Theoretical and Applied Genetics

, Volume 79, Issue 1, pp 17–27

Recombination of Chlamydomonas chloroplast DNA occurs more frequently in the large inverted repeat sequence than in the single-copy regions

  • B. Lemieux
  • M. Turmel
  • C. Lemieux
Originals

Summary

It is well documented that chloroplast DNA (cpDNA) recombination occurs at a relatively high frequency during sexual reproduction of unicellular green algae from the Chlamydomonas genus. Like the cpDNAs of most land plants, those of Chlamydomonas species are divided into two single-copy regions by a large inverted repeat sequence, part of which encodes the chloroplast rRNA genes. In the present study, we scored the inheritance of polymorphic loci spanning the entire chloroplast genome in hybrids recovered from reciprocal interspecific and F1 crosses between Chlamydomonas eugametes and C. moewusii, and from these data, estimated the density of recombination junctions within each region of recombinant cpDNAs. Our results indicate that recombination junctions occur at highly variable frequencies across the three main domains of the chloroplast genome. The large inverted repeat sequence was found to exhibit at least a five-fold higher density of recombination junctions compared to one of the singlecopy regions, whereas junctions in the latter region were five-fold more abundant relative to those in the other single-copy region. This marked difference in the densities of recombination junctions implies that the extent of genetic linkage between two given chloroplast loci will depend not only on their physical distance, but also on their locations within the genome.

Key words

Chloroplast DNA regions Restriction fragment length polymorphisms Recombination frequency Non-Mendelian inheritance Antibiotic resistance markers 

