Skip to main content
Log in

Hybrid lethality of cultured cells of an interspecific F1 hybrid of Nicotiana gossei Domin and N. tabacum L.

  • Physiology and Biochemistry
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Cultured cells were established from the hypocotyl of F1 hybrid seedlings of Nicotiana gossei Domin and N. tabacum L. The cultured cells started to die at 26°C, but not at 37°C, which is similar to what occurred in cells of the original hybrid plants. An increase in the number of cells without cytoplasmic strands and acidification of the cytoplasm followed by decomposition of the mitochondria and chloroplasts indicated that vacuolar collapse plays a central role in the execution of cell death. Oxygen but not light was required for cell death. Cellular levels of the superoxide anion and hydrogen peroxide temporarily increased during the early phase at 26°C, while no such oxidative burst was observed at 37°C. The reactive oxygen intermediates are potentially involved in the death of the hybrid cells.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Amor Y, Chevion M, Levine A (2000) Anoxia pretreatment protects soybean cells against H2O2-induced cell death: possible involvement of peroxidase and of alternative oxidase. FEBS Lett 477:175–180

    Google Scholar 

  • Asada K (1992) Ascorbate peroxidase: a hydrogen peroxide-scavenging enzyme in plants. Physiol Plant 85:235–241

    Google Scholar 

  • Blokhina O, Virolainen E, Fagerstedt K (2003) Antioxidant, oxidative damage and oxygen deprivation stress: a review. Ann Bot 91:179–194

    Article  CAS  PubMed  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Burke JM, Arnold ML (2001) Genetics and the fitness of hybrids. Annu Rev Genet 35:31–52

    Google Scholar 

  • Dat JF, Lope-Delgado H, Foyer CH, Scott IM (1998) Parallel changes in H2O2 and catalase during thermotolerance induced by salicylic acid or heat acclimation in mustard seedlings. Plant Physiol 116:1351–1357

    Article  PubMed  Google Scholar 

  • Dat JF, Pellinen R, Beekmann T, Cotte BVD, Langebartels C, Kangäsjavi J, Inze D, Breusegem FV (2003) Changes in hydrogen peroxide homeostasis trigger an active cell death process in tobacco. Plant J 33:621–632

    Article  CAS  PubMed  Google Scholar 

  • Draper J, Scott R, Hamil J (1988) Transformation of dicotyledonous plant cell using the Ti plasmid of Agrobacterium tumefaciens and the Ri plasmid of A. rhizogenes. In: Draper J, Scott R, Armitage P, Walden R (eds) Plant genetic transformation and gene expression, a laboratory manual. Blackwell Scientific Publ, Oxford, pp 69–160

    Google Scholar 

  • Fukuda H (2000) Programmed cell death of tracheary elements as a paradigm in plants. Plant Mol Biol 44:245–253

    Article  Google Scholar 

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

    Google Scholar 

  • Hiraishi H, Terno A, Razandi M, Sugimoto Y, Harada T, Ivey KJ (1992) Role of cellular superoxide dismutase against reactive oxygen metabolite injury in cultured bovine aortic endothelial cell. J Biol Chem 267:14812–14817

    Google Scholar 

  • Inoue E, Marubshi W, Niwa M (1996) Genomic factors controlling the lethality exhibited in the hybrid between Nicotiana suaveolens Lehm and N. tabacum L. Theor Appl Genet 93:341–347

    Google Scholar 

  • Jabs T, Dietrich RA, Dangl JL (1996) Initiation of runaway cell death in an Arabidopsis mutant by extracellular superoxide. Science 273:1853–1856

    CAS  PubMed  Google Scholar 

  • Jacobson MD, Raff M (1995) Programmed cell death and Bcl-2 protection in very low oxygen. Nature 374:814–816

    Google Scholar 

  • Jiang M, Zhang J (2001) Effect of abscisic acid on active oxygen species, antioxidative defense system and oxidative damage in leaves of maize seedlings. Plant Cell Physiol 42:1265–1273

    Google Scholar 

  • Marubashi W, Onosato K (2002) Q chromosome controls the lethality of interspecific hybrid between Nicotiana tabacumand N. suaveolens. Breed Sci 52:137–142

    Google Scholar 

  • Mino M, Maekawa K, Ogawa K, Yamagishi H, Inoue M (2002) Cell death processes during expression of hybrid lethality in interspecific F1 hybrid between Nicotiana gossei Domin and N. tabacum L. Plant Physiol 130:1776–1787

    Google Scholar 

  • Mino M, Abe S, Suzuki T, Yokoyama H, Kaminaka H, Ogawa K, Morita S, Masumura T, Tanaka K, Inoue M (2004) Hydrogen peroxide functions as a cell death signal for hybrid lethality in the F1 of Nicotiana gossei × N. tabacum. Plant Sci 167:267–274

    Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trend Plant Sci 7:405–410

    Google Scholar 

  • Mittler R, Shulaev V, Seskar M, Lam E (1996) Inhibition of programmed cell death in tobacco plants during a pathogen-induced hypersensitive response at low oxygen pressure. Plant Cell 8:1991–2001

    Google Scholar 

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

    CAS  Google Scholar 

  • Nocter G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279

    Google Scholar 

  • Ogawa K, Iwabuchi M (2001) A mechanism for promoting germination of Zinnia elegans seeds by hydrogen peroxide. Plant Cell Physiol 42:286–291

    Google Scholar 

  • Orr HA. Madden LD, Coyne JA, Goodwin R, Hawley RS (1997) The developmental genetics of hybrid inviability: a mitotic defect in Drosophila hybrids. Genetics 145:1031–1040

    Google Scholar 

  • Orr HA, Presgraves DC (2000) Speciation by postzygotic isolation: forces, genes and molecules. BioEssays 22:1085–1094

    Article  CAS  PubMed  Google Scholar 

  • Pavelic D, Arpagaus S, Rawyler A, Brändle R (2000) Impact of post-anoxia stress on membrane lipids of anoxia-pretreated potato cell. A re-appraisal. Plant Physiol 124:1285–1292

    Google Scholar 

  • Phillips LL (1977) Interspecific incompatibility in Gossypium. IV. Temperature-conditional lethality in hybrid of G. klotzschianum. Am J Bot 64:914–915

    Google Scholar 

  • Phillips LL, Reid RK (1975) Interspecific incompatibility in Gossypium. II. Light and electron microscope studies of cell necrosis and tumorigenesis in hybrids of G. klotzschianum. Am J Bot 62:790–796

    Google Scholar 

  • Presgraves DC, Balagopalan L, Abmayr SM, Orr HA (2003) Adaptive evolution drives divergence of a hybrid inviability gene between two species of Drosophila. Nature 423:715–719

    Article  Google Scholar 

  • Rustérucci C, Aviv DH, Holt III BF, Dangl JL, Parker JE (2001) The disease resistance signaling components EDS1 and PAD4 are essential regulators of the cell death pathway controlled by LSD1 in Arabidopsis. Plant Cell 13:2211–2224

    Google Scholar 

  • Shimizu S, Eguchi Y, Kosaka H, Kamiike W, Matsuda H, Tsujimoto Y (1995) Prevention of hypoxia-induced cell death by Bcl-2 and Bcl-XL. Nature 374:811–813

    Google Scholar 

  • Tjus SE, Scheller HV, Andersson B, Møller BL (2001) Active oxygen produced during selective excitation of photosystem I is damaging not only to photosystem I, but also to photosystem II. Plant Physiol 125:2007–2015

    Google Scholar 

  • Vacca RA, de Pinto MC, Valenti D, Passarella S, Marra E, De Gara L (2004) Production of reactive oxygen species, alteration of cytosolic ascorbate peroxidase, and impairment of mitochondrial metabolism are early events in heat shock-induced programmed cell death in tobacco Bright-Yellow 2 cells. Plant Physiol 134:1100–1112

    Google Scholar 

  • Watanabe N, Che F-S, Iwano M, Takayama S, Nakano T, Yoshida S, Isogai A (1998) Molecular Characterization of photomixotrophic tobacco cells resistant to protoporphyrinogen oxidase-inhibiting herbicides. Plant Physiol 118:751–758

    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

    Google Scholar 

  • Yamada T, Marubashi W, Niwa M (2001) Facile induction of apoptosis into plant cells associated with temperature-sensitive lethality shown on interspecific hybrid from the cross Nicotiana suaveolens × N. tabacum. Plant Cell Physiol 42:204–213

    Google Scholar 

  • Yano A, Suzuki K, Uchimiya H, Shinshi H (1998) Induction of hypersensitive cell death by a fungal protein in cultures of tobacco cells. Mol Plant-Microbe Interact 11:115–123

    Google Scholar 

  • Zeven AC (1981) Eighth supplementary list of wheat varieties classified according to their genotypes for hybrid necrosis. Euphytica 30:521–539

    Google Scholar 

  • Zhou WM, Yoshida K, Shintaku Y, Takeda G (1991) The use of IAA to overcome interspecific hybrid inviability in reciprocal crosses between Nicotiana tabacum L and N. repanda Willd. Theor Appl Genet 82:657–661

    Google Scholar 

Download references

Acknowledgements

We thank Dr. Takehiro Masumura of Laboratory of Genetic Engineering, Graduate School of Agriculture, Kyoto Prefectural University for guidance in manipulating the confocal laser scanning microscope.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Masanobu Mino.

Additional information

Communicated by K.K. Kamo

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mino, M., Misaka, Y., Ueda, J. et al. Hybrid lethality of cultured cells of an interspecific F1 hybrid of Nicotiana gossei Domin and N. tabacum L.. Plant Cell Rep 24, 179–188 (2005). https://doi.org/10.1007/s00299-005-0923-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-005-0923-2

Keywords

Navigation