Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

High transmission of paternal plastid DNA in alfalfa plants demonstrated by restriction fragment polymorphic analysis

  • 62 Accesses

  • 49 Citations

Summary

A high frequency of paternal plastid transmission occurred in progeny from crosses among normal green alfalfa plants. Plastid transmission was analyzed by hybridization of radiolabeled alfalfa plastid DNA (cpDNA) probes to Southern blots of restriction digests of the progeny DNA. Each probe revealed a specific polymorphism differentiating the parental plastid genomes. Of 212 progeny, 34 were heteroplastidic, with their cpDNAs ranging from predominantly paternal to predominantly maternal. Regrowth of shoots from heteroplasmic plants following removal of top growth revealed the persistence of mixed plastids in a given plant. However, different shoots within a green heteroplasmic plant exhibited paternal, maternal, or mixed cpDNAs. Evidence of maternal nuclear genomic influence on the frequency of paternal plastid transmission was observed in some reciprocal crosses. A few tetraploid F1 progeny were obtained from tetraploid (2n=4x=32) Medicago sativa ssp. sativa x diploid (2n=2x=16) M. sativa ssp. falcata crosses, and resulted from unreduced gametes. Here more than the maternal genome alone apparently functioned in controlling plastid transmission. Considering all crosses, only 5 of 212 progeny cpDNAs lacked evidence of a definitive paternal plastid fragment.

This is a preview of subscription content, log in to check access.

References

  1. Bingham ET, Hurley LV, Kaatz DM, Saunders JW (1975) Breeding alfalfa which regenerates from callus tissue in culture. Crop Sci 15:719–721

  2. Birky CW Jr (1983) Relaxed cellular controls and organelle heredity. Science 222:468–475

  3. Chiu W-L, Sears BB (1985) Recombination between chloroplast DNAs does not occur in sexual crosses of Oenothera. Mol Gen Genet 198:525–528

  4. Chiu W-L, Stubbe W, Sears BB (1988) Plastid inheritance in Oenothera: organelle genome modifies the extent of biparental plastid transmission. Curr Genet 13:181–189

  5. Cornu A, Dulieu H (1988) Pollen transmission of plastid-DNA under genotypic control in Petunia hybrida Hort. J Hered 79:40–44

  6. Corriveau JL, Coleman AW (1988) Rapid screening method to detect potential biparental inheritance of plastid DNA and results for over 200 Angiosperm species. Am J Bot 75:1443–1458

  7. Gillham NW (1978) Organelle heredity. Raven Press, New York

  8. Harnes BD (1981) An introduction to polyacrylamide gel electrophoresis. In: Hames BD, Rickwood D (eds) Gel electrophoresis of proteins, a practical approach. Practical Approaches Series. IRL Press, Oxford, pp 1–91

  9. Johnson LB, Palmer JD (1989) Heteroplasmy of chloroplast DNA in Medicago. Plant Mol Biol 12:3–11

  10. Kirk JTO, Tilney-Bassett RAE (1978) The plastids: Their chemistry, structure, growth, and inheritance, 2nd edn. Elsevier/North-Holland Biomedical Press, Amsterdam

  11. Lee DJ, Blake TK, Smith SE (1988) Biparental inheritance of chloroplast DNA and the existence of heteroplasmic cells in alfalfa. Theor Appl Genet 76:545–549

  12. Lee DJ, Blake TK, Smith SE, Bingham ET, Carroll TW (1989) Chloroplast genome mapping and plastid ultrastructure analysis of chlorophyll deficient mutants of alfalfa. Crop Sci 29:190–196

  13. Lesins KA, Lesins I (1979) Genus Medicago (Leguminosae), a taxogenetic study. W. Junk, The Hague

  14. Lilienfeld FA (1962) Plastid behavior in reciprocally different crosses between two races of Medicago truncatula Gaertn. Seiken Zihô 13:3–38

  15. Maniatis T, Fritsch EF, Sambrook J (1982) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor/NY

  16. Medgyesy P, Fejes E, Maliga P (1985) Interspecific chloroplast recombination in a Nicotiana somatic hybrid. Proc Natl Acad Sci USA 82:6960–6964

  17. Metzlaff M, Borner T, Hagemann R (1981) Variations of chloroplast DNAs in the genus Pelargonium and their biparental inheritance. Theor Appl Genet 60:37–41

  18. Miyamura S, Kuroiwa T, Nagata T (1987) Disappearance of plastid and mitochondrial nucleoids during the formation of generative cells of higher plants revealed by fluorescence microscopy. Protoplasma 141:149–159

