Polyadenylation occurs at multiple sites in maize mitochondrial cox2 mRNA and is independent of editing status

Plant Cell

Volumn 11, Issue 8, 1999, Pages 1565-1577

  Lupold, Shelley D ^a,b   Caoile, Angelina G F S ^b   Stern, David B ^b  

^a Department of Population Medicine and Diagnostic Sciences   (United States)

^b School of Integrative Plant Science   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHLOROPLAST; MESSENGER RNA; MITOCHONDRIAL GENETICS; PLANT GENETICS; POLYADENYLATION;

ANIMALIA; EMBRYOPHYTA; ESCHERICHIA COLI; PROKARYOTA; TRACHEOPHYTA; ZEA MAYS;

EID: 0345580792     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.11.8.1565     Document Type: Article

References (55)

1. Avadhani, N.G. (1979). Messenger ribonucleic acid metabolism in mammalian mitochondria: Relationship between the decay of mitochondrial mRNA and their poly(A). Biochemistry 18, 2673-2678.
2. Bachmann, B., Luke, W., and Hunsmann, G. (1990). Improvement of PCR amplified DNA sequencing with the aid of detergents. Nucleic Acids Res. 18, 1309.
3. Bariola, P.A., Howard, C.J., Taylor, C.B., Verburg, M.T., Jaglan, V.D., and Green, P.J. (1994). The Arabidopsis ribonuclease gene RNS1 is tightly controlled in response to phosphate limitation. Plant J. 6, 673-685.
4. Bellaoui, M., Pelletier, G., and Budar, F. (1997). The steady-state level of mRNA from the Ogura cytoplasmic male sterility locus in Brassica cybrids is determined post-transcriptionally by its 3′ region. EMBO J. 16, 5057-5068.
5. Bhat, G.J., Souza, A.E., Feagin, J.E., and Stuart, K. (1992). Transcript-specific developmental regulation of polyadenylation in Trypanosoma brucei mitochondria. Mol. Biochem. Parasitol. 52, 231-240.
6. Brewer, G., and Ross, J. (1988). Poly(A) shortening and degradation of the 3′ A+U-rich sequences of human c-myc mRNA in a cell-free system. Mol. Cell. Biol. 8, 1697-1708.
7. Cermakian, N., lkeda, T.M., Cedergren, R., and Gray, M.W. (1996). Sequences homologous to yeast mitochondrial and bacteriophage T3 and T7 RNA polymerases are widespread throughout the eukaryotic lineage. Nucleic Acids Res. 24, 648-654.
8. Chang, C., Sheen, J., Bligny, M., Niwa, Y., Lerbs-Mache, S., and Stern, D.B. (1999). Functional analysis of two maize cDNAs encoding T7-like RNA polymerases. Plant Cell, 11, 911-926.
9. Dombrowski, S., Brennicke, A., and Binder, S. (1997). 3′-Inverted repeats in plant mitochondrial mRNAs are processing signals rather than transcription terminators. EMBO J. 16, 5069-5076.
10. Fauron, C.M.R., and Havlik, M. (1988), The BamHI, Xhol, and Smal restriction enzyme maps of the normal maize mitochondrial genome genotype B37. Nucleic Acids Res. 16, 10395-10396.
11. Feagin, J.E., Jasmer, D.P., and Stuart, K. (1985). Apocytochrome b and other mitochondrial DNA sequences are differentially expressed during the life cycle of Trypanosoma brucei. Nucleic Acids Res. 13, 4577-4596.
12. Finnegan, P.M., and Brown, G.G. (1990). Transcriptional and posttranscriptional regulation of RNA levels in maize mitochondria. Plant Cell 2, 71-84.
13. Fox, T.D., and Leaver, C.J. (1981). The Zea mays mitochondrial gene coding cytochrome oxidase subunit II has an intervening sequence and does not contain TGA codons. Cell 26, 315-323.
14. Gagliardi, D., and Leaver, C.J. (1999). Polyadenylation accelerates the degradation of the mitochondrial mRNA associated with cytoplasmic male sterility in sunflower. EMBO J., in press.
