Summary
Nucleocytoplasmic determination of male sterility in Thymus vulgaris L. has been assumed in all papers attempting to explain the remarkably high frequencies of male steriles found in natural populations of this species. This paper provides strong evidence that both nuclear and cytoplasmic genes are involved in the determination of male sterility of this species, giving a complex inheritance. Interpopulation and intrapopulation crosses have shown that the ratio of females versus hermaphrodites among offsprings varied widely from 1∶0 to 1∶1. Furthermore, interpopulation crosses consistently yielded a higher frequency of females than intrapopulation crosses. Nucleocytoplasmic inheritance was demonstrated by an absence of male fertiles in backcrosses and asymmetrical segregation in reciprocal crosses. Molecular analysis of the mitochondrial DNA of some of the parents used in crosses suggested the involvement of different cytoplasms in the inheritance of male steriliy.
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References
Ahokas H (1979) Cytoplasmic male sterility in Barley.III. Maintenance of sterility and restoration of fertility in the msml cytoplasm. Euphytica 28:409–420
Assouad MW (1972) Recherches sur la génétique écologique de Thymus vulgaris L. Etude expérimentale du polymorphisme sexuel. PhD thesis, USTL, Montpellier, France
Bailey-Serres JL, Dixon K, Liddell AD, Leaver CJ (1986) Nuclear-mitochondrial interactions in cytoplasmic male-sterile sorghum. Theor Appl Genet 73:252–260
Belhassen E (1989) Etude évolutive du système reproductif de Thymus vulgaris L.: analyse écologique, génétique, et moléculaire de la stérilité-mâle. PhD thesis, USTL, Montpellier, France
Belhassen E, Trabaud L, Couvet D, Gouyon PH (1989) An example of nonequilibrium process: gynodioecy of Thymus vulgaris L. in burned habitats. Evolution 43:662–667
Belhassen E, Beltran M, Couvet D, Dommée B, Gouyon PH, Olivieri I (1990) Evolution of female frequencies in natural populations of Thyme, Thymus vulgaris L. Two alternative hypotheses accepted. CR Acad Sci Paris Ser III 310:371–375
Belhassen E, Atlan A, Couvet D, Gouyon PH, Quétier F (1990b) Mitochondrial DNA of the Labiate Thymus vulgaris L. is small, highly variable, and maternally inherited. (submitted)
Birky LW Jr (1978) Transmission genetics of mitochondria and chloroplastes. Annu Rev Genet 12:471–512
Bonen L, Boer PH, Gray MW (1984) The wheat cytochrome oxidase subunit II gene has an intron insert and three radical amino acid changes relative to maize. EMBO J 3:2531–2536
Boutin V, Pannenbecker G, Ecke W, Schewe G, Saumitou-Laprade P, Jean R, Vernet P, Michaelis G (1987) Cytoplasmic male sterility and nuclear restorer genes in a natural population of Beta maritima: genetical and molecular aspects. Theor Appl Genet 73:625–629
Boutry M, Faber AM, Charbonnier M, Briquet M (1984) Microanalysis of plant mitochondrial protein synthesis products: detection of variant polypeptides associated with cytoplasmic male sterility. Plant Mol Biol 3:445–452
Charlesworth D (1981) A further study of the problem of maintenance of females in gynodioecious species. Heredity 46:27–39
Correns (1908) Die Rolle der männlichen Keimzellen bei der Geschlechtsbestimmung der gynodiözischen Pflanzen. Ber Dtsch Bot Ges 26a:686–701
Cosmides LM, Tooby J (1981) Cytoplasmic inheritance and intragenomic conflict. J Theor Biol 89:83–129
Couvet D (1984) Ecologie évolutive des populations de Thymus vulgaris L.: pourquoi des femelles? PhD thesis, USTL, Montpellier, France
Couvet D, Gouyon PH, Kjellberg F, Valdeyron G (1985) La différenciation nucléocytoplasmique entre populations: une cause de l'existence de femelles dans les populations naturelles. CR Acad Sci Paris Ser III 300:665–668
Couvet D, Bonnemaison F, Gouyon PH (1986) The maintenance of females among hermaphrodites: the importance of nuclear-cytoplasmic interactions. Heredity 57:325–330
Delannay X, Gouyon PH, Valdeyron G (1981) Mathematical study of the evolution of gynodioecy with cytoplasmic inheritance under the effect of a nuclear restorer gene. Genetics 99:169–181
Dellaporta SL, Wood J, Hicks JB (1983) A plant DNA minipreparation: version II. Plant Mol Biol Rep 1:19–21
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 CL (1982) Mitochondrial gene expression and cytoplasmic male sterility in sorghum. Plant Mol Biol 1:89–102
