The petunia restorer of fertility protein is part of a large mitochondrial complex that interacts with transcripts of the CMS-associated locus

Plant Journal

Volumn 49, Issue 2, 2007, Pages 217-227

  Gillman, Jason D ^a   Bentolila, Stéphane ^a   Hanson, Maureen R ^a  

^a Department of Molecular Biology and Genetics   (United States)

Author keywords

Cytoplasmic male sterility; Fertility restoration; Mitochondria; Pentatricopeptide repeat

Indexed keywords

CELLS; FERTILIZERS; PLANTS (BOTANY); PROTEINS; RNA;

CYTOPLASMIC MALE STERILITY; FERTILITY RESTORATION; PENTATRICOPEPTIDE REPEAT;

GENES;

MESSENGER RNA; MITOCHONDRIAL PROTEIN; NUCLEAR PROTEIN; VEGETABLE PROTEIN;

ARTICLE; FERTILITY; GEL CHROMATOGRAPHY; GENE; GENETICS; IMMUNOPRECIPITATION; METABOLISM; OPEN READING FRAME; PETUNIA; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSGENIC PLANT;

CHROMATOGRAPHY, GEL; FERTILITY; GENES, PLANT; IMMUNOPRECIPITATION; MITOCHONDRIAL PROTEINS; NUCLEAR PROTEINS; OPEN READING FRAMES; PETUNIA; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER;

CELLS; FERTILIZERS; GENES; MITOCHONDRIA; NUCLEIC ACIDS; PLANTS; PROTEINS;

ARABIDOPSIS; MAMMALIA; PETUNIA;

EID: 33846055504     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2006.02953.x     Document Type: Article

References (39)

