Skip to main content
SpringerLink
Log in

Inheritance of organelle DNA markers in a pea cross associated with nuclear-cytoplasmic incompatibility

  • Original Paper
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

An unusual biparental mode of plastid inheritance was found in pea, in a cross associated with nuclear-cytoplasmic incompatibility manifested as deficiency of chlorophyll pigmentation. Plastid DNA marker trnK and mitochondrial DNA marker cox1 were analyzed in F1 progeny that received cytoplasm from an accession of a wild subspecies Pisum sativum ssp. elatius. Plants with sectors of green tissue on leaves and seed cotyledons with green patches on an otherwise chlorotic background were found to carry paternally inherited plastid DNA, suggesting that photosynthetic function was affected by nuclear-cytoplasmic conflict and required proliferation of paternally inherited plastids for normal performance. The paternally inherited plastid DNA marker was also observed in the roots. The presence of the paternal marker in cotyledons, roots and leaves was independent of each other. Inheritance of the mitochondrial DNA marker cox1 appeared to be of the maternal type.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Aksyonova E, Sinyavskaya M, Danilenko N, Pershina L, Nakamura C, Davydenko O (2005) Heteroplasmy and paternally oriented shift of the organellar DNA composition in barley-wheat hybrids during backcrosses with wheat parents. Genome 48:761–769

    PubMed  CAS  Google Scholar 

  • Allen JO (2005) Effect of teosinte cytoplasmic genomes on maize phenotype. Genetics 169:863–880

    Article  PubMed  CAS  Google Scholar 

  • Anderson JA, Maan SS (1995) Interspecific nuclear-cytoplasmic compatibility controlled by genes on group 1 chromosomes in durum wheat. Genome 38:803–808

    Google Scholar 

  • Ayliffe MA, Scott NS, Timmis JN (1998) Analysis of plastid DNA-like sequences within the nuclear genomes of higher plants. Mol Biol Evol 15:738–745

    PubMed  CAS  Google Scholar 

  • Backert S, Nielsen BL, Borner T (1997) The mystery of the rings: structure and replication of mitochondrial genomes from higher plants. Trends Plant Sci 2:477–483

    Article  Google Scholar 

  • Bendich AJ (2004) Circular chloroplast chromosomes: the grand illusion. Plant Cell 16:1661–1666

    Article  PubMed  CAS  Google Scholar 

  • Birky CW Jr (1973) On the origin of mitochondrial mutants: evidence for intracellular selection of mitochondria in the origin of antibiotic-resistant cells in yeast. Genetics 74:421–432

    PubMed  CAS  Google Scholar 

  • Birky CW Jr (1995) Uniparental inheritance of mitochondrial and chloroplast genes: mechanisms and evolution. Proc Natl Acad Sci USA 92:11331–11338

    Article  PubMed  CAS  Google Scholar 

  • Birky CW Jr (2001) The inheritance of genes in mitochondria and chloroplasts: laws, mechanisms, and models. Annu Rev Genet 35:125–148

    Article  PubMed  CAS  Google Scholar 

  • Blixt S (1972) Mutation genetics in Pisum. Agri Hortique Genetica 30:1–293

    Google Scholar 

  • Bogdanova VS, Berdnikov VA (2001) Observation of a phenomenon resembling hybrid dysgenesis, in a wild pea subspecies Pisum sativum ssp. elatius. Pisum Genetics 33:5–8

    Google Scholar 

  • Bogdanova VS, Kosterin OE (2006) A case of anomalous chloroplast inheritance in crosses of garden pea involving an accession of wild subspecies. Dokl Biol Sci 406:44–46. Translation from Russian

    Google Scholar 

  • Chiu WL, Sears BB (1993) Plastome-genome interactions affect plastid transmission in Oenothera. Genetics 133:989–997

    PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Corriveau JL, Polans NO, Coleman AW (1989) Cultivar variability for the presence of plastid DNA in pollen of Pisum sativum L.: implications for plastid transmission. Curr Genet 16:47–51

    Article  PubMed  CAS  Google Scholar 

  • Fojtova M, Kovarik A, Matyasek R (2001) Cytosine methylation of plastid genome in higher plants. Fact or artefact? Plant Sci 160:585–593

    Article  PubMed  CAS  Google Scholar 

  • Gehlhar SB, Simons KJ, Maan SS, Kianian SF (2005) Genetic analysis of the species cytoplasm specific gene (scs d) derived from durum wheat. J Hered 96:404–409

    Article  PubMed  CAS  Google Scholar 

  • Goloenko IM, Lukhanina NV, Shimkevich AM, Aksyonova EA, Danilenko NG, Davydenko OG (2002) The productivity characteristics of substituted barley lines with marked chloroplast and mitochondrial genomes. Cell Mol Biol Lett 7(2A):483–491

    PubMed  Google Scholar 

  • Gyllensten U, Wharton D, Josefsson A, Wilson AC (1991) Paternal inheritance of mitochondrial DNA in mice. Nature 352:255–257

    Article  PubMed  CAS  Google Scholar 

  • Hanson MR, Bentolila S (2004) Interactions of mitochondrial and nuclear genes that affect male gametophyte development. Plant Cell. 16(Suppl 2004):S154–S169

    Article  PubMed  CAS  Google Scholar 

  • Jenuth JP, Peterson AC, Shoubridge EA (1997) Tissue-specific selection for different mtDNA genotypes in heteroplasmic mice. Nat Genet 16:93–95

    Article  PubMed  CAS  Google Scholar 

  • Kaneda H, Hayashi J, Takahama S, Taya C, Lindahl KF, Yonekawa H (1995) Elimination of paternal mitochondrial DNA in intraspecific crosses during early mouse embryogenesis. Proc Natl Acad Sci USA 92:4542–4546

