Plant mitochondrial transcription termination factor (mTERF) genes comprise a large family with important roles in regulating organelle gene expression. In this study, a comprehensive database search yielded 31 potential mTERF genes in maize (Zea mays L.) and most of them were targeted to mitochondria or chloroplasts. Maize mTERF were divided into nine main groups based on phylogenetic analysis, and group IX represented the mitochondria and species-specific clade that diverged from other groups. Tandem and segmental duplication both contributed to the expansion of the mTERF gene family in the maize genome. Comprehensive expression analysis of these genes, using microarray data and RNA-seq data, revealed that these genes exhibit a variety of expression patterns. Environmental stimulus experiments revealed differential up or down-regulation expression of maize mTERF genes in seedlings exposed to light/dark, salts and plant hormones, respectively, suggesting various important roles of maize mTERF genes in light acclimation and stress-related responses. These results will be useful for elucidating the roles of mTERF genes in the growth, development and stress response of maize.
Binder S, Brennicke A (2003) Gene expression in plant mitochondria: transcriptional and post-transcriptional control. Philos Trans R Soc Lond B Biol Sci 358(1429): 181–188. doi: 10.1098/rstb.2002.1179
[3]
Liere K, Weihe A, B？rner T (2011) The transcription machineries of plant mitochondria and chloroplasts: composition, function, and regulation. J Plant Physiol 168(12): 1345–1360. doi: 10.1016/j.jplph.2011.01.005
[4]
Kühn K, Bohne AV, Liere K, Weihe A, B？rner T (2007) Arabidopsis single-polypeptide RNA polymerases: accurate in vitro transcription of organellar genes. Plant Cell 19: 959–971. doi: 10.1105/tpc.106.046839
Linder T, Park CB, Asin-Cayuela J, Pellegrini M, Larsson NG, et al. (2005) A family of putative transcription termination factors shared amongst metazoans and plants. Curr Genet 48: 265–269. doi: 10.1007/s00294-005-0022-5
[7]
Roberti M, Bruni F, Polosa PL, Gadaleta MN, Cantatore P (2006) The Drosophila termination factor DmTTF regulates in vivo mitochondrial transcription. Nucleic Acids Res 34(7): 2109–2116. doi: 10.1093/nar/gkl181
[8]
Roberti M, Bruni F, Loguercio Polosa P, Manzari C, Gadaleta MN, et al. (2006) MTERF3, the most conserved member of the mTERF family, is a modular factor involved in mitochondrial protein synthesis. Biochim Biophys Acta 1757(9–10): 1199–11206. doi: 10.1016/j.bbabio.2006.04.026
[9]
Roberti M, Polosa PL, Bruni F, Manzari C, Deceglie S, et al. (2009) The MTERF family proteins: Mitochondrial transcription regulators and beyond. Biochim Biophys Acta 1787(5): 303–311. doi: 10.1016/j.bbabio.2009.01.013
[10]
Kruse B, Narasimhan N, Attardi G (1989) Termination of transcription in human mitochondria: identification and purification of a DNA binding protein factor that promotes termination. Cell 58(2): 391–397. doi: 10.1016/0092-8674(89)90853-2
[11]
Fernandez-Silva P, Martinez-Azorin F, Micol V, Attardi G (1997) The human mitochondrial transcription termination factor (mTERF) is a multizipper protein but binds to DNA as a monomer, with evidence pointing to intramolecular leucine zipper interactions. EMBO J 16(5): 1066–1079. doi: 10.1093/emboj/16.5.1066
[12]
Pellegrini M, Asin-Cayuela J, Erdjument-Bromage H, Tempst P, Larsson NG, et al. (2009) MTERF2 is a nucleoid component in mammalian mitochondria. Biochim Biophys Acta 1787(5): 296–302. doi: 10.1016/j.bbabio.2009.01.018
Park CB, Asin-Cayuela J, Cámara Y, Shi Y, Pellegrini M, et al. (2007) MTERF3 is a negative regulator of mammalian mtDNA transcription. Cell 130(2): 273–285. doi: 10.1016/j.cell.2007.05.046
[15]
Cámara Y, Asin-Cayuela J, Park CB, Metodiev MD, Shi Y, et al. (2011) MTERF4 regulates translation by targeting the methyltransferase NSUN4 to the mammalian mitochondrial ribosome. Cell Metab 13(5): 527–539. doi: 10.1016/j.cmet.2011.04.002
