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. 1997 Nov;147(3):1367–1379. doi: 10.1093/genetics/147.3.1367

Rf8 and Rf* Mediate Unique T-Urf13-Transcript Accumulation, Revealing a Conserved Motif Associated with RNA Processing and Restoration of Pollen Fertility in T-Cytoplasm Maize

C L Dill 1, R P Wise 1, P S Schnable 1
PMCID: PMC1208258  PMID: 9383077

Abstract

Rf8 is a newly described nuclear gene that can substitute for Rf1 to partially restore pollen fertility to male-sterile, T-cytoplasm maize. Families segregating for Rf8 were used to investigate the mechanism of this fertility restoration and to compare it to the restoration conditioned by Rf1. Although Rf8 is unlinked to the rf1 locus, it also alters T-urf13 mitochondrial transcript accumulation and reduces the accumulation of the URF13 protein. Like the 1.6- and 0.6-kilobase (kb) T-urf13 transcripts that accumulate in T-cytoplasm plants carrying Rf1, 1.42- and 0.42-kb transcripts accumulate in plants that are partially restored by Rf8. A survey of T-cytoplasm maize lines, inbreds, and F(1) hybrids by mitochondrial RNA gel blot analyses revealed that Rf8 is rare in maize germplasm. These surveys revealed the presence of another rare, weak restorer factor, Rf*, which is uniquely associated with the accumulation of 1.4- and 0.4-kb T-urf13 transcripts. Primer extension analyses position the 5' termini of the 1.42/0.42-kb and 1.4/0.4-kb transcripts at +137 and +159 nucleotides, respectively, 3' of the AUG initiation codon of the T-urf13 reading frame. The conserved motif, 5'-CNACNNU-3', overlaps the 5' termini of the Rf1-, Rf8-, and Rf*-associated transcripts and the 380 nucleotide, Rf3-associated orf107 transcript from cytoplasmic male sterility sorghum. These results demonstrate that multiple unlinked, nuclear genes can have similar but distinct effects on the expression of the unique T-urf13 mitochondrial coding sequence to restore pollen fertility to T-cytoplasm maize.

