Skip to main content
SpringerLink
Log in

Nicotiana debneyi has a single dominant gene causing hybrid lethality in crosses with N. tabacum

  • Published:
Euphytica Aims and scope Submit manuscript

Abstract

To elucidate the genetic mechanism of hybrid lethality observed in hybrids between cultivated tobacco, Nicotiana tabacum, and wild tobacco species in the section Suaveolentes, genetic analyses were conducted through the triple cross of the hybrids of wild species, including N. benthamiana and N. fragrans, and N. tabacum. N. benthamiana and N. fragrans produced only viable hybrids after crossing with N. tabacum. Subsequently, N. benthamiana and N. fragrans were crossed with N. africana, N. debneyi, and/or N. suaveolens, which produced inviable hybrids after crossing with N. tabacum. Hybrids of the wild species were obtained from four of the six cross combinations. Only when hybrid plants of N. debneyi × N. fragrans, whose hybridity was confirmed by morphological characteristics, random amplified polymorphic DNA analysis, and chromosome observation, were crossed with N. tabacum, triple hybrids were obtained and segregated 1:1 (lethal:viable). Based on these results, a single dominant gene, designated Hybrid Lethality A1 (HLA1), in N. debneyi was found to control hybrid lethality by the interaction with gene(s) on the Q chromosome in N. tabacum. This represents the first report to identify a causal gene for hybrid lethality in the genus Nicotiana.

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

Similar content being viewed by others

References

  • Bomblies K, Lempe J, Epple P, Warthmann N, Lanz C, Dangl JL, Weigle D (2007) Autoimmune response as a mechanism for a Dobzhansky–Muller type incompatibility syndrome in plants. PLoS Biol 5:e236

    Article  PubMed  Google Scholar 

  • Chase MW, Knapp S, Cox AV, Clarkson JJ, Butsko Y, Joseph J, Savolainen V, Parokonny AS (2003) Molecular systematics, GISH and the origin of hybrid taxa in Nicotiana (Solanaceae). Ann Bot 92:107–127

    Article  PubMed  CAS  Google Scholar 

  • Clarkson JJ, Knapp S, Garcia VF, Olmstead RG, Leitch AR, Chase MW (2004) Phylogenetic relationships in Nicotiana (Solanaceae) inferred from multiple plastid DNA region. Mol Phylogenet Evol 33:75–90

    Article  PubMed  CAS  Google Scholar 

  • Clarkson JJ, Kelly LJ, Leitch AR, Knapp S, Chase MW (2010) Nuclear glutamine synthetase evolution in Nicotiana: phylogenetics and the origin of allotetraploid and homoploid (diploid) hybrids. Mol Phylogenet Evol 55:99–112

    Article  PubMed  CAS  Google Scholar 

  • Comai L (2000) Genetic and epigenetic interaction in allopolyploid plants. Plant Mol Biol 43:387–399

    Article  PubMed  CAS  Google Scholar 

  • Coyne JA, Orr HA (2004) Speciation. Sinauer Associates, Sunderland

    Google Scholar 

  • DeVerna JW, Myers JR, Collins GB (1987) Bypassing prefertilization barriers to hybridization in Nicotiana using in vitro pollination and fertilization. Theor Appl Genet 73:665–671

    Article  Google Scholar 

  • Gerstel DU, Burns JA, Burk LG (1979) Interspecific hybridization with an African tobacco, Nicotiana africana Merxm. J Hered 70:342–344

    Google Scholar 

  • Ichitani K, Namigoshi K, Sato M, Taura S, Aoki M, Matsumoto Y, Saitou T, Marubashi W, Kuboyama T (2007) Fine mapping and allelic dosage effect of Hwc1, a complementary hybrid weakness gene in rice. Theor Appl Genet 114:1407–1415

    Article  PubMed  CAS  Google Scholar 

  • Jeuken MJW, Zhang NW, McHale LK, Pelgrom K, den Boer E, Lindhout P, Michelmore RW, Visser RGF, Niks RE (2009) Rin4 causes hybrid necrosis and race-specific resistance in an interspecific lettuce hybrid. Plant Cell 21:3368–3378

    Article  PubMed  CAS  Google Scholar 

  • Kobori S, Marubashi W (2004) Programmed cell death detected in interspecific hybrids of Nicotiana repanda × N. tomentosiformis expressing hybrid lethality. Breed Sci 54:347–350

    Article  Google Scholar 

  • Kuboyama T, Sato T, Matsumoto T, Wu J, Kanamori H, Taura S, Sato M, Marubashi W, Ichitani K (2009) Fine mapping of HWC2, a complementary hybrid weakness gene, and haplotype analysis around the locus in rice. Rice 2:93–103

