Abstract
The mitochondrial atp6 gene in male fertile (N) and CMS (S) pepper has previously been compared and was found to be present in two copies (Kim et al. in J Kor Soc Hort Sci 42:121–127 2001). In the current study, these atp6 copies were amplified by an inverse PCR technique, and the coding region as well as the 5′ and 3′ flanking regions were sequenced. The atp6 copies in CMS pepper were detected as one intact gene and one pseudogene, truncated at the 3′ coding region. When the atp6 genes in pepper were compared to other plant species, pepper, potato, and petunia all possessed a sequence of 12 identical amino acids at the 3′ extended region, which was considered a hallmark of the Solanaceae family. Northern blot analysis showed differences in mRNA band patterns between CMS and restorer lines, indicating that atp6 gene is one of the candidates for CMS in pepper.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Akagi H, Sakamoto M, Shinjyo C, Shimada H, Fujimura T (1994) A unique sequence located downstream from the rice mitochondrial atp6 may cause male sterility. Curr Genet 25:52–58
Araya A, Zabaleta E, Blanc V, Begu D, Hernould M, Mouras A, Litvak S (1998) RNA editing in plant mitochondria, cytoplasmic male sterility and plant breeding. Electronic J Biotech 1:31–39
Bland MM, Levings CS III, Matzinger DF (1987) The ATPase subunit 6 gene of tobacco mitochondria contains an unusual sequence. Curr Genet 12:475–481
Dewey RE, Levings CS III, Timothy DH (1985) Nucleotide sequence of ATPase subunit 6 gene of maize mitochondria. Plant Physiol 79:914–919
Dewey RE, Levings CS III, Timothy DH (1986) Novel recombinations in the maize mitochondrial genome produce a unique transcriptional unit in the Texas male-sterile cytoplasm. Cell 44:439–449
Dewey RE, Timothy DH, Levings CS III (1991) Chimeric mitochondrial genes expressed in the C male-sterile cytoplasm of maize. Curr Genet 20:475–482
Grabau E, Havlik M, Gesteland R (1988) Chimeric organization of two genes for the soybean mitochondrial ATPase subunit 6. Curr Genet 13:83–89
Handa H, Nakajima K (1992) Different organization and altered transcription of the mitochondrial atp6 gene in the male-sterile cytoplasm of rapeseed (Brassica napus L.). Curr Genet 21:153–159
Hanson MR (1991) Plant mitochondrial mutations and male sterility. Annu Rev Genet 25:461–486
Hanson M, Bentolila S (2004) Interactions of mitochondrial and nuclear genes that affect male gametophyte development. Plant Cell 16:S154–S169
Hernould M, Suharsono S, Litvak S, Araya A, Mouras A (1993) Male-sterility induction in transgenic tobacco plants with an unedited atp9 mitochondrial gene from wheat. Proc Natl Acad Sci USA 90:2370–2374
Hiesel R, Haeseler A, Brennicke A (1994) Plant mitochondrial nucleic acid sequences as a tool for phylogenetic analysis. Proc Natl Acad Sci USA 18:634–638
Howad W, Kempken F (1997) Cell type-specific loss of atp6 RNA editing in cytoplasmic male sterile Sorghum bicolor. Proc Natl Acad Sci USA 94:11090–11095
Iwabuchi M, Kyozuka J, Shimamoto K (1993) Processing followed by complete editing of an altered mitochondrial atp6 RNA restores fertility of cytoplasmic male sterile rice. EMBO J 12:1437–1446
Kadowaki K, Suzuki T, Kazama S (1990) A chimeric gene containing the 5′ portion of atp6 is associated with cytoplasmic male-sterility of rice. Mol Gen Genet 224:10–16
Kato S, Kanazawa A, Mikami T, Shimamoto Y (1998) Evolutionary changes in the structures of the cox2 and atp6 loci in the mitochondrial genome of soybean involving recombination across small interspersed sequences. Curr Genet 34:303–312
Kempken F, Howad W, Pring DR (1998) Mutations at specific atp6 codons which cause human mitochondrial diseases also lead to male sterility in a plant. FEBS Lett 441:159–160