Dommée B (1973) Recherches sur la génétique écologique de Thymus vulgaris L. Déterminisme génetique et répartition écologique des formes sexuelles. PhD thesis, USTL, Montpellier, France
Dommée B, Jacquard P (1985) Gynodioecy in thyme, Thymus vulgaris L.: evidence from successional populations. In: Jacquard P, Heim G, Antonovics J (eds), Genetic differentiation and dispersal in Plants. Springer, Berlin, pp 141–164
Duc G (1982) La stérilité-mâle nucléo-cytoplasmique chez la féverole (Vicia faba L.). I. Aspects génétiques de la stérilitémâle nucléo-cytoplasmique. Rev Cytol Biol Vég Bot 5:65–69
Duvick DN (1965) Cytoplasmic pollen sterility in corn. Adv Gent 13:1–56
Falconet D, Lejeune B, Quétier F, Gray MW (1984) Evidence for homologous recombination between repeated sequences containing 18S and 5S ribosomal RNA genes in wheat mitochondrial DNA. EMBO J 3:297–302
Ford BG, Leaver CJ (1980) Nuclear and cytoplasmic genes controlling synthesis of variant mitochondrial polypeptides in male-sterile maize. Proc Natl Acad Sci USA 77:418–422
Frank SA (1988) The evolutionary dynamics of cytoplasmic male sterility. Am Nat 133:345–376
Ganders FR (1978) The genetics and evolution of gynodioecy in Nemophila menziesii (Hyedrophyllaceae). Can J Bot 56:1400–1408
Gouyon PH, Couvet D (1985) Selfish cytoplasm and adaptation: variation in the reproductive system of Thymus vulgaris. In: Haeck J, Woldendorp JW (eds), structure and functioning of plant populations 2. North-Holland, Amsterdam, pp 299–320
Grun P (1976) Cytoplasmic genetics and evolution. Columbia University Press. New York
Horovitz A, Dulberger R (1983) The genetic basis of gender in Silene vulgaris. Heredity 51:371–376
Kheyr-Pour A (1980) Nucleocytoplasmic polymorphism for male sterility in Origanum vulgare L. J Hered 71:253–260
Kheyr-Pour A (1981) Wide nucleo cytoplasmic polymorphism for male sterility in Origanum vulgare L. J Hered 72:45–51
Lebacq P, Squalli D, Duchenne M, Pouletty P, Joannes M (1988) A new sensitive non-isotopic method using sulfonated probes to detect picogram quantities of specific DNA sequences on blot hybridization. J Biochem Biophys Methods 15:255–266
Lewis D (1941) Male sterility in natural populations of hermaphrodite plants. New Phytol 40:56–63
Lewis D, Crowe LK (1956) The genetics and evolution of gynodioecy. Evolution 10:115–125
Maan SS, Lucken KA (1972) Interacting male sterility-male fertility restoration systems for hybrid wheat research. Crop Sci 12:360–364
Newton KJ (1988) Plant mitochondrial genomes: organization, expression, and variation. Annu Rev Plant Physiol Plant Mol Biol 39:503–532
Owen FV (1942) Male sterility in sugar beets produced by complementary effects of cytoplasmic and Mendelian inheritance. Am J Bot 29:692 (Abstr)
Pring DR, Lonsdale DM (1985) Molecular biology of higher plant mtDNA. In Int Rev Cytol 97:1–43
Ross MD (1969) Digenic inheritance of male sterility in Plantago lanceolata. Can J Genet Cytol 11:739–744
Rouwendal GJA, Van Damme JMM, Wessels JGH (1987) Cytoplasmic male sterility in Plantago lanceolata L.: differences between male-sterile cytoplasms at the DNA and RNA level. Theor Appl Genet 75:59–65
Schuster W, Brennicke A (1986) Pseudocopies of the ATPase α-subunit gene in Oenothera mitochondria are present on different circular molecules. Mol Gen Genet 294:29–35
Singh A, Laughnan JR (1972) Instability of S male-sterile cytoplasm in maize. Genetics 71:607–620
Sokal RR, Rohlf FJ (1981) Biometry. WH Freeman, New York
Stevens DP, Richards AJ (1985) Gynodioecy in Saxifraga granulata L. (Saxifragaceae). Plant Syst Evol 151:43–54
Tatlioglu T (1987) Genetic control of temperature sensitivity of cytoplasmic male sterility CMS in Chives (Allium schoenopasum L.). Plant Breed 99:65–76
Thiellement H (1982) Cytoplasmic male sterility in Vicia faba L.. Theor Appl Genet 61:47–52
Thompson KF (1972) Cytoplasmic male sterility in oil-seed rape. Heredity 29:253–257
Van Damme JMM (1983) Gynodioecy in Plantago lanceolata L. II. Inheritance of three male sterility types. Heredity 50:253–273
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Belhassen, E., Dommée, B., Atlan, A. et al. Complex determination of male sterility in Thymus vulgaris L.: genetic and molecular analysis. Theoret. Appl. Genetics 82, 137–143 (1991). https://doi.org/10.1007/BF00226204
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DOI: https://doi.org/10.1007/BF00226204