[16]
Sp？hr H, Habermann B, Gustafsson CM, Larsson NG, Hallberg BM (2012) Structure of the human MTERF4-NSUN4 protein complex that regulates mitochondrial ribosome biogenesis. Proc Natl Acad Sci USA 109(38): 15253–15258. doi: 10.1073/pnas.1210688109
[17]
Babiychuk E, Vandepoele K, Wissing J, Garcia-Diaz M, De Rycke R, et al. (2011) Plastid gene expression and plant development require a plastidic protein of the mitochondrial transcription termination factor family. Proc Natl Acad Sci USA 108(16): 6674–6679. doi: 10.1073/pnas.1103442108
[18]
Kleine T (2012) Arabidopsis thaliana mTERF proteins: evolution and functional classification. Front Plant Sci 3: 233. doi: 10.3389/fpls.2012.00233
[19]
Sch？nfeld C, Wobbe L, Borgst？dt R, Kienast A, Nixon PJ, et al. (2004) The nucleus-encoded protein MOC1 is essential for mitochondrial light acclimation in Chlamydomonas reinhardtii. J Biol Chem 279(48): 50366–50374. doi: 10.1074/jbc.m408477200
[20]
Wobbe L, Nixon PJ (2013) The mTERF protein MOC1 terminates mitochondrial DNA transcription in the unicellular green alga Chlamydomonas reinhardtii. Nucleic Acids Res 41(13): 6553–6567. doi: 10.1093/nar/gkt313
[21]
Meskauskiene R, Würsch M, Laloi C, Vidi PA, Coll NS, et al. (2009) A mutation in the Arabidopsis mTERF-related plastid protein SOLDAT10 activates retrograde signaling and suppresses 1O2-induced cell death. Plant J 60(3): 399–410. doi: 10.1111/j.1365-313x.2009.03965.x
[22]
Quesada V, Sarmiento-Ma？ús R, González-Bayón R, Hricová A, Pérez-Marcos R, et al. Arabidopsis RUGOSA2 encodes an mTERF family member required for mitochondrion, chloroplast and leaf development (2011) Plant J. 68: 738–753. doi: 10.1111/j.1365-313x.2011.04726.x
[23]
Robles P, Micol JL, Quesada V (2012) Arabidopsis MDA1, a nuclear-encoded protein, functions in chloroplast development and abiotic stress responses. PLoS One 7(8): e42924. doi: 10.1371/journal.pone.0042924
[24]
Kim M, Lee U, Small I, des Francs-Small CC, Vierling E (2012) Mutations in an Arabidopsis mitochondrial transcription termination factor-related protein enhance thermotolerance in the absence of the major molecular chaperone HSP101. Plant Cell 24(8): 3349–3365. doi: 10.1105/tpc.112.101006
Letunic I, Doerks T, Bork P (2012) SMART 7: recent updates to the protein domain annotation resource. Nucleic Acids Res 40(Database issue): D302–D305.
[27]
Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22(21): 2688–2690. doi: 10.1093/bioinformatics/btl446
[28]
Emanuelsson O, Brunak S, von Heijne G, Nielsen H (2007) Locating proteins in the cell using TargetP, SignalP and related tools. Nat Protoc 2(4): 953–971. doi: 10.1038/nprot.2007.131
[29]
Small I, Peeters N, Legeai F, Lurin C (2004) Predotar: A tool for rapidly screening proteomes for N-terminal targeting sequences. Proteomics 4(6): 1581–1590. doi: 10.1002/pmic.200300776
[30]
Sun Q, Zybailov B, Majeran W, Friso G, Olinares PD, et al. (2009) PPDB, the Plant Proteomics Database at Cornell. Nucleic Acids Res 37(Database issue): D969–D974.
[31]
Majeran W, Friso G, Asakura Y, Qu X, Huang M, et al. (2011) Nucleoid-enriched proteomes in developing plastids and chloroplasts from maize leaves: a new conceptual framework for nucleoid functions. Plant Physiol 158(1): 156–189. doi: 10.1104/pp.111.188474
[32]
Friso G, Majeran W, Huang M, Sun Q, van Wijk KJ (2010) Reconstruction of metabolic pathways, protein expression, and homeostasis machineries across maize bundle sheath and mesophyll chloroplasts: large-scale quantitative proteomics using the first maize genome assembly. Plant Physiol 152(3): 1219–1250. doi: 10.1104/pp.109.152694
[33]
Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23(21): 2947–2948. doi: 10.1093/bioinformatics/btm404
[34]
Bailey TL, Boden M, Buske FA, Frith M, Grant CE, et al. (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37(Web Server issue): W202–W208.