1. Alfonso, A.A., Bentolila, S. and Hanson, M.R. (2003) Evaluation of the fertility restoring ability of Rf-PPR592 in Petunia. The Philip Agric Sci, 86, 303-315.
2. Bellaoui, M., Grelon, M., Pelletier, G. and Budar, F. (1999) The restorer Rfo gene acts post-translationally on the stability of the ORF138 Ogura CMS-associated protein in reproductive tissues of rapeseed cybrids. Plant Mol. Biol. 40, 893-902.
3. Bentolila, S. and Hanson, M.R. (2001) Identification of a BIBAC clone that co-segregates with the petunia restorer of fertility (Rf) gene. Mol. Genet. Genomics, 266, 223-230.
4. Bentolila, S., Alfonso, A.A. and Hanson, M.R. (2002) A pentatricopeptide repeat-containing gene restores fertility to cytoplasmic male-sterile plants. Proc. Natl Acad. Sci. USA, 99, 10887-10892.
5. Boeshore, M.L., Lifshitz, I., Hanson, M.R. and Izhar, S. (1983) Novel composition of mitochondrial genomes in petunia somatic hybrids derived from cytoplasmic male sterile and fertile plants. Mol. Gen. Genet. 190, 459-467.
6. Clark, E.M., Izhar, S. and Hanson, M.R. (1985) Independent segregation of the plastid genome and cytoplasmic male sterility in petunia somatic hybrids. Mol. Gen. Genet. 199, 440-445.
7. Fisk, D.G., Walker, M.B. and Barkan, A. (1999) Molecular cloning of the maize gene crp1 reveals similarity between regulators of mitochondrial and chloroplast gene expression. EMBO J. 18, 2621-2630.
8. Fujiki, Y., Fowler, S., Shio, H., Hubbard, A.L. and Lazarow, P.B. (1982) Polypeptide and phospholipid composition of the membrane of rat liver peroxisomes: comparison with endoplasmic reticulum and mitochondrial membranes. J. Cell Biol. 93, 103-110.
9. Glick, B.S. (1995) Pathways and energetics of mitochondrial protein import in Saccharomyces cerevisiae. Methods Enzymol. 260, 224-231.
10. Hanson, M.R. and Bentolila, S. (2004) Interactions of mitochondrial and nuclear genes that affect male gametophyte development. Plant Cell, 16, S154-S169.
11. Hanson, M.R., Boeshore, M.L., McClean, P.E., O'Connell, M.A. and Nivison, H.T. (1988) The isolation of mitochondria and mitochondrial DNA. Methods Enzymol. 118, 257-273.
12. Horsch, R.B., Fry, J.E., Hoffmann, N.L., Eichholtz, D., Rogers, S.G. and Fraley, R.T. (1985) A simple and general method for transferring genes into plants. Science, 227, 1229-1231.
13. Jefferson, R., Kavanagh, T.A. and Bevan, M.W. (1987) GUS fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6, 3901-3907.
14. Koc, E.C. and Spremulli, L.L. (2003) RNA-binding proteins of mammalian mitochondria. Mitochondrion, 2, 277-291.
15. Koizuka, N., Imai, R., Fujimoto, H., Hayakawa, T., Kimura, Y., Kohno-Murase, J., Sakai, T., Kawasaki, S. and Imamura, J. (2003) Genetic characterization of a pentatricopeptide repeat protein gene, orf687, that restores fertility in the cytoplasmic male-sterile Kosena radish. Plant J. 34, 407-415.
16. Krause, K., Lopes de Souza, R., Roberts, D.G. and Dieckmann, C.L. (2004) The mitochondrial message-specific mRNA protectors Cbp1 and Pet309 are associated in a high-molecular weight complex. Mol. Biol. Cell, 15, 2674-2683.
17. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680-685.
18. Lahmy, S., Barneche, F., Derancourt, J., Filipowicz, W., Delseny, M. and Echeverria, M. (2000) A chloroplastic RNA-binding protein is a new member of the PPR family. FEBS Lett. 480, 255-260.
19. Liu, L. and McKeehan, W.L. (2002) Sequence analysis of LRPPRC and its SEC1 domain interaction partners suggests roles in cytoskeletal organization, vesicular trafficking, nucleocytosolic shuttling, and chromosome activity. Genomics, 79, 124-136.
20. Lu, B. and Hanson, M.R. (1994) A single homogeneous form of ATP6 protein accumulates in petunia mitochondria despite the presence of differentially edited atp6 transcripts. Plant Cell, 6, 1955-1968.
21. Lurin, C., Andres, C., Aubourg, S., et al. (2004) Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis. Plant Cell, 16, 2089-2103.
22. Manthey, G.M. and McEwen, J.E. (1995) The product of the nuclear gene PET309 is required for translation of mature mRNA and stability or production of intron-containing RNAs derived from the mitochondrial COX1 locus of Saccharomyces cerevisiae. EMBO J. 14, 4031-4043.
23. Manthey, G.M., Przybyla-Zawislak, B.D. and McEwen, J.E. (1998) The Saccharomyces cerevisiae Pet309 protein is embedded in the mitochondrial inner membrane. Eur. J. Biochem. 255, 156-161.
24. Meierhoff, K., Felder, S., Nakamura, T., Bechtold, N. and Schuster, G. (2003) HCF152, an Arabidopsis RNA binding pentatricopeptide repeat protein involved in the processing of chloroplast psbB-psbT-psbH-petB-petD RNAs. Plant Cell, 15, 1480-1495.
25. Mili, S. and Pinol-Roma, S. (2003) LRP130, a pentatricopeptide motif protein with a noncanonical RNA-binding domain, is bound in vivo to mitochondrial and nuclear RNAs. Mol. Cell. Biol. 23, 4972-4982.
26. Napoli, C.A., Fahy, D., Wang, H.Y. and Taylor, L.P. (1999) white anther: a petunia mutant that abolishes pollen flavonol accumulation, induces male sterility, and is complemented by a chalcone synthase transgene. Plant Physiol. 120, 615-622.
27. Nivison, H.T. and Hanson, M.R. (1989) Identification of a mitochondrial protein associated with cytoplasmic male sterility in petunia. Plant Cell, 1, 1121-1130.
28. Nivison, H.T., Sutton, C.A., Wilson, R.K. and Hanson, M.R. (1994) Sequencing, processing, and localization of the petunia CMS-associated mitochondrial protein. Plant J. 5, 613-623.
29. O'Connell, M.A. and Hanson, M.R. (1985) Regeneration of somatic hybrid plants formed between Lycopersicon esculentum and L. pennellii. Theor. Appl. Genet. 70, 1-12.
30. Pring, D.R., Tang, H.V., Howad, W. and Kempken, F. (1999) A unique two-gene gametophytic male sterility system in sorghum involving a possible role of RNA editing in fertility restoration. J. Hered. 90, 386-393.
31. Pruitt, K.D. and Hanson, M.R. (1991) Transcription of the Petunia mitochondrial CMS-associated pcf locus in male sterile and fertility-restored lines. Mol. Gen. Genet. 227, 348-355.
32. Sakamoto, W., Spielewoy, N., Bonnard, G., Murata, M. and Wintz, H. (2000) Mitochondrial localization of AtOXA1, an Arabidopsis homologue of yeast Oxa1p involved in the insertion and assembly of protein complexes in mitochondrial inner membrane. Plant Cell Physiol. 41, 1157-1163.
33. Schmitz-Linneweber, C., Williams-Carrier, R. and Barkan, A. (2005) RNA immunoprecipitation and microarray analysis show a chloroplast pentatricopeptide repeat protein to be associated with the 5′ region of mRNAs whose translation it activates. Plant Cell, 17, 2791-2804.
34. Small, I.D. and Peeters, N. (2000) The PPR motif - a TPR-related motif prevalent in plant organellar proteins. Trends Biochem. Sci. 25, 46-47.
35. Tang, H.V., Pring, D.R., Shaw, L.C., Salazar, R.A., Muza, F.R., Yan, B. and Schertz, K.F. (1996) Transcript processing internal to a mitochondrial open reading frame is correlated with fertility restoration in male-sterile sorghum. Plant J. 10, 123-133.
36. Touzet, P. and Budar, F. (2004) Unveiling the molecular arms race between two conflicting genomes in cytoplasmic male sterility? Trends Plant Sci. 9, 568-570.
37. Wang, Z., Zou, Y., Li, X. et al. (2006) Cytoplasmic male sterility of rice with boro II cytoplasm is caused by a cytotoxic peptide and is restored by two related PPR motif genes via distinct modes of mRNA silencing. Plant Cell, 18, 676-687.
38. Williams, P.M. and Barkan, A. (2003) A chloroplast-localized PPR protein required for plastid ribosome accumulation. Plant J. 36, 675-686.
39. Young, E.G. and Hanson, M.R. (1987) A fused mitochondrial gene associated with cytoplasmic male sterility is developmentally regulated. Cell, 50, 41-49.