15. Gelfand, R., and Attardi, G. (1981). Synthesis and turnover of mitochondrial ribonucleic acid in HeLa cells: The mature ribosomal and messenger ribonucleic acid species are metabolically unstable. Mol. Cell. Biol. 1, 497-511.
16. Gray, M.W. (1992). The endosymbiont hypothesis revisited. Int. Rev. Cytol. 141, 233-357.
17. Groot, G.S., Flavell, R.A., Van Ommen, G.J., and Grivell, L.A. (1974). Yeast mitochondrial RNA does not contain poly(A). Nature 252, 167-169.
18. Hajnsdorf, E., Braun, F., Haugel-Nielsen, J., Le Derout, J., and Regnier, P. (1996). Multiple degradation pathways of the rpsO mRNA of Escherichia coli. RNase E interacts with the 5′ and 3′ extremities of the primary transcript. Biochimie 78, 416-424.
19. Hanic-Joyce, P.J., and Gray, M.W. (1990). Processing of transfer RNA precursors in a wheat mitochondrial extract. J. Biol. Chem. 265, 13782-13791.
20. Haugel-Nielsen, J., Hajnsdorf, E., and Regnier, P. (1996). The rpsO mRNA of Escherichia coli is polyadenylated at multiple sites resulting from endonucleolytic processing and exonucleolytic degradation. EMBO J. 15, 3144-3152.
21. Hayes, R., Kudla, J., and Gruissem, W. (1999). Degrading chloroplast mRNA: The role of polyadenylation. Trends Biochem. Sci. 24, 199-202.
22. Hedtke, B., Borner, T., and Weihe, A. (1997). Mitochondrial and chloroplast phage-type RNA polymerases in Arabidopsis. Science 277, 809-811.
23. Hendler, F.J., Padmanaban, G., Patzer, J., Ryan, R., and Rabinowitz, M. (1975). Yeast mitochondrial RNA contains a short polyadenylic acid segment. Nature 258, 357-359.
24. Hirsch, M., and Penman, S. (1973). Mitochondrial polyadenylic acid-containing RNA: Localization and characterization. J. Mol. Biol. 80, 379-391.
25. Kaleikau, E.K., Andre, C.P., and Walbot, V. (1992). Structure and expression of the rice mitochondrial apocytochrome b gene cob-1 and pseudogene cob-2. Curr. Genet. 22, 463-470.
26. Kempken, F., and Howad, W. (1996). Mitochondrial RNA editing is sequence specific and independent of transcript abundance in Sorghum bicolor. Curr. Genet. 30, 186-189.
27. Koslowsky, D.J., and Yahampath, G. (1997). Mitochondrial mRNA 3′ cleavage/polyadenylation and RNA editing in Trypanosoma brucei are independent events. Mol. Biochem. Parasitol. 90, 81-94.
28. Kudla, J., Hayes, R., and Gruissem, W. (1996). Polyadenylation accelerates degradation of chloroplast mRNA. EMBO J. 15, 7137-7146.
29. Li, Q., and Hunt, A.G. (1997). The polyadenylation of RNA in plants. Plant Physiol. 115, 321-325.
30. Li, Z., Pandit, S., and Deutscher, M.P. (1998). Polyadenylation of stable RNA precursors in vivo. Proc. Natl. Acad. Sci. USA 95, 12158-12162.
31. Lisitsky, I., Klaff, P., and Schuster, G. (1996). Addition of poly(A)-rich sequences to endonucleolytic cleavage sites in the degradation of spinach chloroplast mRNA. Proc. Natl. Acad. Sci. USA 93, 13398-13403.
32. Lisitsky, I., Kotler, A., and Schuster, G. (1997). The mechanism of preferential degradation of polyadenylated RNA in the chloroplast: The exoribonuclease 100RNP-polynucleotide phosphorylase displays high binding affinity for poly(A) sequence. J. Biol. Chem. 272, 17648-17653.
33. Lonsdale, D.M., Hodge, T.P., and Fauron, C.M.-R. (1984). The physical map and organization of the mitochondrial genome from the fertile cytoplasm of maize. Nucleic Acids Res. 12, 9249-9261.
34. Lu, B., and Hanson, M.R. (1992). A single nuclear gene specifies the abundance and extent of RNA editing of a plant mitochondrialtranscript. Nucleic Acids Res. 20, 5699-5703.