[35]
Martin M, Cho J, Cesare AJ, Griffith JD, Attardi G (2005) Termination factor-mediated DNA loop between termination and initiation sites drives mitochondrial rRNA synthesis. Cell 123(7): 1227–1240. doi: 10.1016/j.cell.2005.09.040
[36]
Sp？hr H, Samuelsson T, H？llberg BM, Gustafsson CM (2010) Structure of mitochondrial transcription termination factor 3 reveals a novel nucleic acid-binding domain. Biochem Biophys Res Commun 397(3): 386–390. doi: 10.1016/j.bbrc.2010.04.130
[37]
Yakubovskaya E, Mejia E, Byrnes J, Hambardjieva E, Garcia-Diaz M (2010) Helix unwinding and base flipping enable human MTERF1 to terminate mitochondrial transcription. Cell 141(6): 982–993. doi: 10.1016/j.cell.2010.05.018
[38]
Yakubovskaya E, Guja KE, Mejia E, Castano S, Hambardjieva E, et al. (2012) Structure of the essential MTERF4: NSUN4 protein complex reveals how an MTERF protein collaborates to facilitate rRNA modification. Structure 20(11): 1940–1947. doi: 10.1016/j.str.2012.08.027
[39]
Groves MR, Hanlon N, Turowski P, Hemmings BA, Barford D (1999) The structure of the protein phosphatase 2A PR65/A subunit reveals the conformation of its 15 tandemly repeated HEAT motifs. Cell 96(1): 99–110. doi: 10.1016/s0092-8674(00)80963-0
[40]
Sibanda BL, Chirgadze DY, Blundell TL (2010) Crystal structure of DNA-PKcs reveals a large open-ring cradle comprised of HEAT repeats. Nature 463: 118–121. doi: 10.1038/nature08648
[41]
Edwards TA, Pyle SE, Wharton RP, Aggarwal AK (2001) Structure of Pumilio reveals similarity between RNA and peptide binding motifs. Cell 105(2): 281–289. doi: 10.1016/s0092-8674(01)00318-x
[42]
Zhang Y (2008) I-TASSER server for protein 3D structure prediction. BMC Bioinformatics 9: 40. doi: 10.1186/1471-2105-9-40
[43]
Zhang Y, Skolnick J (2005) TM-align: a protein structure alignment algorithm based on the TM-score. Nucleic Acids Res 33(7): 2302–2309. doi: 10.1093/nar/gki524
[44]
Soderlund C, Bomhoff M, Nelson WM (2011) SyMAP v3.4: a turnkey synteny system with application to plant genomes. Nucleic Acids Res 39(10): e68. doi: 10.1093/nar/gkr123
[45]
Van Bel M, Proost S, Wischnitzki E, Movahedi S, Scheerlinck C, et al. (2012) Dissecting plant genomes with the PLAZA comparative genomics platform. Plant Physiol 158(2): 590–600. doi: 10.1104/pp.111.189514
[46]
Nakashima K, Ito Y, Yamaguchi-Shinozaki K (2009) Transcriptional regulatory networks in response to abiotic stresses in Arabidopsis and grasses. Plant Physiol 149(1): 88–95. doi: 10.1104/pp.108.129791
[47]
Khong G, Richaud F, Coudert Y, Pati PK, Santi C, et al. (2008) Modulating rice stress tolerance by transcription factors. Biotechnol Genet Eng Rev 25: 381–403. doi: 10.5661/bger-25-381
[48]
Baker SS, Wilhelm KS, Thomashow MF (1994) The 5′-region of Arabidopsis thaliana cor15a has cis-acting elements that confer cold-, drought- and ABA-regulated gene expression. Plant Mol Biol 24(5): 701–713. doi: 10.1007/bf00029852
[49]
Chang WC, Lee TY, Huang HD, Huang HY, Pan RL (2008) PlantPAN: Plant promoter analysis navigator, for identifying combinatorial cis-regulatory elements with distance constraint in plant gene groups. BMC Genomics 9: 561. doi: 10.1186/1471-2164-9-561
[50]
Sekhon RS, Lin H, Childs KL, Hansey CN, Buell CR, et al. (2011) Genome-wide atlas of transcription during maize development. Plant J 66(4): 553–563. doi: 10.1111/j.1365-313x.2011.04527.x
[51]
Eisen MB, Spellman PT, Brown PO, Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 95(25): 14863–14868. doi: 10.1073/pnas.95.25.14863
[52]
Duarte JM, Cui L, Wall PK, Zhang Q, Zhang X, et al. (2006) Expression pattern shifts following duplication indicative of subfunctionalization and neofunctionalization in regulatory genes of Arabidopsis. Mol Biol Evol 23(2): 469–478. doi: 10.1093/molbev/msj051
[53]
Winter D, Vinegar B, Nahal H, Ammar R, Wilson GV, et al. (2007) An “Electronic Fluorescent Pictograph” browser for exploring and analyzing large-scale biological data sets. PLoS One 2(8): e718. doi: 10.1371/journal.pone.0000718
[54]
Li P, Ponnala L, Gandotra N, Wang L, Si Y, et al. (2010) The developmental dynamics of the maize leaf transcriptome. Nat Genet 42(12): 1060–1067. doi: 10.1038/ng.703
[55]
Schnable PS, Ware D, Fulton RS, Stein JC, Wei F, et al. (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326: 1112–1115.