    Article  PubMed  CAS  Google Scholar 

  • Laser B, Mohr S, Odenbach W, Oettler G, Kück U (1997) Parental and novel copies of the mitochondrial orf25 gene in the hybrid crop-plant triticale: predominant transcriptional expression of the maternal gene copy. Curr Genet 32:337–347

    Article  PubMed  CAS  Google Scholar 

  • Mogensen HL (1996) The hows and whys of cytoplasmic inheritance in seed plants. Am J Bot 83:383–404

    Article  Google Scholar 

  • Moreira CD, Gmitter FG Jr, Grosser JW, Huang S, Ortega VM, Chase CD (2002) Inheritance of organelle DNA sequences in a Citrus-Poncirus intergeneric cross. J Hered 93:174–178

    Article  PubMed  CAS  Google Scholar 

  • Nagata N, Saito C, Sakai A, Kuroiwa H, Kuroiwa T (1999) The selective increase or decrease of organellar DNA in generative cells just after pollen mitosis one controls cytoplasmic inheritance. Planta 209:53–65

    Article  PubMed  CAS  Google Scholar 

  • Neuhaus HE, Emes MJ (2000) Nonphotosynthetic metabolism in plastids. Annu Rev Plant Physiol Plant Mol Biol 51:111–140

    Article  PubMed  CAS  Google Scholar 

  • Polans NO, Corriveau JL, Coleman AW (1990) Plastid inheritance in Pisum sativum L. Curr Genet 18:477–480

    Article  PubMed  CAS  Google Scholar 

  • Race HR, Herrmann RG, Martin W (1999) Why have organelles retained genomes? Trends Genet 15:364–370

    Article  PubMed  CAS  Google Scholar 

  • Ruiz ON, Daniell H (2005) Engineering cytoplasmic male sterility via the chloroplast genome by expression of {beta}-ketothiolase. Plant Physiol 138:1232–1246

    Article  PubMed  CAS  Google Scholar 

  • Schmitz-Linneweber C, Kushnir S, Babiychuk E, Poltnigg P, Herrmann RG, Maier RM (2005) Pigment deficiency in nightshade/tobacco cybrids is caused by the failure to edit the plastid ATPase a-subunit mRNA. Plant Cell 17:1815–1828

    Article  PubMed  CAS  Google Scholar 

  • Schnable PS, Wise RP (1998) The molecular basis of cytoplasmic male sterility and fertility restoration. Trends Plant Sci 3:175–180

    Article  Google Scholar 

  • Simons KJ, Gehlhar SB, Maan SS, Kianian SF (2003) Detailed mapping of the species cytoplasm-specific (scs) gene in durum wheat. Genetics 165:2129–2136

    PubMed  CAS  Google Scholar 

  • Siniavskaia MG, Danilenko NG, Davydenko OG, Ermishina NM, Bel’ko NB, Gordei IA (2004) [Inheritance of organelle DNA in rye (Secale cereale L.) and wheat (x Triticale Thch.) hybrids] Genetika 40:218–223. Russian

    Google Scholar 

  • Soliman K, Fedak G, Allard RW (1987) Inheritance of organelle DNA in barley and Hordeum x Secale intergeneric hybrids. Genome 29:867–872

    CAS  Google Scholar 

  • Storm K, Handig I, Reyniers E, Oostra BA, Kooy RF, Willems PJ (1998) Incomplete EcoRI digestion may lead to false diagnosis of fragile X syndrome. Hum Genet 102:54–56

    Article  PubMed  CAS  Google Scholar 

  • Tsunewaki K, Wang GZ, Matsuoka Y (1996) Plasmon analysis of Triticum (wheat) and Aegilops. 1. Production of alloplasmic common wheats and their fertilities. Genes Genet Syst 71:293–311

    Article  PubMed  CAS  Google Scholar 

  • Tsunewaki K, Wang GZ, Matsuoka Y (2002) Plasmon analysis of Triticum (wheat) and Aegilops. 2. Characterization and classification of 47 plasmons based on their effects on common wheat phenotype. Genes Genet Syst 77:409–427

    Article  PubMed  CAS  Google Scholar 

  • van der Hulst RG, Meirmans P, van Tienderen PH, van Damme JM (2004) Nuclear-cytoplasmic male-sterility in diploid dandelions. Heredity 93:43–50

    Article  PubMed  Google Scholar 

  • Wolfe KH, Li WH, Sharp PM (1987) Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNA. Proc Natl Acad Sci USA 84:9054–9058

    Article  PubMed  CAS  Google Scholar 

  • Zhu T, Mogensen HL, Smith SE (1993) Quantitative, three-dimensional analysis of alfalfa egg cells in two genotypes: implications for biparental plastid inheritance. Planta 190:143–150

    Google Scholar 

Download references

Acknowledgments

The author is very grateful to Dr. Norman Weeden for checking English language and useful comments on the manuscript, to Dr. Oleg Kosterin for fruitful discussion. This work was supported by by the “Biosphere origin and evolution” project of the Russian Academy of Sciences.

Author information

Authors and Affiliations

  1. Institute of Cytology and Genetics, Acad. Lavrentiev ave. 10, Novosibirsk, 630090, Russia

    Vera S. Bogdanova

Authors
  1. Vera S. Bogdanova
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Vera S. Bogdanova.

Additional information

Communicated by R. Hagemann.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bogdanova, V.S. Inheritance of organelle DNA markers in a pea cross associated with nuclear-cytoplasmic incompatibility. Theor Appl Genet 114, 333–339 (2007). https://doi.org/10.1007/s00122-006-0436-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-006-0436-6

Keywords

Search

Navigation