Summary
Nuclear influences on mitochondrial transcription and genome organization were analysed in six different male-fertile and male-sterile alloplasmic Nicotiana cultivars. The alloplasmic materials were compared with the corresponding nuclear species (N. tabacum) and cytoplasmic donor species (N. debneyi, N. rapanda or N. suaveolens) in Northern and Southern analyses using twelve different mitochondrial genes as probes. The investigation revealed that the nucleus exerts extensive influence on the expression and structure of the mitochondrial genome. For the majority of the probes, changes in both mitochondrial transcription and DNA patterns in alloplasmic cultivars were detected. Even though changes in transcription patterns, which correlated with male sterility, were detected for three of the probes (atpA, orf25 and coxII), the changes were not consistent for all the male-sterile materials. Likewise, no consistent association between mtDNA restriction patterns and cytoplasmic male sterility (CMS) was detected.
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References
Attardi G, Schatz G (1988) Biogenesis of mitochondria. Annu Rev Cell Biol 4:289–333
Bailey-Serres J, Dixon LK, Liddell AD, Leaver CJ (1986) Nuclear-mitochondrial interactions in cytoplasmic male-sterile sorghum. Theor Appl Genet 73:252–260
Bland MM, Matzinger DF, Levings CS III (1985) Comparison of the mitochondrial genome of Nicotiana tabacum with its progenitor species. Theor Appl Genet 69:535–541
Bland MM, Levings CS III, Matzinger DF (1986) The tobacco mitochondrial ATPase subunit 9 gene is closely linked to an open reading frame for a ribosomal protein. Mol Gen Genet 204:8–16
Bonen L, Bird S (1988) Sequence analysis of the wheat mitochondrial atp6 gene reveals a fused upstream reading frame and markedly divergent N-termini among plant ATP6 proteins. Gene 73:47–56
Bonen L, Gray MW (1980) Organization and expression of the mitochondrial genome of plants I. The genes for wheat mitochondrial ribosomal and transfer RNA: evidence for an unusual arrangement. Nucleic Acids Res 8:319–335
Bonen L, Boer PH, McIntosh JE, Gray MW (1987) Nucleotide sequence of the wheat mitochondrial gene for subunit I of cytochrome oxidase. Nucleic Acids Res 15:6734
Braun CJ, Levings CS III (1985) Nucleotide sequence of the F1-ATPase alpha subunit gene from maize mitochondria. Plant Physiol 79:571–577
Breiman A, Galun E (1990) Nuclear-mitochondrial interrelation in angiosperms. Plant Sci 71:3–19
Burk LG (1967) An interspecific bridge-cross: Nicotiana repanda through N. sylvestris to N. tabacum. J Hered 58:215–218
Burns JA, Gerstel DU (1981) Role of nucleolar chromosomes in anther-restoration of male-sterile tobacco. J Hered 72:413–318
Burns JA, Gerstel DU, Sand SA (1978) Cytoplasmic male sterility in Nicotiana, restoration of fertility, and the nucleolus. II. N. debneyi cytoplasm. Genetics 90:151–159
Cooper P, Newton KJ (1989) Maize nuclear background regulates the synthesis of a 22-kDa polypeptide in Zea luxurians mitochondria. Proc Natl Acad Sci USA 86:7423–7426
Cooper P, Butler E, Newton KJ (1990) Identification of a maize nuclear gene which influences the size and number of cox2 transcripts in mitochondria of perennial teosintes. Genetics 126:461–467
Dale RMK, Mendu N, Ginsburg H, Kridl JC (1984) Sequence analysis of the maize mitochondrial 26S rRNA gene and flanking regions. Plasmid 11:141–150
Dawson AJ, Jones VP, Leaver CJ (1984) The apocytochrome b gene in maize mitochondria does not contain introns and is preceded by a potential ribosome binding site. EMBO J 3:2107–2113
