Patel AA, Steitz JA (2003) Splicing double: insights from the second spliceosome. Nat Rev Mol Cell Biol 4:960-970
167. Toor N, Keating KS, Taylor SD, Pyle AM (2008) Crystal structure of a self-spliced group II intron. Science 320:77-82
168. Keating KS, Toor N, Perlman PS, Pyle AM (2010) A structural analysis of the group II intron active site and implications for the spliceosome. RNA 16:1-9
169. Eickbush TH (1994) Origins and evolutionary relationships of retroelements. In: Morse SS (ed) The evolutionary biology of viruses. Raven, New York, pp 121-157
170. Rogozin IB, Carmel L, Csuros M, Koonin EV (2012) Origin and evolution of spliceosomal introns. Biol Direct 7:11. doi: 10.1186/1745-6150-7-11
171. Mohr G, Lambowitz AM (2003) Putative proteins related to group II intron reverse transcriptase/ maturases are encoded by nuclear genes in higher plants. Nucleic Acids Res 31:647-652
172. Koonin EV (2006) The origin of introns and the role in eukaryogenesis: a compromise solution to the introns-early versus introns-late debate? Biol Direct 1:22. doi: 10.1186/1745-6150-1-22
173. Koonin EV (2011) The origins of eukaryotes: endosymbiosis, the strange story of introns, and the ultimate importance of unique events in evolution. In: Pearson Education Inc. (ed) The logic of chance: the nature and origin of biological evolution, 1st edn. FT Press Science, Upper Saddle River, pp 171-224
174. Nisa-Martínez R, Laporte P, Jiménez-Zurdo JI, Frugier F, Crespi M, Toro N (2013) Localization of a bacterial group II intron-encoded protein in eukaryotic nuclear splicingrelated cell compartments. PLoS One 8(12):e84056. doi: 10.1371/journal.pone.0084056 , eCollection 2013
175. Spector DL, Lamond AI (2011) Nuclear speckles. Cold Spring Harb Perspect Biol 3:a000646. doi: 10.1101/cshperspect.a000646
176. Dai LX, Zimmerly S (2002) The dispersal of five group II introns among natural populations of Escherichia coli . RNA 8:1294-1307
177. Fernandez-Lopez M, Munoz-Adelantado E, Gillis M, Willems A, Toro N (2005) Dispersal and evolution of the Sinorhizobium meliloti group II RmInt1 intron in bacteria that interact with plants. Mol Biol Evol 22:1518-1528
178. Leclercq S, Cordaux R (2012) Selection-driven extinction dynamics for group II introns in Enterobacteriales. PLoS One 7:e52268
179. Simon DM, Clarke NA, McNeil BA, Johnson I, Pantuso D, Dai L et al (2008) Group II introns in eubacteria and archaea: ORF-less introns and new varieties. RNA 14:1704-1713
180. Chillón I, Martínez-Abarca F, Toro N (2010) Splicing of the Sinorhizobium meliloti RmInt1 group II intron provides evidence of retroelement behavior. Nucleic Acids Res 39:1095-1104
181. Toro N, Martínez-Rodríguez L, Martínez-Abarca F (2014) Insights into the history of a bacterial group II intron remnant from the genomes of the nitrogen-fixing symbionts Sinorhizobium meliloti and Sinorhizobium medicae . Heredity. doi:10.1038/hdy.2014.32