[56]
Forner J, Weber B, Thuss S, Wildum S, Binder S (2007) Mapping of mitochondrial mRNA termini in Arabidopsis thaliana: t-elements contribute to 5′ and 3′ end formation. Nucleic Acids Res 35: 3676–3692. doi: 10.1093/nar/gkm270
[57]
Gagliardi D, Binder S (2007) Expression of the plant mitochondrial genome. In D Logan, ed, Plant Mitochondria. Blackwell Publishing, Ames, IA, 50–95.
[58]
Lynch M, Conery JS (2000) The evolutionary fate and consequences of duplicate genes. Science 290: 1151–1155. doi: 10.1126/science.290.5494.1151
[59]
Hammani K, Barkan A (2014) An mTERF domain protein functions in group II intron splicing in maize chloroplasts. Nucleic Acids Res In press.
[60]
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215(3): 403–410. doi: 10.1016/s0022-2836(05)80360-2
[61]
Soderlund C, Descour A, Kudrna D, Bomhoff M, Boyd L, et al. (2009) Sequencing, mapping, and analysis of 27,455 maize full-length cDNAs. PLoS Genet 5(11): e1000740. doi: 10.1371/journal.pgen.1000740
[62]
Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, et al. (2012) The Pfam protein families database. Nucleic Acids Res 40(Database issue): D290–D301.
[63]
Schnable JC, Lyons E (2011) Comparative genomics with maize and other grasses: from genes to genomes! Maydica. 56: 183–200.
[64]
Guo AY, Zhu QH, Chen X, Luo JC (2007) GSDS: a gene structure display server. Yi Chuan 29(8): 1023–1026. doi: 10.1360/yc-007-1023
[65]
Crooks GE, Hon G, Chandonia JM, Brenner SE (2004) WebLogo: a sequence logo generator. Genome Res 14(6): 1188–1190. doi: 10.1101/gr.849004
[66]
Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93(1): 77–78. doi: 10.1093/jhered/93.1.77
[67]
Peng X, Zhao Y, Cao J, Zhang W, Jiang H, et al. (2012) CCCH-type zinc finger family in maize: genome-wide identification, classification and expression profiling under abscisic acid and drought treatments. PLoS One 7(7): e40120. doi: 10.1371/journal.pone.0040120
[68]
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32(5): 1792–1797. doi: 10.1093/nar/gkh340
[69]
Cao B, Porollo A, Adamczak R, Jarrell M, Meller J (2006) Enhanced recognition of protein transmembrane domains with prediction-based structural profiles. Bioinformatics 22(3): 303–309. doi: 10.1093/bioinformatics/bti784
[70]
Jiménez-Menéndez N, Fernández-Millán P, Rubio-Cosials A, Arnan C, Montoya J, et al. (2010) Human mitochondrial mTERF wraps around DNA through a left-handed superhelical tandem repeat. Nat Struct Mol Biol 17(7): 891–893. doi: 10.1038/nsmb.1859
[71]
Schrodinger L (2013) The PyMOL Molecular Graphics System, Version 1.6.0.0. Portland, OR, USA.
[72]
Dash S, Van Hemert J, Hong L, Wise RP, Dickerson JA (2012) PLEXdb: gene expression resources for plants and plant pathogens. Nucleic Acids Res 40(Database issue): D1194–D1201.
[73]
Saldanha AJ (2004) Java Treeview–extensible visualization of microarray data. Bioinformatics 20(17): 3246–3248. doi: 10.1093/bioinformatics/bth349
[74]
Haring M, Offermann S, Danker T, Horst I, Peterhansel C, et al. (2007) Chromatin immunoprecipitation: optimization, quantitative analysis and data normalization. Plant Methods 3: 11. doi: 10.1186/1746-4811-3-11
[75]
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT method. Methods 25(4): 402–408. doi: 10.1006/meth.2001.1262
