Evolution of plant mitochondrial intron-encoded maturases: Frequent lineage-specific loss and recurrent intracellular transfer to the nucleus

Journal of Molecular Evolution

Volumn 77, Issue 1-2, 2013, Pages 43-54

  Guo, Wenhu ^a,b   Mower, Jeffrey P ^a,c  

^a UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^b UNIVERSITY OF NEBRASKA   (United States)

^c UNIVERSITY OF NEBRASKA LINCOLN   (United States)

Author keywords

Intracellular transfer; Intron encoded proteins; Land plant genomes; Maturase genes; Splicing factors

Indexed keywords

BRYOPHYTA; EMBRYOPHYTA; LYCOPODIOPHYTA; MAGNOLIOPHYTA; PHYSCOMITRELLA PATENS; SELAGINELLA MOELLENDORFFII; VITACEAE; VITIS VINIFERA;

VEGETABLE PROTEIN;

ARTICLE; CLASSIFICATION; ENZYMOLOGY; GENETICS; INTRACELLULAR SPACE; INTRON; METABOLISM; MITOCHONDRIAL GENE; MITOCHONDRION; MOLECULAR EVOLUTION; MOLECULAR GENETICS; PHYLOGENY; PLANT; PROTEIN TRANSPORT;

EVOLUTION, MOLECULAR; GENES, MITOCHONDRIAL; INTRACELLULAR SPACE; INTRONS; MITOCHONDRIA; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLANT PROTEINS; PLANTS; PROTEIN TRANSPORT;

EID: 84883796852     PISSN: 00222844     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00239-013-9579-7     Document Type: Article

References (64)