Day DA, Neuburger M, Douce R (1985) Biochemical characterization of chlorophyll-free mitochondria from pea leaves. Aust J Plant Physiol 12:219–228
De Paepe R, Chétrit P, Vitart V, Ambard-Bretteville F, Prat D, Vedel F (1990) Several nuclear genes control both male sterility and mitochondrial protein synthesis in Nictotiana sylvestris protoclones. Mol Gen Genet 222:206–210
Dewey RE, Levings CS III, Timothy DH (1985 a) Nucleotide sequence of ATPase 6 subunit gene of maize mitochondria. Plant Physiol 79:914–919
Dewey RE, Schuster AM, Levings CS III, Timothy DH (1985 b) Nucleotide sequence of F0-ATPase proteolipid (subunit 9) gene of maize mitochondria. Proc Natl Acad Sci USA 82:1015–1019
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 (1987) A mitochondrial protein associated with cytoplasmic male sterility in the T cytoplasm of maize. Proc Natl Acad Sci USA 84:5374–5378
Dixon LK, Leaver CJ (1982) Mitochondrial gene expression and cytoplasmic male sterility in sorghum. Plant Mol Biol 1: 89–102
Duchenne M, Lejeune B, Fouillard P, Quetier F (1989) Comparison of the organization and expression of mtDNA of fertile and male-sterile sugar beet varieties (Beta vulgaris L.). Theor Appl Genet 78:633–640
Escote-Carlson LJ, Gabay-Laughnan S, Laughnan JR (1990) Nuclear genotype affects mitochondrial genome organization of CMS-S maize. Mol Gen Genet 223:457–464
Fox TD, Leaver CJ (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
Gerstel DU, Burns JA, Burk LG (1978) Cytoplasmic male sterility in Nicotiana, restoration of fertility, and the nucleolus. Genetics 89:157–169
Gualberto JM, Wintz H, Weil J-H, Grienenberger J-M (1988) The genes coding for subunit 3 of NADH dehydrogenase and for ribosomal protein S12 are present in the wheat and maize mitochondrial genomes and are cotranscribed. Mol Gen Genet 215:118–127
Gwynn B, Dewey RE, Sederoff RR, Timothy DH, Levings CS III (1987) Sequence of the 18S-5S ribosomal gene region and the cytochrome oxidase II gene from mtDNA of Zea diploperennis. Theor Appl Genet 74:781–788
Håkansson G, van der Mark F, Bennett HT, Glimelius K (1988) Variant mitochondrial protein and DNA patterns associated with cytoplasmic male-sterile lines of Nicotiana. Theor Appl Genet 78:431–437
Hosfield GL, Wernsman EA (1974) Effect of an alien cytoplasm and fertility restoring factor on growth, agronomic characters, and chemical constituents in a male-sterile variety of flue-cured tobacco. Crop Science 14:575–577
Kaul MLH (1988) Male sterility in higher plants. In: Frankel R, Grossman M, Linskens HF, Maliga P, Riley R (eds) Monographs on Theoretical and Applied Genetics, vol 10. Springer-Verlag, Berlin
Kennell JC, Wise RP, Pring DR (1987) Influence of nuclear background on transcription of a maize mitochondrial region associated with Texas male sterile cytoplasm. Mol Gen Genet 210:399–406
Kofer W, Glimelius K, Bonnett HT (1991) Modifications of mitochondrial DNA cause changes in floral development in homeotic-like mutants of tobacco. Plant Cell 3 (8)
Köhler HR, Lössl A, Zetsche K (1991) Cytoplasmic male sterility in sunflower is correlated with the cotranscription of a new open reading frame with the atpA gene. Mol Gen Genet (in press)
Landgren M, Glimelius K (1990) Analysis of chloroplast and mitochondrial segregation in three different combinations of somatic hybrids produced within Brassicaceae. Theor Appl Genet 80:776–784
Leaver CJ, Hack E, Dawson AJ, Isaac PG, Jones VP (1983) Mitochondrial genes and their expression in higher plants. In: Schweyen RJ, Wolf K, Kandewitz F (eds) Mitochondria 1983. Walter de Gruyter, Berlin New York, pp 269–283
Levings CS III, Brown GG (1989) Molecular biology of plant mitochondria. Cell 56:171–179
