Silent Mitochondrial and Active Nuclear Genes for Subunit 2 of Cytochrome C Oxidase (cox2) in Soybean: Evidence for RNA-mediated Gene Transfer

Overview

Journal EMBO J

Specialties Biotechnology
Molecular Biology

Date 1992 Nov 1

PMID 1382979

Citations 49

Authors

P S Covello

M W Gray

Affiliations

Soon will be listed here.

Abstract

In most plants and other eukaryotes investigated, the mitochondrial genome carries the gene encoding subunit 2 of cytochrome c oxidase (cox2). In this paper, we show that the previously reported mitochondrial cox2 of soybean is actually silent, and that there is an expressed, single-copy, nucleus-encoded cox2. Molecular cloning and sequence analysis of cox2 cDNA and genomic clones show that the soybean nuclear gene encodes an N-terminal extension that resembles a signal sequence for mitochondrial import and whose coding sequence is separated by an intron from that corresponding to mtDNA-encoded cox2. Comparison of soybean mitochondrial and nuclear cox2 sequences clearly indicates that in an ancestor of soybean, cox2 was transferred from the mitochondrion to the nucleus via a C-to-U edited RNA intermediate.

Citing Articles

Targeted knockout of a conserved plant mitochondrial gene by genome editing.

Forner J, Kleinschmidt D, Meyer E, Gremmels J, Morbitzer R, Lahaye T Nat Plants. 2023; 9(11):1818-1831.

PMID: 37814021 PMC: 10654050. DOI: 10.1038/s41477-023-01538-2.

EMP32 is required for the -splicing of intron 2 and seed development in maize.

Yang Y, Ding S, Liu X, Tang J, Wang Y, Sun F RNA Biol. 2020; 18(4):499-509.

PMID: 32936708 PMC: 7971235. DOI: 10.1080/15476286.2020.1817267.

The Roles of Mitochondrion in Intergenomic Gene Transfer in Plants: A Source and a Pool.

Zhao N, Wang Y, Hua J Int J Mol Sci. 2018; 19(2).

PMID: 29439501 PMC: 5855769. DOI: 10.3390/ijms19020547.

Mitochondrial Retroprocessing Promoted Functional Transfers of rpl5 to the Nucleus in Grasses.

Wu Z, Sloan D, Brown C, Rosenblueth M, Palmer J, Ong H Mol Biol Evol. 2017; 34(9):2340-2354.

PMID: 28541477 PMC: 5850859. DOI: 10.1093/molbev/msx170.

Numtogenesis as a mechanism for development of cancer.

Singh K, Choudhury A, Tiwari H Semin Cancer Biol. 2017; 47:101-109.

PMID: 28511886 PMC: 5683947. DOI: 10.1016/j.semcancer.2017.05.003.

References

Gualberto J, Lamattina L, Bonnard G, Weil J, Grienenberger J . RNA editing in wheat mitochondria results in the conservation of protein sequences. Nature. 1989; 341(6243):660-2. DOI: 10.1038/341660a0. View

Gantt J, Baldauf S, Calie P, Weeden N, Palmer J . Transfer of rpl22 to the nucleus greatly preceded its loss from the chloroplast and involved the gain of an intron. EMBO J. 1991; 10(10):3073-8. PMC: 453023. DOI: 10.1002/j.1460-2075.1991.tb07859.x. View

Gray M . The evolutionary origins of organelles. Trends Genet. 1989; 5(9):294-9. DOI: 10.1016/0168-9525(89)90111-x. View

Gray M . Origin and evolution of mitochondrial DNA. Annu Rev Cell Biol. 1989; 5:25-50. DOI: 10.1146/annurev.cb.05.110189.000325. View

Stanford A, Bevan M, Northcote D . Differential expression within a family of novel wound-induced genes in potato. Mol Gen Genet. 1989; 215(2):200-8. DOI: 10.1007/BF00339718. View

Joyce P, Gray M . Chloroplast-like transfer RNA genes expressed in wheat mitochondria. Nucleic Acids Res. 1989; 17(14):5461-76. PMC: 318170. DOI: 10.1093/nar/17.14.5461. View

Holm L, Saraste M, Wikstrom M . Structural models of the redox centres in cytochrome oxidase. EMBO J. 1987; 6(9):2819-23. PMC: 553708. DOI: 10.1002/j.1460-2075.1987.tb02578.x. View

Grabau E . Cytochrome oxidase subunit II gene is adjacent to an initiator methionine tRNA gene in soybean mitochondrial DNA. Curr Genet. 1987; 11(4):287-93. DOI: 10.1007/BF00355402. View

Corpet F . Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res. 1988; 16(22):10881-90. PMC: 338945. DOI: 10.1093/nar/16.22.10881. View

10.

Helms C, Dutchik J, Olson M . A lambda DNA protocol based on purification of phage on DEAE-cellulose. Methods Enzymol. 1987; 153:69-82. DOI: 10.1016/0076-6879(87)53048-8. View

11.

Gellissen G, Michaelis G . Gene transfer. Mitochondria to nucleus. Ann N Y Acad Sci. 1987; 503:391-401. DOI: 10.1111/j.1749-6632.1987.tb40625.x. View

12.

von Heijne G . Why mitochondria need a genome. FEBS Lett. 1986; 198(1):1-4. DOI: 10.1016/0014-5793(86)81172-3. View

13.

Mogen B, MacDonald M, Graybosch R, Hunt A . Upstream sequences other than AAUAAA are required for efficient messenger RNA 3'-end formation in plants. Plant Cell. 1990; 2(12):1261-72. PMC: 159971. DOI: 10.1105/tpc.2.12.1261. View

14.

Palmer J . Contrasting modes and tempos of genome evolution in land plant organelles. Trends Genet. 1990; 6(4):115-20. DOI: 10.1016/0168-9525(90)90125-p. View

15.

Thorsness P, Fox T . Escape of DNA from mitochondria to the nucleus in Saccharomyces cerevisiae. Nature. 1990; 346(6282):376-9. DOI: 10.1038/346376a0. View

16.

Jukes T, Osawa S . The genetic code in mitochondria and chloroplasts. Experientia. 1990; 46(11-12):1117-26. DOI: 10.1007/BF01936921. View

17.

Baldauf S, Palmer J . Evolutionary transfer of the chloroplast tufA gene to the nucleus. Nature. 1990; 344(6263):262-5. DOI: 10.1038/344262a0. View

18.

Hiesel R, Wissinger B, Schuster W, Brennicke A . RNA editing in plant mitochondria. Science. 1989; 246(4937):1632-4. DOI: 10.1126/science.2480644. View

19.

Wolfe K, Li W, Sharp P . Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proc Natl Acad Sci U S A. 1987; 84(24):9054-8. PMC: 299690. DOI: 10.1073/pnas.84.24.9054. View

20.

Cavalier-Smith T . The simultaneous symbiotic origin of mitochondria, chloroplasts, and microbodies. Ann N Y Acad Sci. 1987; 503:55-71. DOI: 10.1111/j.1749-6632.1987.tb40597.x. View