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Selected References

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  1. Bailey-Serres J., Hanson D. K., Fox T. D., Leaver C. J. Mitochondrial genome rearrangement leads to extension and relocation of the cytochrome c oxidase subunit I gene in sorghum. Cell. 1986 Nov 21;47(4):567–576. doi: 10.1016/0092-8674(86)90621-5. [DOI] [PubMed] [Google Scholar]
  2. Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1006/abio.1976.9999. [DOI] [PubMed] [Google Scholar]
  3. Braun C. J., Siedow J. N., Levings C. S., 3rd Fungal toxins bind to the URF13 protein in maize mitochondria and Escherichia coli. Plant Cell. 1990 Feb;2(2):153–161. doi: 10.1105/tpc.2.2.153. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Dewey R. E., Levings C. S., 3rd, Timothy D. H. Novel recombinations in the maize mitochondrial genome produce a unique transcriptional unit in the Texas male-sterile cytoplasm. Cell. 1986 Feb 14;44(3):439–449. doi: 10.1016/0092-8674(86)90465-4. [DOI] [PubMed] [Google Scholar]
  5. Dewey R. E., Siedow J. N., Timothy D. H., Levings C. S., 3rd A 13-kilodalton maize mitochondrial protein in E. coli confers sensitivity to Bipolaris maydis toxin. Science. 1988 Jan 15;239(4837):293–295. doi: 10.1126/science.3276005. [DOI] [PubMed] [Google Scholar]
  6. Dewey R. E., Timothy D. H., Levings C. S. A mitochondrial protein associated with cytoplasmic male sterility in the T cytoplasm of maize. Proc Natl Acad Sci U S A. 1987 Aug;84(15):5374–5378. doi: 10.1073/pnas.84.15.5374. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Forde B. G., Leaver C. J. Nuclear and cytoplasmic genes controlling synthesis of variant mitochondrial polypeptides in male-sterile maize. Proc Natl Acad Sci U S A. 1980 Jan;77(1):418–422. doi: 10.1073/pnas.77.1.418. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Gultyaev A. P., van Batenburg F. H., Pleij C. W. The computer simulation of RNA folding pathways using a genetic algorithm. J Mol Biol. 1995 Jun 30;250(1):37–51. doi: 10.1006/jmbi.1995.0356. [DOI] [PubMed] [Google Scholar]
  9. Korth K. L., Kaspi C. I., Siedow J. N., Levings C. S., 3rd URF13, a maize mitochondrial pore-forming protein, is oligomeric and has a mixed orientation in Escherichia coli plasma membranes. Proc Natl Acad Sci U S A. 1991 Dec 1;88(23):10865–10869. doi: 10.1073/pnas.88.23.10865. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Laughnan J. R., Gabay-Laughnan S. Cytoplasmic male sterility in maize. Annu Rev Genet. 1983;17:27–48. doi: 10.1146/annurev.ge.17.120183.000331. [DOI] [PubMed] [Google Scholar]
  11. Levings C. S., 3rd Thoughts on Cytoplasmic Male Sterility in cms-T Maize. Plant Cell. 1993 Oct;5(10):1285–1290. doi: 10.1105/tpc.5.10.1285. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Maloney A. P., Traynor P. L., Levings C. S., 3rd, Walbot V. Identification in maize mitochondrial 26S rRNA of a short 5'-end sequence possibly involved in transcription initiation and processing. Curr Genet. 1989 Mar;15(3):207–212. doi: 10.1007/BF00435507. [DOI] [PubMed] [Google Scholar]
  13. Matthews D. E., Gregory P., Gracen V. E. Helminthosporium maydis Race T Toxin Induces Leakage of NAD from T Cytoplasm Corn Mitochondria. Plant Physiol. 1979 Jun;63(6):1149–1153. doi: 10.1104/pp.63.6.1149. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Potter S., Durovic P., Russell A., Wang X., de Jong-Wong D., Dennis P. P. Preribosomal RNA processing in archaea: characterization of the RNP endonuclease mediated processing of precursor 16S rRNA in the thermoacidophile Sulfolobus acidocaldarius. Biochem Cell Biol. 1995 Nov-Dec;73(11-12):813–823. doi: 10.1139/o95-089. [DOI] [PubMed] [Google Scholar]
  15. Rottmann W. H., Brears T., Hodge T. P., Lonsdale D. M. A mitochondrial gene is lost via homologous recombination during reversion of CMS T maize to fertility. EMBO J. 1987 Jun;6(6):1541–1546. doi: 10.1002/j.1460-2075.1987.tb02398.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Schnable P. S., Wise R. P. Recovery of heritable, transposon-induced, mutant alleles of the rf 2 nuclear restorer of T-cytoplasm maize. Genetics. 1994 Mar;136(3):1171–1185. doi: 10.1093/genetics/136.3.1171. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Singh M., Hamel N., Menassa R., Li X. Q., Young B., Jean M., Landry B. S., Brown G. G. Nuclear genes associated with a single Brassica CMS restorer locus influence transcripts of three different mitochondrial gene regions. Genetics. 1996 May;143(1):505–516. doi: 10.1093/genetics/143.1.505. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Tang H. V., Pring D. R., Shaw L. C., Salazar R. A., Muza F. R., Yan B., Schertz K. F. Transcript processing internal to a mitochondrial open reading frame is correlated with fertility restoration in male-sterile sorghum. Plant J. 1996 Jul;10(1):123–133. doi: 10.1046/j.1365-313x.1996.10010123.x. [DOI] [PubMed] [Google Scholar]
  19. Thomas P. S. Hybridization of denatured RNA and small DNA fragments transferred to nitrocellulose. Proc Natl Acad Sci U S A. 1980 Sep;77(9):5201–5205. doi: 10.1073/pnas.77.9.5201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Wang S., Browning K. S., Miller W. A. A viral sequence in the 3'-untranslated region mimics a 5' cap in facilitating translation of uncapped mRNA. EMBO J. 1997 Jul 1;16(13):4107–4116. doi: 10.1093/emboj/16.13.4107. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Wise R. P., Dill C. L., Schnable P. S. Mutator-induced mutations of the rf1 nuclear fertility restorer of T-cytoplasm maize alter the accumulation of T-urf13 mitochondrial transcripts. Genetics. 1996 Jul;143(3):1383–1394. doi: 10.1093/genetics/143.3.1383. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Wise R. P., Pring D. R., Gengenbach B. G. Mutation to male fertility and toxin insensitivity in Texas (T)-cytoplasm maize is associated with a frameshift in a mitochondrial open reading frame. Proc Natl Acad Sci U S A. 1987 May;84(9):2858–2862. doi: 10.1073/pnas.84.9.2858. [DOI] [PMC free article] [PubMed] [Google Scholar]

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