Distant Sequences Determine 5' End Formation of Cox3 Transcripts in Arabidopsis Thaliana Ecotype C24

Overview

Journal Nucleic Acids Res

Publisher Oxford University Press

Specialty Biochemistry

Date 2005 Aug 19

PMID 16107557

Citations 20

Authors

Joachim Forner

Barbel Weber

Caterina Wietholter

Rhonda C Meyer

Stefan Binder

Affiliations

Soon will be listed here.

Abstract

The genomic environments and the transcripts of the mitochondrial cox3 gene are investigated in three Arabidopsis thaliana ecotypes. While the proximate 5' sequences up to nucleotide position -584, the coding regions and the 3' flanking regions are identical in Columbia (Col), C24 and Landsberg erecta (Ler), genomic variation is detected in regions further upstream. In the mitochondrial DNA of Col, a 1790 bp fragment flanked by a nonanucleotide direct repeat is present beyond position -584 with respect to the ATG. While in Ler only part of this insertion is conserved, this sequence is completely absent in C24, except for a single copy of the nonanucleotide direct repeat. Northern hybridization reveals identical major transcripts in the three ecotypes, but identifies an additional abundant 60 nt larger mRNA species in C24. The extremities of the most abundant mRNA species are identical in the three ecotypes. In C24, an extra major 5' end is abundant. This terminus and the other major 5' ends are located in identical sequence regions. Inspection of Atcox3 transcripts in C24/Col hybrids revealed a female inheritance of the mRNA species with the extra 5' terminus. Thus, a mitochondrially encoded factor determines the generation of an extra 5' mRNA end.

Citing Articles

Imprinting but not cytonuclear interactions determines seed size heterosis in Arabidopsis hybrids.

June V, Song X, Chen Z Plant Physiol. 2024; 195(2):1214-1228.

PMID: 38319651 PMC: 11142339. DOI: 10.1093/plphys/kiae061.

Repeats of Unusual Size in Plant Mitochondrial Genomes: Identification, Incidence and Evolution.

Wynn E, Christensen A G3 (Bethesda). 2018; 9(2):549-559.

PMID: 30563833 PMC: 6385970. DOI: 10.1534/g3.118.200948.

The Complexity of Mitochondrial Complex IV: An Update of Cytochrome c Oxidase Biogenesis in Plants.

Mansilla N, Racca S, Gras D, Gonzalez D, Welchen E Int J Mol Sci. 2018; 19(3).

PMID: 29495437 PMC: 5877523. DOI: 10.3390/ijms19030662.

The application of RNA-seq to the comprehensive analysis of plant mitochondrial transcriptomes.

Stone J, Storchova H Mol Genet Genomics. 2014; 290(1):1-9.

PMID: 25182379 DOI: 10.1007/s00438-014-0905-6.

P-class pentatricopeptide repeat proteins are required for efficient 5' end formation of plant mitochondrial transcripts.

Binder S, Stoll K, Stoll B RNA Biol. 2013; 10(9):1511-9.

PMID: 24184847 PMC: 3858434. DOI: 10.4161/rna.26129.

References

Sakamoto W, Kondo H, Murata M, Motoyoshi F . Altered mitochondrial gene expression in a maternal distorted leaf mutant of Arabidopsis induced by chloroplast mutator. Plant Cell. 1996; 8(8):1377-90. PMC: 161258. DOI: 10.1105/tpc.8.8.1377. View

Kubo T, Nishizawa S, Sugawara A, Itchoda N, Estiati A, Mikami T . The complete nucleotide sequence of the mitochondrial genome of sugar beet (Beta vulgaris L.) reveals a novel gene for tRNA(Cys)(GCA). Nucleic Acids Res. 2000; 28(13):2571-6. PMC: 102699. DOI: 10.1093/nar/28.13.2571. View

Hoffmann M, Kuhn J, Daschner K, Binder S . The RNA world of plant mitochondria. Prog Nucleic Acid Res Mol Biol. 2001; 70:119-54. DOI: 10.1016/s0079-6603(01)70015-3. View

Dombrowski S, Hoffmann M, Guha C, Binder S . Continuous primary sequence requirements in the 18-nucleotide promoter of dicot plant mitochondria. J Biol Chem. 1999; 274(15):10094-9. DOI: 10.1074/jbc.274.15.10094. View

Mackenzie , McIntosh . Higher plant mitochondria . Plant Cell. 1999; 11(4):571-86. PMC: 144202. DOI: 10.1105/tpc.11.4.571. View

