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Maternal inheritance of cytoplasmic organelles in intergeneric hybrids of Carica papaya L. and Vasconcellea spp. (Caricaceae Dumort., Brassicales)

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Abstract

The mode of inheritance of chloroplast and mitochondrial DNA has been determined in intergeneric hybrids between C. papaya and four different Vasconcellea species by employing a restriction fragment length polymorphism analysis of a PCR-amplified chloroplast and mitochondrial DNA region. Artificial F1 hybrids were produced between a female specimen of C. papaya and male specimens of either V. parviflora, V. goudotiana, V. cundinamarcensis or V. quercifolia. The hybridization patterns of all hybrids correspond in all cases with that of the C. papaya mother, and are different from that of the paternal Vasconcellea species, thus indicating the maternal inheritance of cpDNA and mtDNA in intergeneric hybrids between C. papaya and wild relatives of the Vasconcellea genus.

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Abbreviations

cpDNA:

chloroplast DNA

mtDNA:

mitochondrial DNA

PCR:

polymerase chain reaction

PRSV:

papaya ringspot virus

RFLP:

restriction fragment length polymorphism

References

  • Ahuja, I., P.B. Bhaskar, S.K. Bangal & S.S. Bangal, 2003. Synthesis and cytogenetic characterization of intergeneric hybrids of Diplotaxis siifolia with Brassica rapa and B. juncea. Plant Breed 122: 447–449.

    Article  Google Scholar 

  • Anderson, E.D. & J.N. Owens, 1999. Megagametophyte development, fertilization, and cytoplasmic inheritance in Taxus brevifolia. Int J Plant Sci 160: 459–469.

    Article  Google Scholar 

  • Asadi Abkenar, A., S. Isshiki & Y. Tashiro, 2004. Maternal inheritance of chloroplast DNA in intergeneric sexual hybrids of “true citrus fruit trees” revealed by PCR-RFLP analysis. J Hort Sci Biotechnol 79: 360–363.

    Google Scholar 

  • Banga, S.S., P.B. Bhaskar & I. Ahuja, 2003. Synthesis of intergeneric hybrids and establishment of genomic affinity between Diplotaxis catholica and crop Brassica species. Theor Appl Genet 106: 1244–1247.

    PubMed  Google Scholar 

  • Boblenz, K., T. Nothnagel & M. Metzlaff, 1990. Paternal inheritance of plastids in the genus Daucus. Mol Gen Genet 220: 489–491.

    Article  Google Scholar 

  • Birky, C.W., 1995. Uniparental inheritance of mitochondrial and chloroplast genes: Mechanisms and evolution. Proc Natl Acad Sci 92: 11331–11338.

    PubMed  Google Scholar 

  • Cardi, T., T. Bastia, L. Monti & E.D. Earle, 1999. Organelle DNA and male fertility variation in Solanum spp. and interspecific somatic hybrids. Theor Appl Genet 99: 819–828.

    Google Scholar 

  • Cato, S. & T. Richardson, 1996. Inter- and intraspecific polymorphism at chloroplast SSR loci and the inheritance of plastids in Pinus radiata D. Don. Theor Appl Genet 93: 587–592.

    Google Scholar 

  • Chat, J., L. Chalak & R.J. Petit, 1999. Strict paternal inheritance of chloroplast DNA and maternal inheritance of mitochondrial DNA in intraspecific crosses of kiwifruit. Theor Appl Genet 99: 314–322.

    Article  Google Scholar 

  • Chen, J., C.G. Tauer & Y. Huang, 2002. Paternal chloroplast inheritance in pine hybrids detected with trnL–trnF intergenic region polymorphism. Theor Appl Genet 104: 1307–1311.

    PubMed  Google Scholar 

  • Cipriani, G., R. Testolin & M. Morgante, 1995. Paternal inheritance of plastids in interspecific hybrids of the genus Actinidia revealed by PCR-amplification of chloroplast DNA fragments. Mol Gen Genet 247: 693–697.

    Article  PubMed  Google Scholar 

  • Corriveau, J.L. & A.W. Coleman, 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.

    Google Scholar 

  • Cruzan, M.B., M.L. Arnold, S.E. Carney & K.R. Wollenberg, 1993. cpDNA inheritance in interspecific crosses and evolutionary inference in Louisana irises. Am J Bot 80: 344–350.

