1,335
Views
7
CrossRef citations to date
0
Altmetric
Research Paper

Major contribution of transcription initiation to 5’-end formation of mitochondrial steady-state transcripts in maize

, , , , , & show all
Pages 104-117 | Received 16 Oct 2018, Accepted 13 Dec 2018, Published online: 06 Jan 2019

References

  • Neupert W. Mitochondrial gene expression: a playground of evolutionary tinkering. Annu Rev Biochem. 2016;85:65–76.
  • Gualberto JM, Mileshina D, Wallet C, et al. The plant mitochondrial genome: dynamics and maintenance. Biochimie. 2014;100:107–120.
  • Forner J, Weber B, Thuss S, et al. Mapping of mitochondrial mRNA termini in Arabidopsis thaliana: t-elements contribute to 5ʹ and 3ʹ end formation. Nucleic Acids Res. 2007;35:3676–3692.
  • Choi BY, Acero MM, Bonen L. Mapping of wheat mitochondrial mRNA termini and comparison with breakpoints in DNA homology among plants. Plant Mol Biol. 2012;80:539–552.
  • Kuhn K, Weihe A, Borner T. Multiple promoters are a common feature of mitochondrial genes in Arabidopsis. Nucleic Acids Res. 2005;33:337–346.
  • Mulligan RM, Lau GT, Walbot V. Numerous transcription initiation sites exist for the maize mitochondrial genes for subunit 9 of the ATP synthase and subunit 3 of cytochrome oxidase. Proc Natl Acad Sci U S A. 1988;85:7998–8002.
  • Mulligan RM, Maloney AP, Walbot V. RNA processing and multiple transcription initiation sites result in transcript size heterogeneity in maize mitochondria. Mol Gen Genet. 1988;211:373–380.
  • Hammani K, Giege P. RNA metabolism in plant mitochondria. Trends Plant Sci. 2014;19:380–389.
  • Canino G, Bocian E, Barbezier N, et al. Arabidopsis encodes four tRNase Z enzymes. Plant Physiol. 2009;150:1494–1502.
  • Gutmann B, Gobert A, Giege P. PRORP proteins support RNase P activity in both organelles and the nucleus in Arabidopsis. Gene Dev. 2012;26:1022–1027.
  • Haïli N, Arnal N, Quadrado M, et al. The pentatricopeptide repeat MTSF1 protein stabilizes the nad4 mRNA in Arabidopsis mitochondria. Nucleic Acids Res. 2013;41:6650–6663.
  • Kuhn J, Tengler U, Binder S. Transcript lifetime is balanced between stabilizing stem-Loop structures and degradation-promoting polyadenylation in plant mitochondria. Mol Cell Biol. 2001;21:731–742.
  • Dombrowski S, Brennicke A, Binder S. 3ʹ-Inverted repeats in plant mitochondrial mRNAs are processing signals rather than transcription terminators. Embo J. 1997;16:5069–5076.
  • Wang C, Aube F, Planchard N, et al. The pentatricopeptide repeat protein MTSF2 stabilizes a nad1 precursor transcript and defines the 3ʹ end of its 5ʹ-half intron. Nucleic Acids Res. 2017;45:6119–6134.
  • Ruwe H, Wang G, Gusewski S, et al. Systematic analysis of plant mitochondrial and chloroplast small RNAs suggests organelle-specific mRNA stabilization mechanisms. Nucleic Acids Res. 2016;44:7406–7417.
  • Binder S, Stoll K, Stoll B. P-class pentatricopeptide repeat proteins are required for efficient 5ʹ end formation of plant mitochondrial transcripts. RNA Biol. 2013;10:1511–1519.
  • Binder S, Stoll K, Stoll B Maturation of 5ʹ ends of plant mitochondrial RNAs. Physiol Plantarum 2016; 157:280–288.
  • Yan B, Pring DR. Transcriptional initiation sites in sorghum mitochondrial DNA indicate conserved and variable features. Curr Genet. 1997;32:287–295.
  • Rapp WD, Stern DB. A conserved 11 nucleotide sequence contains an essential promoter element of the maize mitochondrial atp1 gene. Embo J. 1992;11:1065–1073.
  • Lupold DS, Caoile AG, Stern DB. The maize mitochondrial cox2 gene has five promoters in two genomic regions, including a complex promoter consisting of seven overlapping units. J Biol Chem. 1999;274:3897–3903.
  • Caoile AG, Stern DB. A conserved core element is functionally important for maize mitochondrial promoter activity in vitro. Nucleic Acids Res. 1997;25:4055–4060.
  • Rapp WD, Lupold DS, Mack S, et al. Architecture of the maize mitochondrial atp1 promoter as determined by linker-scanning and point mutagenesis. Mol Cell Biol. 1993;13:7232–7238.
  • Giese A, Thalheim C, Brennicke A, et al. Correlation of nonanucleotide motifs with transcript initiation of 18S rRNA genes in mitochondria of pea, potato and Arabidopsis. Mol Gen Genet. 1996;252:429–436.