Small I, Suffolk R, Leaver C . Evolution of plant mitochondrial genomes via substoichiometric intermediates. Cell. 1989; 58(1):69-76. DOI: 10.1016/0092-8674(89)90403-0. View

Lupold D, Caoile A, Stern D . Polyadenylation occurs at multiple sites in maize mitochondrial cox2 mRNA and is independent of editing status. Plant Cell. 1999; 11(8):1565-78. PMC: 144286. DOI: 10.1105/tpc.11.8.1565. View

Schmid K, Rosleff Sorensen T, Stracke R, Torjek O, Altmann T, Mitchell-Olds T . Large-scale identification and analysis of genome-wide single-nucleotide polymorphisms for mapping in Arabidopsis thaliana. Genome Res. 2003; 13(6A):1250-7. PMC: 403656. DOI: 10.1101/gr.728603. View

Schuster W, Brennicke A . Conserved sequence elements at putative processing sites in plant mitochondria. Curr Genet. 1989; 15(3):187-92. DOI: 10.1007/BF00435505. View

10.

Stupar R, Lilly J, Town C, Cheng Z, Kaul S, Buell C . Complex mtDNA constitutes an approximate 620-kb insertion on Arabidopsis thaliana chromosome 2: implication of potential sequencing errors caused by large-unit repeats. Proc Natl Acad Sci U S A. 2001; 98(9):5099-103. PMC: 33170. DOI: 10.1073/pnas.091110398. View

11.

Binder S . Mitochondrial nucleic acid purification and analysis. Methods Mol Biol. 1995; 49:383-9. DOI: 10.1385/0-89603-321-X:383. View

12.

Unseld M, Marienfeld J, Brandt P, Brennicke A . The mitochondrial genome of Arabidopsis thaliana contains 57 genes in 366,924 nucleotides. Nat Genet. 1997; 15(1):57-61. DOI: 10.1038/ng0197-57. View

13.

Andre C, Levy A, Walbot V . Small repeated sequences and the structure of plant mitochondrial genomes. Trends Genet. 1992; 8(4):128-32. DOI: 10.1016/0168-9525(92)90370-J. View

14.

Small I, Isaac P, Leaver C . Stoichiometric differences in DNA molecules containing the atpA gene suggest mechanisms for the generation of mitochondrial genome diversity in maize. EMBO J. 1987; 6(4):865-9. PMC: 553476. DOI: 10.1002/j.1460-2075.1987.tb04832.x. View

15.

Notsu Y, Masood S, Nishikawa T, Kubo N, Akiduki G, Nakazono M . The complete sequence of the rice (Oryza sativa L.) mitochondrial genome: frequent DNA sequence acquisition and loss during the evolution of flowering plants. Mol Genet Genomics. 2002; 268(4):434-45. DOI: 10.1007/s00438-002-0767-1. View

16.

Perrin R, Meyer E, Zaepfel M, Kim Y, Mache R, Grienenberger J . Two exoribonucleases act sequentially to process mature 3'-ends of atp9 mRNAs in Arabidopsis mitochondria. J Biol Chem. 2004; 279(24):25440-6. DOI: 10.1074/jbc.M401182200. View

17.

Ullrich H, Lattig K, Brennicke A, Knoop V . Mitochondrial DNA variations and nuclear RFLPs reflect different genetic similarities among 23 Arabidopsis thaliana ecotypes. Plant Mol Biol. 1997; 33(1):37-45. DOI: 10.1023/a:1005720910028. View

18.

Bollenbach T, Lange H, Gutierrez R, Erhardt M, Stern D, Gagliardi D . RNR1, a 3'-5' exoribonuclease belonging to the RNR superfamily, catalyzes 3' maturation of chloroplast ribosomal RNAs in Arabidopsis thaliana. Nucleic Acids Res. 2005; 33(8):2751-63. PMC: 1110743. DOI: 10.1093/nar/gki576. View

19.

Jander G, Norris S, Rounsley S, Bush D, Levin I, Last R . Arabidopsis map-based cloning in the post-genome era. Plant Physiol. 2002; 129(2):440-50. PMC: 1540230. DOI: 10.1104/pp.003533. View

20.

Kuhn K, Weihe A, Borner T . Multiple promoters are a common feature of mitochondrial genes in Arabidopsis. Nucleic Acids Res. 2005; 33(1):337-46. PMC: 546163. DOI: 10.1093/nar/gki179. View