title: Evolution of plant mitochondrial intron-encoded maturases: frequent lineage-specific loss and recurrent intracellular transfer to the nucleus.
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.
authors: Center for Plant Science Innovation, University of Nebraska, Lincoln, NE, 68588, USA.
authors: Wenhu
authors: W
authors: Guo
authors: Jeffrey P
authors: JP
authors: Mower
mesh_terms: D019143:Evolution, Molecular; D050259:Genes, Mitochondrial; D042541:Intracellular Space / Q000378:metabolism; D007438:Introns; D008928:Mitochondria / Q000201:enzymology* / Q000235:genetics*; D008969:Molecular Sequence Data; D010802:Phylogeny; D010940:Plant Proteins / Q000235:genetics* / Q000378:metabolism; D010944:Plants / Q000145:classification / Q000235:genetics* / Q000378:metabolism*; D021381:Protein Transport
chemical_list: D010940:Plant Proteins
references: Nature. 2007 Sep 27;449(7161):463-7
references: 17721507
references: EMBO J. 2003 Sep 1;22(17):4555-65
references: 12941706
references: Gene. 2009 Jun 1;438(1-2):17-25
references: 19236909
references: Mol Biol Evol. 2007 Mar;24(3):699-709
references: 17175527
references: Mol Biol Evol. 2006 Feb;23(2):380-91
references: 16267141
references: Gene. 2006 Feb 1;366(2):285-91
references: 16376027
references: Nat Genet. 1997 Jan;15(1):57-61
references: 8988169
references: Science. 2011 May 20;332(6032):960-3
references: 21551031
references: Proc Jpn Acad Ser B Phys Biol Sci. 2008;84(1):17-23
references: 18941284
references: J Biol Chem. 2005 Oct 21;280(42):35085-8
references: 16150738
references: Nucleic Acids Res. 2003 Jan 1;31(1):424-6
references: 12520040
references: Planta. 2011 Oct;234(4):647-56
references: 21850456
references: Mol Biol Evol. 2005 Sep;22(9):1903-18
references: 15930151
references: Plant Cell Physiol. 2006 Jun;47(6):772-83
references: 16621844
references: Mol Biol Evol. 2009 Jan;26(1):99-110
references: 18922764
references: Curr Genet. 2009 Dec;55(6):601-9
references: 19756627
references: Mol Phylogenet Evol. 2004 Jul;32(1):246-63
references: 15186811
references: BMC Plant Biol. 2012 May 01;12:61
references: 22548759
references: Cell. 1995 Aug 25;82(4):545-54
references: 7664334
references: Cold Spring Harb Perspect Biol. 2011 Aug 01;3(8):a003616
references: 20463000
references: BMC Plant Biol. 2007 Aug 22;7:45
references: 17714582
references: Plant J. 2012 Aug;71(3):413-26
references: 22429648
references: Mol Phylogenet Evol. 2005 Sep;36(3):484-93
references: 15922630
references: Curr Genet. 2010 Feb;56(1):53-61
references: 19998039
references: Mol Phylogenet Evol. 2003 Dec;29(3):380-95
references: 14615181
references: PLoS One. 2011;6(10):e25836
references: 21998706
references: Proc Natl Acad Sci U S A. 2010 Feb 16;107(7):3245-50
references: 20133623
references: Proc Natl Acad Sci U S A. 1992 Nov 15;89(22):10648-52
references: 1332054
references: Mol Biol Evol. 2011 Oct;28(10):2731-9
references: 21546353
references: PLoS One. 2012;7(4):e35168
references: 22511984
references: Plant Cell. 2003 Aug;15(8):1888-903
references: 12897260
references: Curr Genet. 2006 Aug;50(2):137-47
references: 16721603
references: Plant Physiol. 1998 Sep;118(1):9-17
references: 9733521
references: Mol Biol Evol. 2009 Dec;26(12):2795-808
references: 19713327
references: Mol Plant. 2010 Jul;3(4):691-705
references: 20603383
references: Wiley Interdiscip Rev RNA. 2013 May-Jun;4(3):295-316
references: 23536311
references: Bioinformatics. 2003 Aug 12;19(12):1572-4
references: 12912839
references: Mol Biol Evol. 1999 Apr;16(4):441-52
references: 10331271
references: PLoS One. 2009 Jun 19;4(6):e5982
references: 19543388
references: Mol Biol Evol. 2008 Aug;25(8):1762-77
references: 18524785
references: Nucleic Acids Res. 2012 Jan;40(Database issue):D1178-86
references: 22110026
references: Nucleic Acids Res. 2003 Jan 15;31(2):647-52
references: 12527773
references: Science. 2008 Jan 4;319(5859):64-9
references: 18079367
references: J Mol Biol. 1992 Jan 5;223(1):1-7
references: 1731062
references: Mol Biol Evol. 2009 Mar;26(3):631-48
references: 19074760
references: J Mol Evol. 2009 Jun;68(6):665-78
references: 19475442
references: Mol Biol Evol. 2007 Apr;24(4):1068-74
references: 17283365
references: Mol Biol Evol. 2008 Mar;25(3):603-15
references: 18192697
references: Nucleic Acids Res. 2001 Mar 1;29(5):1238-50
references: 11222775
references: EMBO J. 1988 Nov;7(11):3501-8
references: 2463163
references: Nucleic Acids Res. 2011 Apr;39(7):2890-902
references: 21138958
references: RNA. 2009 Dec;15(12):2299-311
references: 19946041
references: Mol Biol Evol. 2011 Jul;28(7):2077-86
references: 21289370
references: Nucleic Acids Res. 2004 Mar 19;32(5):1792-7
references: 15034147
references: Syst Biol. 2010 May;59(3):307-21
references: 20525638
references: RNA. 2001 Aug;7(8):1142-52
references: 11497432
references: Genome Biol Evol. 2011;3:344-58
references: 21436122