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Evolution of Plant Mitochondrial Intron-Encoded Maturases: Frequent Lineage-Specific Loss and Recurrent Intracellular Transfer to the Nucleus

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Abstract

Among land plants, mitochondrial and plastid group II introns occasionally encode proteins called maturases that are important for splicing. Angiosperm nuclear genomes also encode maturases that are targeted to the organelles, but it is not known whether nucleus-encoded maturases exist in other land plant lineages. To examine the evolutionary diversity and history of this essential gene family, we searched for maturase homologs in recently sequenced nuclear and mitochondrial genomes from diverse land plants. We found that maturase content in mitochondrial genomes is highly lineage specific, such that orthologous maturases are rarely shared among major land plant groups. The presence of numerous mitochondrial pseudogenes in the mitochondrial genomes of several species implies that the sporadic maturase distribution is due to frequent inactivation and eventual loss over time. We also identified multiple maturase paralogs in the nuclear genomes of the lycophyte Selaginella moellendorffii, the moss Physcomitrella patens, and the representative angiosperm Vitis vinifera. Phylogenetic analyses of organelle- and nucleus-encoded maturases revealed that the nuclear maturase genes in angiosperms, lycophytes, and mosses arose by multiple shared and independent transfers of mitochondrial paralogs to the nuclear genome during land plant evolution. These findings indicate that plant mitochondrial maturases have experienced a surprisingly dynamic history due to a complex interaction of multiple evolutionary forces that affect the rates of maturase gain, retention, and loss.

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References

  • Adams KL, Palmer JD (2003) Evolution of mitochondrial gene content: gene loss and transfer to the nucleus. Mol Phylogenet Evol 29:380–395

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Bonen L (2011) RNA splicing in plant mitochondria. In: Kempken F (ed) Plant mitochondria. Springer, New York, pp 131–155

    Chapter  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Dai L, Toor N, Olson R, Keeping A, Zimmerly S (2003) Database for mobile group II introns. Nucleic Acids Res 31:424–426

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Duff RJ (2006) Divergent RNA editing frequencies in hornwort mitochondrial nad5 sequences. Gene 366:285–291

    Article  PubMed  Google Scholar 

  • Duffy AM, Kelchner SA, Wolf PG (2009) Conservation of selection on matK following an ancient loss of its flanking intron. Gene 438:17–25

    Article  PubMed  CAS  Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Germain A, Hotto AM, Barkan A, Stern DB (2013) RNA processing and decay in plastids. Wiley Interdiscip Rev RNA 4:295

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Hausner G (2012) Introns, mobile elements, and plasmids. In: Bullerwell CE (ed) Organelle genetics. Springer, Berlin Heidelberg, pp 329–357

    Chapter  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Krause K (2011) Piecing together the puzzle of parasitic plant plastome evolution. Planta 234:647–656

    Article  PubMed  CAS  Google Scholar 

  • Lambowitz AM, Zimmerly S (2011) Group II introns: mobile ribozymes that invade DNA. Cold Spring Harb Perspect Biol 3:a003616

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Martin W, Herrmann RG (1998) Gene transfer from organelles to the nucleus: how much, what happens, and why? Plant Physiol 118:9–17

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Chapter  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Ohyama K, Takemura M (2008) Molecular evolution of mitochondrial introns in the liverwort Marchantia polymorpha. Proc Jpn Acad Ser B 84:17–23

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Toor N, Hausner G, Zimmerly S (2001) Coevolution of group II intron RNA structures with their intron-encoded reverse transcriptases. RNA 7:1142–1152

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Zimmerly S, Guo H, Perlman PS, Lambowitz AM (1995) Group II intron mobility occurs by target DNA-primed reverse transcription. Cell 82:545–554

    Article  PubMed  CAS  Google Scholar 

  • Zimmerly S, Hausner G, Wu X (2001) Phylogenetic relationships among group II intron ORFs. Nucleic Acids Res 29:1238–1250

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank members of the Mower lab and Sally Mackenzie’s lab for stimulating discussions, Dawn Simon and Linda Bonen for assisting with group II intron classifications, and Dawn Simon, Linda Bonen, and Ido Keren for critically reading an earlier version of the manuscript. This work was supported by startup funds from the University of Nebraska-Lincoln (JPM) and by the National Science Foundation (IOS-1027529 and MCB-1125386 to JPM).

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  1. Center for Plant Science Innovation, University of Nebraska, Lincoln, NE, 68588, USA

    Wenhu Guo & Jeffrey P. Mower

  2. School of Biological Sciences, University of Nebraska, Lincoln, NE, 68588, USA

    Wenhu Guo

  3. Department of Agronomy and Horticulture, University of Nebraska, Lincoln, NE, 68583, USA

    Jeffrey P. Mower

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Correspondence to Jeffrey P. Mower.

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Guo, W., Mower, J.P. Evolution of Plant Mitochondrial Intron-Encoded Maturases: Frequent Lineage-Specific Loss and Recurrent Intracellular Transfer to the Nucleus. J Mol Evol 77, 43–54 (2013). https://doi.org/10.1007/s00239-013-9579-7

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