    Google Scholar 

  • De Cosa, B., W. Moar, S.B. Lee, M. Miller & H. Daniell, 2001. Overexpression of the Bt Cry2Aa2 operon in chloroplasts leads to formation of insecticidal crystals. Nat Biotechnol 19: 71–74.

    Article  PubMed  Google Scholar 

  • Demesure, B., N. Sodzi & R.J. Petit, 1995. A set of universal primers for amplification of polymorphic non-coding regions of mitochondrial and chloroplast DNA in plants. Mol Ecol 4: 129–131.

    PubMed  Google Scholar 

  • Drew, R.A., 1988. Rapid clonal propagation of papaya in vitro from mature field-grown trees. Hort Sci 23: 60–611.

    Google Scholar 

  • Drew, R.A., 1992. Improved techniques for in vitro propagation and germplasm storage of papaya. Hort Sci 27: 1122–1124.

    Google Scholar 

  • Drew, R.A., C.M. O’Brien & P.M. Magdalita, 1998. Development of interspecific Carica hybrids. Acta Hort 461: 285–292.

    Google Scholar 

  • Dumolin, S., B. Demesure & R.J. Petit, 1995. Inheritance of chloroplast and mitochondrial genomes in pedunculate oak investigated with an efficient PCR-method. Theor Appl Genet 91: 1253–1256.

    Article  Google Scholar 

  • Dumolin-Lapègue, S., M.H. Pemonge & R.J. Petit, 1997. An enlarged set of consensus primers for the study of organelle DNA in plants. Mol Ecol 6: 393–397.

    Article  PubMed  Google Scholar 

  • Earle, E.D., 1995. Mitochondrial DNA in somatic hybrids and cybrids. In: C.S. Levings & I.I.I. Vasil (Eds.), The molecular biology of plant mitochondria, Kluwer Academic Publishers, Dordrecht, pp. 557–584.

    Google Scholar 

  • Fauré, S., J.-L. Noyer, F. Carreel, J.P. Horry, F. Bakry & C. Lanaud, 1994. Maternal inheritance of chloroplast genome and paternal inheritance of mitochondrial genome in bananas (Musa acuminata). Curr Genet 25: 265–269.

    Article  PubMed  Google Scholar 

  • Gastony, G.J. & G. Yatskievych, 1992. Maternal inheritance of the chloroplast and mitochondrial genomes in cheilanthoid ferns. Am J Bot 79: 716–722.

    Google Scholar 

  • Gianordoli, M., 1974. A cytological investigation on gametese and fecundation among Caphalotaxus drupaceae. In: H.F. Linskens (Ed.), Fertilization in higher plants, North-Holland, Amsterdam, pp. 221–232.

  • Gonsalves, D., 1998. Control of papaya ringspot virus in papaya: A case study. Ann Rev Phytol 36: 415–437.

    Article  Google Scholar 

  • Guillon, J.M. & C. Raquin, 2000. Maternal inheritance of chloroplasts in the horsetail Equisetum variegatum (Schleich.). Curr Genet 37: 53–56.

    Article  PubMed  Google Scholar 

  • Hagemann, R., 1992. Plastid genetics in higher plants. In: R.G. Hermann (Ed.), Cell organelles, Springer-Verlag, Wien, Austria, pp. 65–96.

    Google Scholar 

  • Harris, S.A. & R. Ingram, 1991. Chloroplast DNA and biosystematics: The effects of intraspecific diversity and plastid transmission. Taxon 40: 393–412.

    Google Scholar 

  • Heifetz, P.B., 2000. Genetic engineering of the chloroplast. Biochemie 82: 655–666.

    Article  Google Scholar 

  • Hu, Z.M., S.Y. Hu & Z.J. Zhong, 1996. Paternal inheritance of plastid DNA in genus Pharbitis. Acta Bot Sin 38: 253–256.

    Google Scholar 

  • Isshiki, S., T. Uchiyama, Y. Tashiro & S. Miyazaki, 1998. RFLP analysis of a PCR amplified region of chloroplast DNA in eggplant and related Solanum species. Euphytica 102: 295–299.

    Article  Google Scholar 

  • Kaur, D. & S.P. Bhatnagar, 1984. Fertilization and formation of neocytoplasm in Agathis robusta. Phytomorph 34: 56–60.

    Google Scholar 

  • Lakshmi, M., P. Senthilkumar, M. Parani, M.N. Jithesh & A.K. Parida, 2000. PCR-RFLP analysis of chloroplast gene regions in Cajanus (Leguminosae) and allied genera. Euphytica 116: 243–250.