1. Adams KL, Palmer JD (2003) Evolution of mitochondrial gene content: gene loss and transfer to the nucleus. Mol Phylogenet Evol 29:380-395
2. Banks JA, Nishiyama T, Hasebe M, Bowman JL, Gribskov M, dePamphilis C, Albert VA, Aono N, Aoyama T, Ambrose BA, Ashton NW, Axtell MJ, Barker E, Barker MS, Bennetzen JL, Bonawitz ND, Chapple C, Cheng C, Correa LG, Dacre M, DeBarry J, Dreyer I, Elias M, Engstrom EM, Estelle M, Feng L, Finet C, Floyd SK, Frommer WB, Fujita T, Gramzow L, Gutensohn M, Harholt J, Hattori M, Heyl A, Hirai T, Hiwatashi Y, Ishikawa M, Iwata M, Karol KG, Koehler B, Kolukisaoglu U, Kubo M, Kurata T, Lalonde S, Li K, Li Y, Litt A, Lyons E, Manning G, Maruyama T, Michael TP, Mikami K, Miyazaki S, Morinaga S, Murata T, Mueller-Roeber B, Nelson DR, Obara M, Oguri Y, Olmstead RG, Onodera N, Petersen BL, Pils B, Prigge M, Rensing SA, Riano-Pachon DM, Roberts AW, Sato Y, Scheller HV, Schulz B, Schulz C, Shakirov EV, Shibagaki N, Shinohara N, Shippen DE, Sorensen I, Sotooka R, Sugimoto N, Sugita M, Sumikawa N, Tanurdzic M, Theissen G, Ulvskov P, Wakazuki S, Weng JK, Willats WW, Wipf D, Wolf PG, Yang L, Zimmer AD, Zhu Q, Mitros T, Hellsten U, Loque D, Otillar R, Salamov A, Schmutz J, Shapiro H, Lindquist E, Lucas S, Rokhsar D, Grigoriev IV (2011) The Selaginella genome identifies genetic changes associated with the evolution of vascular plants. Science 332:960-963
3. Boer PH, Gray MW (1988) Genes encoding a subunit of respiratory NADH dehydrogenase (ND1) and a reverse transcriptase-like protein (RTL) are linked to ribosomal RNA gene pieces in Chlamydomonas reinhardtii mitochondrial DNA. EMBO J 7:3501-3508
4. Bonen L (2011) RNA splicing in plant mitochondria. In: Kempken F (ed) Plant mitochondria. Springer, New York, pp 131-155
5. Caprara MG, Waring RB (2005) Group I introns and their maturases: uninvited, but welcome guests. In: Belfort M, Wood D, Stoddard B, Derbyshire V (eds) Homing endonucleases and inteins. Springer, Berlin, Heidelberg, pp 103-119
6. Chaw SM, Shih AC, Wang D, Wu YW, Liu SM, Chou TY (2008) The mitochondrial genome of the gymnosperm Cycas taitungensis contains a novel family of short interspersed elements, Bpu sequences, and abundant RNA-editing sites. Mol Biol Evol 25:603-615
7. Dai L, Toor N, Olson R, Keeping A, Zimmerly S (2003) Database for mobile group II introns. Nucleic Acids Res 31:424-426
8. 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
9. Delannoy E, Fujii S, Colas des Francs-Small C, Brundrett M, Small I (2011) Rampant gene loss in the underground orchid Rhizanthella gardneri highlights evolutionary constraints on plastid genomes. Mol Biol Evol 28:2077-2086
10. Dombrovska O, Qiu Y-L (2004) Distribution of introns in the mitochondrial gene nad1 in land plants: phylogenetic and molecular evolutionary implications. Mol Phylogenet Evol 32:246-263
11. Duff RJ (2006) Divergent RNA editing frequencies in hornwort mitochondrial nad5 sequences. Gene 366:285-291
12. Duffy AM, Kelchner SA, Wolf PG (2009) Conservation of selection on matK following an ancient loss of its flanking intron. Gene 438:17-25
13. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792-1797
14. Funk HT, Berg S, Krupinska K, Maier UG, Krause K (2007) Complete DNA sequences of the plastid genomes of two parasitic flowering plant species, Cuscuta reflexa and Cuscuta gronovii. BMC Plant Biol 7:45
15. Germain A, Hotto AM, Barkan A, Stern DB (2013) RNA processing and decay in plastids. Wiley Interdiscip Rev RNA 4:295
16. Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD, Fazo J, Mitros T, Dirks W, Hellsten U, Putnam N, Rokhsar DS (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 40:D1178-D1186
17. Goremykin VV, Salamini F, Velasco R, Viola R (2009) Mitochondrial DNA of Vitis vinifera and the issue of rampant horizontal gene transfer. Mol Biol Evol 26:99-110
18. Grewe F, Herres S, Viehöver P, Polsakiewicz M, Weisshaar B, Knoop V (2011) A unique transcriptome: 1782 positions of RNA editing alter 1406 codon identities in mitochondrial mRNAs of the lycophyte Isoetes engelmannii. Nucleic Acids Res 39:2890-2902
19. Groth-Malonek M, Wahrmund U, Polsakiewicz M, Knoop V (2007) Evolution of a pseudogene: exclusive survival of a functional mitochondrial nad7 gene supports Haplomitrium as the earliest liverwort lineage and proposes a secondary loss of RNA editing in Marchantiidae. Mol Biol Evol 24:1068-1074
20. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307-321
21. Hausner G (2012) Introns, mobile elements, and plasmids. In: Bullerwell CE (ed) Organelle genetics. Springer, Berlin Heidelberg, pp 329-357