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References

  1. Aldrich J, Cherney B, Merlin E, Williams C, Mets LJ (1985) Recombination within the inverted repeat sequences of the Chlamydomonas reinhardtii chloroplast genome produces two orientation isomers. Curr Genet 9:233–238Google Scholar
  2. Birky CW, Van Winkle-Swift KP, Sears BB, Boynton JE, Gillham NW (1981) Frequency distributions for chloroplast genes in Chlamydomonas zygote clones: evidence for random drift. Plasmid 6:173–192Google Scholar
  3. Blowers AD, Bogorad L, Shark KB, Sanford JC (1989) Studies on Chlamydomonas chloroplast transformation: foreign DNA can be stably maintained in the chromosome. The Plant Cell 1:123–132Google Scholar
  4. Boynton JE, Gillham NW, Harris EH, Hosler JP, Johnson AM, Jones AR, Randolph-Anderson BL, Robertson D, Klein TM, Shark KB, Sanford JC (1988) Chloroplast transformation in Chlamydomonas with high velocity microprojectiles. Science 240:1534–1538Google Scholar
  5. Cain JR (1979) Survival and mating behavior of progeny and germination of zygotes from intra- and interspecific crosses of Chlamydomonas eugametos and C. moewusii (Chlorophyceae, Volvocales). Phycologia 18:24–29Google Scholar
  6. Cavalier-Smith T (1970) Electron microscopic evidence for chloroplast fusion in zygotes of Chlamydomonas reinhardtii. Nature 228:333–335Google Scholar
  7. Coleman AW, Maguire MJ (1983) Cytological detection of the basis of uniparental inheritance of plastid DNA in Chlamydomonas moewusii. Curr Genet 7:211–218Google Scholar
  8. Dron M, Rahire M, Rochaix J-D (1982) Sequence of the chloroplast DNA region of Chlamydomonas reinhardtii containing the gene for the large subunit of ribulose bisphosphate carboxylase and parts of its flanking genes. J Mol Biol 162:775–793Google Scholar
  9. Erickson JM, Rahire M, Rochaix J-D, Mets LJ (1986) Herbicide resistance and cross-resistance: changes at three distinct sites in the herbicide-binding protein. Science 228:204–207Google Scholar
  10. Gauthier A, Turmel M, Lemieux C (1988) Mapping of chloroplast mutations conferring resistance to antibiotics in Chlamydomonas: evidence for a novel site of streptomycin resistance in the small subunit rRNA. Mol Gen Genet 214:192–197Google Scholar
  11. Gillham NW (1978) Organelle heredity. Raven Press, New YorkGoogle Scholar
  12. Gowans CS (1960) Some genetic investigations on Chlamydomonas eugametos. Z Vererbungsl 91:63–73Google Scholar
  13. Harris EH (1989) The Chlamydomonas sourcebook. Academic Press, San DiegoGoogle Scholar
  14. Harris EH, Boynton JE, Gillham NW, Tingle CL, Fox SB (1977) Mapping of chloroplast genes involved in chloroplast ribosome biogenesis in Chlamydomonas reinhardtii. Mol Gen Genet 155:249–266PubMedGoogle Scholar
  15. Harris EH, Boynton JE, Gillham NW (1987) Interaction of nuclear and chloroplast mutations in biogenesis of chloroplast ribosomes in Chlamydomonas. In: Wiessner W, Robinson DG (eds) Algal development. Molecular and cellular aspects. Springer, Berlin Heidelberg New York, pp 142–149 (Proceedings life sciences)Google Scholar
  16. Harris EH, Burkhart BD, Gillham NW, Boynton JE (1989) Antibiotic resistance mutations in the chloroplast 16S and 23S rRNA genes of Chlamydomonas reinhardtii: correlation of genetic and physical maps of the chloroplast genome. Genetics (in press)Google Scholar
  17. Kuroiwa T, Kawano S, Nishibayashi S, Sato C (1982) Epifluorescent microscopic evidence for maternal inheritance of chloroplast DNA. Nature 298:481–483Google Scholar
  18. Lee RW, Lemieux C (1986) Biparental inheritance of nonMendelian gene markers in Chlamydomonas moewusii. Genetics 113:589–600Google Scholar
  19. Lemieux C, Lee RW (1987) Non-reciprocal recombination between alleles of the chloroplast 23S rRNA gene in interspecific Chlamydomonas crosses. Proc Natl Acad Sci USA 84:4166–4170Google Scholar
  20. Lemieux B, Lemieux C (1985) Extensive sequence rearrangements in the chloroplast genomes of the green algae @@@Chlamydomonas eugametos and Chlamydomonas reinhardtii. Curr Genet 10:213–219Google Scholar
  21. Lemieux C, Turmel M, Lee RW (1981) Physical evidence for recombination of chloroplast DNA in hybrid progeny of Chlamydomonas eugametos and C. moewusii. Curr Genet 3:97–103Google Scholar
  22. Lemieux C, Turmel M, Seligy VL, Lee RW (1984) Chloroplast DNA recombination in interspecific hybrids of Chlamydomonas: linkage between a nonmendelian locus for streptomycin resistance and restriction fragments coding for the 16S rRNA. Proc Natl Acad Sci USA 81:1164–1168Google Scholar
  23. Lemieux B, Turmel M, Lemieux C (1985a) Chloroplast DNA variation in Chlamydomonas and its potential application to the systematics of this genus. BioSystems 18:292–298Google Scholar
  24. Lemieux C, Turmel M, Seligy VL, Lee RW (1985b) The large subunit of ribulose-1,5-bisphosphate carboxylase-oxygenase is encoded in the inverted repeat of the Chlamydomonas eugametos chloroplast genome. Curr Genet 9:139–145Google Scholar
  25. Lemieux C, Turmel M, Lee RW, Bellemare G (1985c) A 21 kilobase-pair deletion/addition difference in the inverted repeat sequence of chloroplast DNA from Chlamydomonas eugametos and C. Moewusii. Plant Mol Biol 5:77–84Google Scholar
  26. Lemieux B, Turmel M, Lemieux C (1988) Unidirectional gene conversions in the chloroplast of Chlamydomonas interspecific hybrids. Mol Gen Genet 212:48–55Google Scholar
  27. Maniatis T, Fritsch EF, Sambrook J (1982) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor/NYGoogle Scholar
  28. Medgyesy P, Fejes E, Maliga P (1985) Interspecific chloroplast recombination in a Nicotiana somatic hybrid. Proc Natl Acad Sci USA 82:6960–6964Google Scholar
  29. Mets LJ, Geist LJ (1983) Linkage of a known chloroplast gene mutation to the uniparental genome of Chlamydomonas reinhardtii. Genetics 105:559–579Google Scholar
  30. Myers AM, Grant DM, Rabert DK, Harris EH, Boynton JE, Gillham NW (1982) Mutants of Chlamydomonas reinhardtii with physical alterations in their chloroplast DNA. Plasmid 7:133–151Google Scholar
  31. Palmer JD, Boynton JE, Gillham NW, Harris EH (1985) Evolution and recombination of the large inverted repeat in Chlamydomonas chloroplast DNA. In: Arntzen C, Bogorad L, Bonitz S, Steinback K (eds) Molecular biology of the photosynthetic apparatus. Cold Spring Harbor Laboratory Press, Cold Spring Harbor/NY, pp 269–278Google Scholar
  32. Rochaix JD (1978) Restriction endonuclease map of the chloroplast DNA of Chlamydomonas reinhardii. J Mol Biol 126:597–617Google Scholar
  33. Southern EM (1975) Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol 98:503–517PubMedGoogle Scholar
  34. Turmel M, Bellemare G, Lemieux C (1987) Physical mapping of differences between the chloroplast DNAs of the interfertile algae Chlamydomonas eugametos and Chlamydomonas moewusii. Curr Genet 11:543–552Google Scholar
  35. Turmel M, Lemieux B, Lemieux C (1988) The chloroplast genome of the green alga Chlamydomonas moewusii: localization of protein-coding genes and transcriptionally active regions. Mol Gen Genet 214:412–419Google Scholar
  36. Van Winkle-Swift KP, Birky CW Jr (1978) The non-reciprocality of organelle gene recombination in Chlamydomonas reinhardtii and Saccharomyces cerevisiae. Mol Gen Genet 166:193–209Google Scholar

Copyright information

© Springer-Verlag 1990

Authors and Affiliations

  • B. Lemieux
    • 1
  • M. Turmel
    • 1
  • C. Lemieux
    • 1
  1. 1.Département de Biochimie, Faculté des Sciences et de GénieUniversité LavalQuébecCanada
  2. 2.MSU/DOE Plant Research LaboratoryEast LansingUSA

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