  19. Molin WT, Meyers SP, Baer GR, Schrader LE (1982) Ploidy effects in isogenic populations of alfalfa. II. Photosynthesis, chloroplast number, ribulose-1,5-bisphosphate carboxylase, chlorophyll, and DNA in protoplasts. Plant Physiol 70:1710–1714

  20. Neale DB, Sederoff RR (1989) Paternal inheritance of chloroplast DNA and maternal inheritance of mitochondrial DNA in loblolly pine. Theor Appl Genet 77:212–216

  21. Palmer JD (1986) Isolation and structural analysis of chloroplast DNA. Methods Enzymol 118:167–186

  22. Palmer JD, Osorio B, Aldrich J, Thompson WF (1987) Chloroplast DNA evolution among legumes: Loss of a large inverted repeat occurred prior to other sequence rearrangements. Curr Genet 11:275–286

  23. Pankiw P, Siemens B (1976) Anik alfalfa. Can J Plant Sci 56:203–205

  24. Pfeiffer TW, Bingham ET (1983) Abnormal meiosis in alfalfa, Medicago sativa: cytology of 2 N egg and 4 N pollen formation. Can J Genet Cytol 25:107–112

  25. Pyke KA, Leech RM (1987) The control of chloroplast number in wheat mesophyll cells. Planta 170:416–420

  26. Quiros CF (1981) Starch gel electrophoresis technique used with alfalfa and other Medicago species. Can J Plant Sci 61:745–749

  27. Reed KC, Mann DA (1985) Rapid transfer of DNA from agarose gels to nylon membranes. Nucleic Acids Res 13:7207–7221

  28. Rogers SO, Bendich AJ (1985) Extraction of DNA from milligram amounts of fresh, herbarium and mummified plant tissues. Plant Mol Biol 5:69–76

  29. Rose RJ, Johnson LB, Kemble RJ (1986) Restriction endonuclease studies on the chloroplast and mitochondrial DNAs of alfalfa (Medicago sativa L.) protoclones. Plant Mol Biol 6:331–338

  30. Scowcroft WR, Larkin PJ (1981) Chloroplast DNA assorts randomly in intraspecific somatic hybrids of Nicotiana debneyi. Theor Appl Genet 60:179–184

  31. Smith SE, Bingham ET, Fulton RW (1986) Transmission of chlorophyll deficiencies in Medicago sativa, evidence for biparental inheritance of plastids. J Hered 77:35–38

  32. Snow R (1963) Alcoholic hydrochloric acid-carmine as a stain for chromosomes in squash preparations. Stain Technol 38:9–13

  33. Szmidt AE, Aldén T, Hällgren J-E (1987) Paternal inheritance of chloroplast DNA in Larix. Plant Mol Biol 9:59–64

  34. Thanh ND, Medgyesy P (1989) Limited chloroplast gene transfer via recombination overcomes plastome-genome incompatibility between Nicotiana tabacum and Solanum tuberosum. Plant Mol Biol 12:87–93

  35. Tilney-Bassett RAE, Abdel-Wahab OAL (1982) Irregular segregation at the Pr locus controlling plastid inheritance in Pelargonium; gametophytic lethal or incompatibility system? Theor Appl Genet 62:187–191

  36. Tilney-Bassett RAE, Birky CW Jr (1981) The mechanism of the mixed inheritance of chloroplast genes in Pelargonium. Evidence from gene frequency distributions among the progeny of crosses. Theor Appl Genet 60:43–53

  37. Viands DR, Sun P, Barnes DK (1988) Pollination control: mechanical and sterility. In: Hanson AA, Barnes DK, Hill RR Jr (eds) Alfalfa and alfalfa improvement. Agron. Monogr 29. Am Soc Agron, Crop Sci Soc Am, and Soil Sci Soc Am, Madison, pp 931–960

  38. Wagner DB, Furnier GR, Saghai-Maroof MA, Williams SM, Dancik BP, Allard RW (1987) Chloroplast DNA polymorphisms in lodgepole and jack pines and their hybrids. Proc Natl Acad Sci USA 84:2097–2100

Download references

Author information

Additional information

Contribution No. 89-524-J from the Kansas Agricultural Experiment Station, Kansas State University, Manhattan

Communicated by R. Hagemann

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Masoud, S.A., Johnson, L.B. & Sorensen, E.L. High transmission of paternal plastid DNA in alfalfa plants demonstrated by restriction fragment polymorphic analysis. Theoret. Appl. Genetics 79, 49–55 (1990). https://doi.org/10.1007/BF00223786

Download citation

Key words

  • Chloroplast DNA
  • Medicago sativa
  • Maternal plastid transmission
  • Biparental plastid inheritance
  • Heteroplasmy