22. Hausner G, Olson R, Simon D, Johnson I, Sanders ER, Karol KG, McCourt RM, Zimmerly S (2006) Origin and evolution of the chloroplast trnK (matK) intron: a model for evolution of group II intron RNA structures. Mol Biol Evol 23:380-391
23. Hecht J, Grewe F, Knoop V (2011) Extreme RNA editing in coding islands and abundant microsatellites in repeat sequences of Selaginella moellendorffii mitochondria: the root of frequent plant mtDNA recombination in early tracheophytes. Genome Biol Evol 3:344-358
24. Iorizzo M, Senalik D, Szklarczyk M, Grzebelus D, Spooner D, Simon P (2012) De novo assembly of the carrot mitochondrial genome using next generation sequencing of whole genomic DNA provides first evidence of DNA transfer into an angiosperm plastid genome. BMC Plant Biol 12:61
25. Jaillon O, Aury JM, Noel B, Policriti A, Clepet C, Casagrande A, Choisne N, Aubourg S, Vitulo N, Jubin C, Vezzi A, Legeai F, Hugueney P, Dasilva C, Horner D, Mica E, Jublot D, Poulain J, Bruyere C, Billault A, Segurens B, Gouyvenoux M, Ugarte E, Cattonaro F, Anthouard V, Vico V, Del Fabbro C, Alaux M, Di Gaspero G, Dumas V, Felice N, Paillard S, Juman I, Moroldo M, Scalabrin S, Canaguier A, Le Clainche I, Malacrida G, Durand E, Pesole G, Laucou V, Chatelet P, Merdinoglu D, Delledonne M, Pezzotti M, Lecharny A, Scarpelli C, Artiguenave F, Pe ME, Valle G, Morgante M, Caboche M, Adam-Blondon AF, Weissenbach J, Quetier F, Wincker P (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449:463-467
26. Keren I, Bezawork-Geleta A, Kolton M, Maayan I, Belausov E, Levy M, Mett A, Gidoni D, Shaya F, Ostersetzer-Biran O (2009) AtnMat2, a nuclear-encoded maturase required for splicing of group-II introns in Arabidopsis mitochondria. RNA 15:2299-2311
27. Keren I, Tal L, des Francs-Small CC, Araujo WL, Shevtsov S, Shaya F, Fernie AR, Small I, Ostersetzer-Biran O (2012) nMAT1, a nuclear-encoded maturase involved in the trans-splicing of nad1 intron 1, is essential for mitochondrial complex I assembly and function. Plant J 71:413-426
28. Krause K (2011) Piecing together the puzzle of parasitic plant plastome evolution. Planta 234:647-656
29. Lambowitz AM, Zimmerly S (2011) Group II introns: mobile ribozymes that invade DNA. Cold Spring Harb Perspect Biol 3:a003616
30. Laroche J, Bousquet J (1999) Evolution of the mitochondrial rps3 intron in perennial and annual angiosperms and homology to nad5 intron 1. Mol Biol Evol 16:441-452
31. Li L, Wang B, Liu Y, Qiu YL (2009) The complete mitochondrial genome sequence of the hornwort Megaceros aenigmaticus shows a mixed mode of conservative yet dynamic evolution in early land plant mitochondrial genomes. J Mol Evol 68:665-678
32. Liu Y, Xue JY, Wang B, Li L, Qiu YL (2011) The mitochondrial genomes of the early land plants Treubia lacunosa and Anomodon rugelii: dynamic and conservative evolution. PLoS ONE 6:e25836
33. Liu Y, Wang B, Cui P, Li L, Xue JY, Yu J, Qiu YL (2012) The mitochondrial genome of the lycophyte Huperzia squarrosa: the most archaic form in vascular plants. PLoS ONE 7:e35168
34. Martin W, Herrmann RG (1998) Gene transfer from organelles to the nucleus: how much, what happens, and why? Plant Physiol 118:9-17
35. McNeal JR, Kuehl JV, Boore JL, Leebens-Mack J, dePamphilis CW (2009) Parallel loss of plastid introns and their maturase in the genus Cuscuta. PLoS ONE 4:e5982
36. Meng Q, Wang Y, Liu XQ (2005) An intron-encoded protein assists RNA splicing of multiple similar introns of different bacterial genes. J Biol Chem 280:35085-35088
37. 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
38. Mower JP, Jain K, Hepburn NJ (2012a) The role of horizontal transfer in shaping the plant mitochondrial genome. In: Laurence M-D (ed) Advances in botanical research. Academic Press, New York, pp 41-69
39. Mower JP, Sloan DB, Alverson AJ (2012b) Plant mitochondrial genome diversity: the genomics revolution. In: Wendel JF, Greilhuber J, Dolezel J, Leitch IJ (eds) Plant genome diversity volume 1: plant genomes, their residents, and their evolutionary dynamics. Springer, Vienna, pp 123-144
40. 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 NAD4 transcript and altered carbon metabolism in Arabidopsis thaliana. Plant Cell Physiol 47:772-783
41. Oda K, Yamato K, Ohta E, Nakamura Y, Takemura M, Nozato N, Akashi K, Kanegae T, Ogura Y, Kohchi T et al (1992) Gene organization deduced from the complete sequence of liverwort Marchantia polymorpha mitochondrial DNA. A primitive form of plant mitochondrial genome. J Mol Biol 223:1-7
42. Ohyama K, Takemura M (2008) Molecular evolution of mitochondrial introns in the liverwort Marchantia polymorpha. Proc Jpn Acad Ser B 84:17-23