Kempken F, Mullen JA, Pring DR, Tang HV (1991) RNA editing of sorghum mitochondrial atp6 transcripts changes 15 amino acids and generates a carboxy-terminus identical to yeast. Curr Genet 20:417–422
Kim DH, Kang JG, Kim S, Kim BD (2001) Identification of coxII and atp6 region as associated to CMS in Capsicum annuum by using RFLP and long and accurate PCR. J Kor Soc Hort Sci 42:121–127
Krishnasamy S, Grant RA, Makaroff CA (1994) Subunit 6 of the Fo-ATP synthase complex from cytoplasmic male-sterile radish: RNA editing and NH2-terminal protein sequencing. Plant Mol Biol 24:129–141
Kubo T, Nishizawa S, Mikami T (1999) Alterations in organization and transcription of the mitochondrial genome of cytoplasmic male sterile sugar beet (Beta vulgaris L.). Mol Gen Genet 262:283–290
Kumar R, Levings CS III (1993) RNA editing of a chimeric maize mitochondrial gene transcript is sequence specific. Curr Genet 23:154–159
Loessl A, Adler N, Horn R, Frei U, Wenzel G (1999) Chondriome-type characterization of potato: mt alpha, beta, gamma, delta, epsilon and novel plastid-mitochondrial configurations in somatic hybrids. Theor Appl Genet 99:1–10
Lu B, Hanson MR (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
Makaroff CA, Palmer JD (1988) Mitochondrial DNA rearrangements and transcriptional alterations in the male-sterile cytoplasm of ogura radish. Mol Cell Biol 8:1474–1480
Makaroff CA, Apel IJ, Palmer JD (1989) The atp6 coding region has been disrupted and a novel reading frame generated in the mitochondrial genome of cytoplasmic male-sterile radish. J Biol Chem 264:11706–11713
Marienfeld J, Unseld M, Brandt P, Brennicke A (1996) Genomic recombination of the mitochondrial atp6 gene in Arabidopsis thaliana at the protein processing site creates two different presequences. DNA Res 3:287–290
Michon T, Galante M, Velours J (1988) NH2-terminal sequence of the isolated yeast ATP synthase subunit 6 reveals post-translational cleavage. Eur J Biochem 172:621–625
Peterson PA (1958) Cytoplasmically inherited male sterility in Capsicum. Am Nat 92:111–119
Schnable PS, Wise RP (1998) The molecular basis of cytoplasmic male sterility and fertility restoration. Trends Plant Sci 3:175–180
Schuster W, Brennicke A (1987) Nucleotide sequence of the Oenothera ATPase subunit 6 gene. Nucl Acids Res 15:9092
Sparks RB, Dale RMK (1980) Characterization of 3H-labelled supercoiled mitochondrial DNA from tobacco suspension culture cells. Nucl Acids Res 16:3787–3799
Spassova M, Moneger F, Leaver CJ, Petrov P, Atanassov A, Nijkamp HJ, Hille J (1994) Characterization and expression of the mitochondrial genome of a new type of cytoplasmic male-sterile sunflower. Plant Mol Biol 26:1819–1831
Yoo IW (1990) The inheritance of male sterility and its utilization for breeding in pepper (Capsicum spp.). Ph D Dissertation Kyung Hee University
Acknowledgements
This research was supported by a grant from the Center for Plant Molecular Genetics and Breeding Research (CPMGBR) through the Korea Science and Engineering Foundation (KOSEF) and the Korea Ministry of Science and Technology (MOST).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Ralph Bock
GenBank accession number: DQ126682 (atp6-1 genomic sequence common to fertile and CMS pepper), DQ126681 (Fertile atp6-2 genomic sequence), DQ126680 (CMS pseudo-atp6-2 genomic sequence)
Rights and permissions
About this article
Cite this article
Kim, D.H., Kim, BD. The organization of mitochondrial atp6 gene region in male fertile and CMS lines of pepper (Capsicum annuum L.). Curr Genet 49, 59–67 (2006). https://doi.org/10.1007/s00294-005-0032-3
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00294-005-0032-3