    Article  Google Scholar 

  • Ladiges PY, Marks CE, Nelson G (2011) Biogeography of Nicotiana section Suaveolentes (Solanaceae) reveals geographical tracks in arid Australia. J Biogeogr 38:2066–2077

    Article  Google Scholar 

  • Mizuno N, Hosogi N, Park P, Takumi S (2010) Hypersensitive response-like reaction is associated with hybrid necrosis in interspecific crosses between tetraploid wheat and Aegilops tauschii Coss. PLoS One 5:e11326

    Article  PubMed  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4325

    Article  PubMed  CAS  Google Scholar 

  • Reed SM, Collins GB (1978) Interspecific hybrids in Nicotiana through in vitro culture of fertilized ovules. J Hered 69:311–315

    Google Scholar 

  • Song L, Guo W, Zhang T (2009) Interaction of novel Dobzhansky–Muller type genes for the induction of hybrid lethality between Gossypium hirsutum and G. barbadense cv. Coastland R4–4. Theor Appl Genet 119:33–41

    Article  PubMed  CAS  Google Scholar 

  • Tezuka T, Marubashi W (2004) Apoptotic cell death observed during the expression of hybrid lethality in interspecific hybrids between Nicotiana tabacum and N. suaveolens. Breed Sci 54:59–66

    Article  CAS  Google Scholar 

  • Tezuka T, Marubashi W (2006a) Hybrid lethality in interspecific hybrids between Nicotiana tabacum and N. suaveolens: evidence that the Q chromosome causes hybrid lethality based on Q-chromosome-specific DNA markers. Theor Appl Genet 112:1172–1178

    Article  PubMed  CAS  Google Scholar 

  • Tezuka T, Marubashi W (2006b) Genomic factors lead to programmed cell death during hybrid lethality in interspecific hybrids between Nicotiana tabacum and N. debneyi. SABRAO J Breed Genet 38:69–81

    Google Scholar 

  • Tezuka T, Kuboyama T, Matsuda T, Marubashi W (2007) Possible involvement of genes on the Q chromosome of Nicotiana tabacum in expression of hybrid lethality and programmed cell death during interspecific hybridization to N. debneyi. Planta 226:753–764

    Article  PubMed  CAS  Google Scholar 

  • Tezuka T, Kuboyama T, Matsuda T, Marubashi W (2010) Seven of eight species in Nicotiana section Suaveolentes have common factors leading to hybrid lethality in crosses with Nicotiana tabacum. Ann Bot 106:267–276

    Article  PubMed  CAS  Google Scholar 

  • Wheeler HM (1945) A contribution to the cytology of the Australian-South Pacific species of Nicotiana. Proc Natl Acad Sci USA 31:177–185

    Article  PubMed  CAS  Google Scholar 

  • Williams JGK, Kubelik AR, Livak KJ, Rafalski JA, Tingey SV (1990) DNA polymorphisms amplified by arbitrary primers are useful as genetic markers. Nucleic Acids Res 18:6531–6535

    Article  PubMed  CAS  Google Scholar 

  • Yamada T, Marubashi W, Niwa M (1999) Detection of four lethality types in interspecific crosses among Nicotiana species through the use of three rescue methods for lethality. Breed Sci 49:203–210

    Article  Google Scholar 

Download references

Acknowledgments

We thank Japan Tobacco, Inc., Iwata, Japan, for providing seeds of cultivated and wild species of the genus Nicotiana. This work was partly supported by a Grant-in-Aid for Young Scientists (Start-up; No. 20880024) from the Japan Society for the Promotion of Science, Japan.

Author information

Authors and Affiliations

  1. Graduate School of Life and Environmental Sciences, Osaka Prefecture University, Sakai, Osaka, 599-8531, Japan

    Takahiro Iizuka, Masayuki Oda & Takahiro Tezuka

  2. College of Agriculture, Ibaraki University, Ami, Ibaraki, 300-0393, Japan

    Tsutomu Kuboyama

  3. School of Agriculture, Meiji University, Kawasaki, Kanagawa, 214-8571, Japan

    Wataru Marubashi

Authors
  1. Takahiro Iizuka
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tsutomu Kuboyama
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Wataru Marubashi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Masayuki Oda
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Takahiro Tezuka
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Takahiro Tezuka.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Iizuka, T., Kuboyama, T., Marubashi, W. et al. Nicotiana debneyi has a single dominant gene causing hybrid lethality in crosses with N. tabacum . Euphytica 186, 321–328 (2012). https://doi.org/10.1007/s10681-011-0570-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10681-011-0570-3

Keywords

Search

Navigation