43. Pombert JF, Otis C, Lemieux C, Turmel M (2005) The chloroplast genome sequence of the green alga Pseudendoclonium akinetum (Ulvophyceae) reveals unusual structural features and new insights into the branching order of chlorophyte lineages. Mol Biol Evol 22:1903-1918
44. Pombert JF, Beauchamp P, Otis C, Lemieux C, Turmel M (2006) The complete mitochondrial DNA sequence of the green alga Oltmannsiellopsis viridis: evolutionary trends of the mitochondrial genome in the Ulvophyceae. Curr Genet 50:137-147
45. Rensing SA, Lang D, Zimmer AD, Terry A, Salamov A, Shapiro H, Nishiyama T, Perroud PF, Lindquist EA, Kamisugi Y, Tanahashi T, Sakakibara K, Fujita T, Oishi K, Shin IT, Kuroki Y, Toyoda A, Suzuki Y, Hashimoto S, Yamaguchi K, Sugano S, Kohara Y, Fujiyama A, Anterola A, Aoki S, Ashton N, Barbazuk WB, Barker E, Bennetzen JL, Blankenship R, Cho SH, Dutcher SK, Estelle M, Fawcett JA, Gundlach H, Hanada K, Heyl A, Hicks KA, Hughes J, Lohr M, Mayer K, Melkozernov A, Murata T, Nelson DR, Pils B, Prigge M, Reiss B, Renner T, Rombauts S, Rushton PJ, Sanderfoot A, Schween G, Shiu SH, Stueber K, Theodoulou FL, Tu H, Van de Peer Y, Verrier PJ, Waters E, Wood A, Yang L, Cove D, Cuming AC, Hasebe M, Lucas S, Mishler BD, Reski R, Grigoriev IV, Quatrano RS, Boore JL (2008) The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319:64-69
46. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572-1574
47. Sanchez-Puerta MV, Cho Y, Mower JP, Alverson AJ, Palmer JD (2008) Frequent, phylogenetically local horizontal transfer of the cox1 group I intron in flowering plant mitochondria. Mol Biol Evol 25:1762-1777
48. Schmitz-Linneweber C, Barkan A (2007) RNA splicing and RNA editing in chloroplasts. In: Bock R (ed) Cell and molecular biology of plastids. Springer, Berlin/Heidelberg, pp 213-248
49. 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
50. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731-2739
51. Terasawa K, Odahara M, Kabeya Y, Kikugawa T, Sekine Y, Fujiwara M, Sato N (2007) The mitochondrial genome of the moss Physcomitrella patens sheds new light on mitochondrial evolution in land plants. Mol Biol Evol 24:699-709
52. Toor N, Hausner G, Zimmerly S (2001) Coevolution of group II intron RNA structures with their intron-encoded reverse transcriptases. RNA 7:1142-1152
53. Turmel M, Otis C, Lemieux C (2003) The mitochondrial genome of Chara vulgaris: insights into the mitochondrial DNA architecture of the last common ancestor of green algae and land plants. Plant Cell 15:1888-1903
54. Turmel M, Gagnon MC, O'Kelly CJ, Otis C, Lemieux C (2009) The chloroplast genomes of the green algae Pyramimonas, Monomastix, and Pycnococcus shed new light on the evolutionary history of prasinophytes and the origin of the secondary chloroplasts of euglenids. Mol Biol Evol 26:631-648
55. Ueda M, Kadowaki K (2012) Gene content and gene transfer from mitochondria to the nucleus during evolution. In: Laurence M-D (ed) Advances in botanical research. Academic Press, New York, pp 21-40
56. Unseld M, Marienfeld JR, Brandt P, Brennicke A (1997) The mitochondrial genome of Arabidopsis thaliana contains 57 genes in 366,924 nucleotides. Nat Genet 15:57-61
57. Wang B, Xue J, Li L, Liu Y, Qiu YL (2009) The complete mitochondrial genome sequence of the liverwort Pleurozia purpurea reveals extremely conservative mitochondrial genome evolution in liverworts. Curr Genet 55:601-609
58. Wikstrom N, Pryer KM (2005) Incongruence between primary sequence data and the distribution of a mitochondrial atp1 group II intron among ferns and horsetails. Mol Phylogenet Evol 36:484-493
59. Wolfe KH, Morden CW, Palmer JD (1992) Function and evolution of a minimal plastid genome from a nonphotosynthetic parasitic plant. Proc Natl Acad Sci USA 89:10648-10652
60. Xue JY, Liu Y, Li L, Wang B, Qiu YL (2010) The complete mitochondrial genome sequence of the hornwort Phaeoceros laevis: retention of many ancient pseudogenes and conservative evolution of mitochondrial genomes in hornworts. Curr Genet 56:53-61
61. 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
62. Zimmerly S, Guo H, Perlman PS, Lambowitz AM (1995) Group II intron mobility occurs by target DNA-primed reverse transcription. Cell 82:545-554
63. Zimmerly S, Hausner G, Wu X (2001) Phylogenetic relationships among group II intron ORFs. Nucleic Acids Res 29:1238-1250
64. Zoschke R, Nakamura M, Liere K, Sugiura M, Borner T, Schmitz-Linneweber C (2010) An organellar maturase associates with multiple group II introns. Proc Natl Acad Sci USA 107:3245-3250