35. Maier, R.M., Zeltz, P., Kossel, H., Bonnard, G., Gualberto, J.M., and Grienenberger, J.M. (1996). RNA editing in plant mitochondria and chloroplasts. Plant Mol. Biol. 32, 343-365.
36. Marchfelder, A., and Brennicke, A. (1994). Characterization and partial purification of tRNA processing activities from potato mitochondria. Plant Physiol. 105, 1247-1254.
37. Moore, A.L., and Proudlove, M.O. (1983). Mitochondria and submitochondrial particles. In Isolation of Membranes and Organelles from Plant Cells, A.L. Moore, ed (London: Academic Press), pp. 153-184.
38. Mulligan, P.M., Leon, P., and Walbot, V. (1991). Transcriptional and post-transcriptional regulation of maize mitochondrial gene expression. Mol. Cell. Biol. 11, 533-543.
39. Ojala, D., Montoya, J., and Attardi, G. (1981). tRNA punctuation model of RNA processing in human mitochondria. Nature 290, 470-474.
40. Pereira de Souza, A., Jubier, M.F., Delcher, E., Lancelin, D., and Lejeune, B. (1991). A frans-splicing model for the expression of the tripartite nad5 gene in wheat and maize mitochondria. Plant Cell 3, 1363-1378.
41. Rapp, W.D., and Stern, D.B. (1992). A conserved 11 nucleotide sequence contains an essential promoter element of the maize mitochondrial atp 1 gene. EMBO J. 11, 1065-1073.
42. Rose, K.M., Morris, H.P., and Jacob, S.T. (1975). Mitochondrial poly(A) polymerase from a poorly differentiated hepatoma: Purification and characteristics. Biochemistry 14, 1025-1032.
43. Rothnie, H.M. (1996). Plant mRNA 3′-end formation. Plant Mol. Biol. 32, 43-61.
44. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual, 2nd ed, Vol. 2 (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press).
45. Sarkar, N. (1997). Polyadenylation of mRNA in prokaryotes. Annu. Rev. Biochem. 66, 173-197.
46. Stern, D.B., and Newton, K.J. (1986). Isolation of plant mitochondrial RNA. Methods Enzymol. 118, 488-496.
47. Stern, D.B., Dyer, T.A., and Lonsdale, D.M. (1982). Organization of the mitochondrial ribosomal RNA genes of maize. Nucleic Acids Res. 10, 3333-3340.
48. Tracy, R.L., and Stern, D.B. (1995). Mitochondrial transcription initiation: Promoter structures and RNA polymerases. Curr. Genet. 28, 205-216.
49. Wahle, E., and Keller, W. (1992). The biochemistry of 3′-end cleavage and polyadenylation of messenger RNA precursors. Annu. Rev. Biochem. 61, 419-440.
50. Wilson, R.K., and Hanson, M.R. (1996). Preferential RNA editing at specific sites within transcripts of two plant mitochondrial genes does not depend on transcriptional context or nuclear genotype. Curr. Genet. 30, 502-508.
51. Xu, F., Lin Chao, S., and Cohen, S.N. (1993). The Escherichia coli pcnB gene promotes adenylation of antisense RNAI of ColE1-type plasmids in vivo and degradation of RNAI decay intermediates. Proc. Natl. Acad. Sci. USA 90, 6756-6760.
52. Yang, A.J., and Mulligan, R.M. (1991). RNA editing intermediates of cox2 transcripts in maize mitochondria. Mol. Cell. Biol. 11, 4278-4281.
53. Yen, Y., and Green, P.J. (1991). Identification and properties of the major ribonucleases of Arabidopsis thaliana. Plant Physiol. 97, 1487-1493.
54. Young, D.A., Allen, R.L., Harvey, A.J., and Lonsdale, D.M. (1998). Characterization of a gene encoding a single-subunit bacteriophage-type RNA polymerase from maize that is alternatively spliced. Mol. Gen. Genet. 260, 30-37.
55. Yuckenberg, P.D., and Phillips, S.L. (1982). Oligoadenylate is present in the mitochondrial RNA of Saccharomyces cerevisiae. Mol. Cell. Biol. 2, 450-456.