    Article  Google Scholar 

  • Laroche, J., P. Li, L. Maggia & J. Bousquet, 1997. Molecular evolution of angiosperm mitochondrial exons and introns. Proc Natl Acad Sci 94: 5722–5727.

    Article  PubMed  Google Scholar 

  • Ma, X., J.A. Considine & G. Yan, 2004. Chloroplast DNA variation and inheritance in waxflowers. Aust J Bot 52: 55–61.

    Article  Google Scholar 

  • Magdalita, P.M., S.W. Adkins, I.D. Godwin & R.A. Drew, 1996. An improved embryo-rescue protocol for a Carica interspecific hybrid. Aust J Bot 44: 343–353.

    Google Scholar 

  • Magdalita, P.M., R.A. Drew, S.W. Adkins & I.D. Godwin, 1997. Morphological, molecular and cytological analyses of Carica papaya × C. cauliflora interspecific hybrids. Theor Appl Genet 95: 224–229.

    Article  Google Scholar 

  • Manshardt, R.M. & T.F. Wenslaff, 1989. Inter-specific hybridization of papaya with other species. J Am Soc Hort Sci 114: 689–694.

    Google Scholar 

  • Masoud, S.A., L.B. Johnson & E.L. Sorensen, 1990. High transmission of paternal plastid DNA in alfalfa plants demonstrated by restriction fragment polymorphic analysis. Theor Appl Genet 79: 49–55.

    Article  Google Scholar 

  • Milligan, B.G., 1992. Is organelle DNA strictly maternally inherited? Power analysis of binomial distribution. Am J Bot 79: 1325–1328.

    Google Scholar 

  • Mogensen, H.L., 1996. The hows and whys of cytoplasmic inheritance in seed plants. Am J Bot 83: 383–404.

    Google Scholar 

  • Neale, D.B., N. Wheeler & R. Allard, 1986. Paternal inheritance of chloroplast DNA in Douglas-fir. Can J Forest Res 16: 1152–1154.

    Google Scholar 

  • Neale, D.B., K.A. Marshall & R.R. Sederoff, 1989. Chloroplast and mitochondrial DNA are paternally inherited in Sequoia sempervirens D. Don. Endl. Proc Natl Acad Sci 86: 9347–9349.

    Google Scholar 

  • Neale, D.B., K.A. Marshall & D.E. Harry, 1991. Inheritance of chloroplast and mitochondrial DNA in incense cedar (Calocedrus decurrens Torr.). Can J Forest Res 21: 717–720.

    Google Scholar 

  • Neale, D.B. & R.R. Sederoff, 1989. Paternal inheritance of chloroplast DNA and maternal inheritance of mitochondrial DNA in loblolly pine. Theor Appl Genet 77: 212–216.

    Article  Google Scholar 

  • Ogihara, Y., T. Terachi & T. Sasakuma, 1991. Molecular analysis of the hot spot region related to length mutation in wheat chloroplast DNAs. I. Nucleotide divergence of genes and intergenic spacer regions located in the hot spot region. Genetics 129: 321–332.

    Google Scholar 

  • Pennell, R.I. & P.R. Bell, 1988. Insemination of the archegonium and fertilization of in Taxus baccate L. J Cell Sci 89: 551–559.

    Google Scholar 

  • Prakash, S., 2001. Utilization of wild germplasm of Brassica allies in developing cytoplasmic male sterility–fertility restoration systems in Indian mustard Brassica juncea. In: H. Liu & T. Fu (Eds.), Proceedings of the International Symposium on Rapeseed Science, Science Press, New York, pp. 63–67.

  • Reboud, X. & C. Zeyl, 1994. Organelle inheritance in plants. Heredity 72: 132–140.

    Google Scholar 

  • Scheldeman, X., 2002. Distribution and potential of cherimoya (Annona cherimola Mill.) and highland papayas (Vasconcellea spp.) in Ecuador, PhD Thesis, Ghent University, 176 pp.

  • Sewell, M.M., Y.L. Qiu, C.R. Parks & M.W. Chase, 1993. Genetic evidence for trace paternal transmission of plastids in Liriodendron and Magnolia (Magnoliaceae). Am J Bot 80: 854–858.

    Google Scholar 

  • Shore, J.S. & M. Triassi, 1998. Paternally biased cpDNA inheritance in Turnera ulmifolia (Turneraceae). Am J Bot 85: 328–332.