Mackenzie SA, Pring DR, Bassett MJ, Chase CD (1988) Mitochondrial DNA rearrangement associated with fertility restoration and cytoplasmic reversion to fertility in cytoplasmic male sterile Phaseolus vulgaris L. Proc Natl Acad Sci USA 85:2714–2717
Makaroff CA, Palmer JD (1987) Extensive mitochondrial-specific transcription of the Brassica campestris mitochondrial genome. Nucleic Acids Res 15:5141–5156
Mulligan RM, Maloney AP, Walbot V (1988) RNA processing and multiple transcription initiation sites result in transcript size heterogeneity in maize mitochondria. Mol Gen Genet 211:373–380
Newton KJ, Coe EH Jr (1986) Mitochondrial DNA changes in abnormal growth (nonchromosomal stripe) mutants of maize. Proc Natl Acad Sci USA 83:7363–7366
Nivison HT, Hanson MR (1989) Identification of a mitochondrial protein associated with cytoplasmic male sterility in petunia. Plant Cell 1:1121–1130
Reed SM, Burns JA (1986) Cross-restoration between Nicotiana cytoplasmic male-sterile and restored lines. J Hered 77:159–163
Saalaoui E, Litvak S, Araya A (1990) The apocytochrome b from an alloplasmic line of wheat (T. aestivum, cytoplasm-T. timopheevi) exists in two differently expressed forms. Plant Sci 66:237–246
Sambrook E, Fritsch F, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York
Sand SA, Christoff GT (1973) Cytoplasmic-chromosomal interactions and altered differentiation in tobacco. J Hered 64:24–30
Schmitz UK, Michaelis G (1988) Dwarfism and male sterility in interspecific hybrids of Epilobium. 2. Expression of mitochondrial genes and structure of the mitochondrial DNA. Theor Appl Genet 76:565–569
Schweppenhauser MA, Mann TJ (1968) Restoration of staminal fertility in Nicotiana by introgression. Can J Genet Cytol 10:401–411
Small ID, Isaac PG, Leaver CJ (1987) Stoichiometric differences in DNA molecules containing the atpA gene suggest mechanisms for the generation of mitochondrial genome diversity in maize. EMBO J 6:865–869
Stamper SE, Dewey RE, Bland MM, Levings CS III (1987) Characterization of the urf13-T and an unidentified reading frame, ORF 25, in maize and tobacco mitochondria. Curr Genet 12:457–463
Stern DB, Bang AG, Thompson WF (1986) The watermelon mitochondrial URF-1 gene: evidence for a complex structure. Curr Genet 10:857–869
Taylor WC (1989) Regulatory interactions between nuclear and plastid genomes. Annu Rev Plant Physiol Plant Mol Biol 40:211–233
Tzagoloff A, Myers AM (1986) Genetics of mitochondrial biogenesis. Annu Rev Biochem 55:249–285
Verwoerd TC, Dekker BMM, Hoekema A (1989) A small-scale procedure for the rapid isolation of plant RNAs. Nucleic Acids Res 17:2362
Walker NH, Qin J, Abbott AG (1987) Northern hybridization analysis of mitochondrial gene expression in maize cytoplasm with varied nuclear background. Theor Appl Genet 74:531–537
Wintz H, Chen H-C, Pillay DTN (1989) Partial characterization of the gene coding for subunit IV of soybean mitochondrial NADH dehydrogenase. Curr Genet 15:155–160
Wissinger B, Hiesel R, Schuster W, Brennicke A (1988) The NADH-dehydrogenase subunit 5 gene in Oenothera mitochondria contains two introns and is cotranscribed with the 5S rRNA gene. Mol Gen Genet 212:56–65
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Communicated by D.M. Lonsdale
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Håkansson, G., Glimelius, K. Extensive nuclear influence on mitochondrial transcription and genome structure in male-fertile and male-sterile alloplasmic Nicotiana materials. Molec. Gen. Genet. 229, 380–388 (1991). https://doi.org/10.1007/BF00267459
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DOI: https://doi.org/10.1007/BF00267459