  • Zhang YF, Suzuki M, Sun F, et al. The mitochondrion-targeted PENTATRICOPEPTIDE REPEAT78 protein is required for nad5 mature mRNA stability and seed development in maize. Mol Plant. 2017;10:1321–1333.
  • Wang HQ, Wang K, Du QG, et al. Maize Urb2 protein is required for kernel development and vegetative growth by affecting pre-ribosomal RNA processing. New Phytol. 2018;218:1233–1246.
  • Clifton SW, Minx P, Fauron CM, et al. Sequence and comparative analysis of the maize NB mitochondrial genome. Plant Physiol. 2004;136:3486–3503.
  • Maloney AP, Traynor PL, Levings CS 3rd, et al. Identification in maize mitochondrial 26S rRNA of a short 5ʹ-end sequence possibly involved in transcription initiation and processing. Curr Genet. 1989;15:207–212.
  • Liere K, Weihe A, Borner T. The transcription machineries of plant mitochondria and chloroplasts: composition, function, and regulation. J Plant Physiol. 2011;168:1345–1360.
  • Bailey TL, Boden M, Buske FA, et al. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res. 2009;37:W202–8.
  • Calixte S, Bonen L. Developmentally-specific transcripts from the ccmFN-rps1 locus in wheat mitochondria. Mol Genet Genomics. 2008;280:419–426.
  • Haouazine-Takvorian N, Takvorian A, Jubier MF, et al. Genes encoding subunit 6 of NADH dehydrogenase and subunit 6 of ATP synthase are co-transcribed in maize mitochondria. Curr Genet. 1997;31:63–69.
  • Hanic-Joyce PJ, Spencer DF, Gray MW. In vitro processing of transcripts containing novel tRNA-like sequences (‘t-elements’) encoded by wheat mitochondrial DNA. Plant Mol Biol. 1990;15:551–559.
  • Zuker M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 2003;31:3406–3415.
  • Williams MA, Johzuka Y, Mulligan RM. Addition of non-genomically encoded nucleotides to the 3ʹ-terminus of maize mitochondrial mRNAs: truncated rps12 mRNAs frequently terminate with CCA. Nucleic Acids Res. 2000;28:4444–4451.
  • Shikanai T. RNA editing in plants: machinery and flexibility of site recognition. BBA-Bioenergetics. 2015;1847:779–785.
  • Stern DB, Goldschmidt-Clermont M, Hanson MR. Chloroplast RNA metabolism. Annu Rev Plant Biol. 2010;61:125–155.
  • Pfalz J, Bayraktar OA, Prikryl J, et al. Site-specific binding of a PPR protein defines and stabilizes 5ʹ and 3ʹ mRNA termini in chloroplasts. Embo J. 2009;28:2042–2052.
  • Kishine M, Takabayashi A, Munekage Y, et al. Ribosomal RNA processing and an RNase R family member in chloroplasts of Arabidopsis. Plant Mol Biol. 2004;55:595–606.
  • Hayes R, Kudla J, Schuster G, et al. Chloroplast mRNA 3ʹ-end processing by a high molecular weight protein complex is regulated by nuclear encoded RNA binding proteins. Embo J. 1996;15:1132–1141.
  • Luro S, Germain A, Sharwood RE, et al. RNase J participates in a pentatricopeptide repeat protein-mediated 5ʹ end maturation of chloroplast mRNAs. Nucleic Acids Res. 2013;41:9141–9151.
  • Perrin R, Meyer EH, Zaepfel M, et al. Two exoribonucleases act sequentially to process mature 3ʹ-ends of atp9 mRNAs in Arabidopsis mitochondria. J Biol Chem. 2004;279:25440–25446.
  • Kazama T, Yagi Y, Toriyama K, et al. Heterogeneity of the 5ʹ-end in plant mRNA may be involved in mitochondrial translation. Front Plant Sci. 2013;4:517.
  • Gobert A, Gutmann B, Taschner A, et al. A single Arabidopsis organellar protein has RNase P activity. Nat Stuct Mol Biol 2010; 17:740–U113.
  • Bellaoui M, Pelletier G, Budar F. The steady-state level of mRNA from the Ogura cytoplasmic male sterility locus in Brassica cybrids is determined post-transcriptionally by its 3ʹ region. Embo J. 1997;16:5057–5068.
  • Marzluff WF. Metazoan replication-dependent histone mRNAs: a distinct set of RNA polymerase II transcripts. Curr Opin Cell Biol. 2005;17:274–280.
  • Liu YJ, Xiu ZH, Meeley R, et al. Empty pericarp5 encodes a pentatricopeptide repeat protein that is required for mitochondrial RNA editing and seed development in maize. Plant Cell. 2013;25:868–883.
  • Meyer EH, Tomaz T, Carroll AJ, et al. Remodeled respiration in ndufs4 with low phosphorylation efficiency suppresses Arabidopsis germination and growth and alters control of metabolism at night. Plant Physiol. 2009;151:603–619.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.