    Google Scholar 

  • Shiriashi, S., H. Maeda, T. Toda, K. Seido & Y. Sasaki, 2001. Incomplete paternal inheritance of chloroplast DNA recognized in Chamaecyparis obtusa using an intraspecific polymorphism of the trnD–trnY intergenic spacer region. Theor Appl Genet 102: 935–941.

    Article  Google Scholar 

  • Smith, S.E., 1989. Biparental inheritance of organelles and its implications in crop improvement. Plant Breed Rev 6: 361–393.

    Google Scholar 

  • Szmidt, A.E., T. Alden & J.E. Hallgren, 1987. Paternal inheritance of chloroplast DNA in Larix. Plant Mol Biol 9: 59–64.

    Article  Google Scholar 

  • Taberlet, P., L. Gielly, G. Pautou & J. Bouvet, 1991. Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Mol Biol 17: 1105–1109.

    Article  PubMed  Google Scholar 

  • Tadashi, H., G.S. Buzard, R.J. Calvert & C.M. Weghorst, 1993. ‘Cold SSCP’: A simple, rapid and non-radioactive method for optimized single-strand conformation polymorphism analyses. Nucl Acids Res 21: 3637–3642.

    PubMed  Google Scholar 

  • Testolin, R. & G. Cipriani, 1997. Paternal inheritance of chloroplast DNA and maternal inheritance of mitochondrial DNA in the genus Actinidia. Theor Appl Genet 94: 897–903.

    Article  Google Scholar 

  • Van Droogenbroeck, B., T. Kyndt, I. Maertens, E. Romeijn-Peeters, X. Scheldeman, J.P. Romero-Motochi, P. Van Damme, P. Goethebeur & G. Gheysen, 2004. Phylogenetic analysis of the highland papayas (Vasconcellea) and allied genera (Caricaceae) using PCR-RFLP. Theor Appl Genet 108: 1473–1486.

    Article  PubMed  Google Scholar 

  • Vendramin, G. & B. Ziegenhagen, 1997. Characterisation and inheritance of polymorphic plastid microsatellites in Abies. Genome 40: 857–864.

    PubMed  Google Scholar 

  • Wagner, D., D. Govindaraju, C. Yeatman & J. Pitel, 1989. Paternal chloroplast DNA inheritance in diallel cross of Jack pine (Pinus banksiana Lamb.). J Hered 80: 483–485.

    Google Scholar 

  • Yamada, A., S. Miyamura & T. Hori, 1993. Cytological study on plastid inheritance of Cryptomeria japonica D. Don. Plant Morphol 5: 19–29.

    Google Scholar 

  • Yang, T.W., Y.A. Yang & Z. Xiong, 2000. Paternal inheritance of chloroplast DNA in interspecific hybrids in the genus Larrea (Zygophyllaceae). Am J Bot 87: 1452–1458.

    PubMed  Google Scholar 

  • Zuccarello, G.C., J.A. West, M. Kamiya & R.J. King, 1999. A rapid method to score plastid haplotypes in red seaweeds and its use in determining parental inheritance of plastids in the red alga Bostrychia (Ceramiales). Hydrobiologia 401: 207–214.

    Article  Google Scholar 

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  1. B. Van Droogenbroeck

    Present address: Department of Plant Systems Biology, Flanders Interuniversitary Institute of Biotechnology, Ghent University, Technologiepark 927, B-9052, Zwijnaarde, Belgium

Authors and Affiliations

  1. Department of Molecular Biotechnology, Faculty of Agricultural and Applied Biological Sciences, Ghent University, Coupure Links 653, B-9000, Gent, Belgium

    B. Van Droogenbroeck, I. Maertens, A. Haegeman, T. Kyndt & G. Gheysen

  2. School of Biomolecular and Biomedical Science, Griffith University, Nathan Campus, Brisbane, Queensland, 4111, Australia

    C. O’Brien & R. A. Drew

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  1. B. Van Droogenbroeck
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  2. I. Maertens
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  3. A. Haegeman
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Van Droogenbroeck, B., Maertens, I., Haegeman, A. et al. Maternal inheritance of cytoplasmic organelles in intergeneric hybrids of Carica papaya L. and Vasconcellea spp. (Caricaceae Dumort., Brassicales). Euphytica 143, 161–168 (2005). https://doi.org/10.1007/s10681-005-3156-0

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