Advertisement

Planta

, Volume 217, Issue 5, pp 690–698 | Cite as

Overproduced ethylene causes programmed cell death leading to temperature-sensitive lethality in hybrid seedlings from the cross Nicotiana suaveolens × N. tabacum

  • Tetsuya Yamada
  • Wataru MarubashiEmail author
Original Article

Abstract

Reproductive isolation mechanisms (RIMs) often become obstacles in crossbreeding. Hybrid lethality is a subtype of RIM but its physiological mechanism remains poorly elucidated. Interspecific hybrids of Nicotiana suaveolens Lehm. × N. tabacum L. cv. Hicks-2 expressed temperature-sensitive lethality. This lethality was induced by programmed cell death (PCD) that was accompanied by the characteristic changes of animal apoptosis in hybrid seedlings at 28 °C but not at 36 °C. When hybrid seedlings were cultured at 28 °C, DNA fragmentation started in the cotyledon, and nuclear fragmentation subsequently progressed with lethal symptoms spreading throughout the seedlings. At 28 °C, ethylene production in hybrid seedlings was detectable at a high level compared with the level in parental seedlings. In contrast, the ethylene production rate in hybrid seedlings cultured at 36 °C was equal to that in parental seedlings. Treatment with ethylene biosynthetic inhibitors, amino-oxyacetic acid and amino-ethoxyvinyl glycine, suppressed lethal symptoms and apoptotic changes, and also prolonged survival of hybrid seedlings. Thus, the increase in the ethylene production rate correlated closely with expression of lethal symptoms and apoptotic changes in hybrid seedlings. From these observations, we conclude that overproduced ethylene acts as an essential factor mediating PCD and subsequent lethality in hybrid seedlings. Furthermore, the present study has provided the first evidence that ethylene is involved in the phenomenon of hybrid lethality.

Keywords

Apoptosis Ethylene Hybrid lethality Nicotiana (programmed cell death) Programmed cell death Temperature sensitivity 

Abbreviations

AOA

amino-oxyacetic acid

AVG

amino-ethoxyvinyl glycine

CTAB

cetyltrimethylammonium bromide

DAG

days after germination

PCD

programmed cell death

RIMs

reproductive isolation mechanisms

Notes

Acknowledgement

This work was partly supported by Grant-in Aid for Exploratory Research No. 12876002 and Scientific Research (A) No. 13306003 from the Ministry of Education, Science, Sports and Culture, Japan.

References

  1. Abeles FB, Morgan PW, Saltveit Jr ME (2000) Ethylene in plant biology, 2nd edn. Academic Press, San DiegoGoogle Scholar
  2. Afford S, Randhawa S (2000) Apoptosis. Mol Pathol 53:55–63CrossRefPubMedGoogle Scholar
  3. Asai T, Stone JM, Heard JE, Kovtun Y, Yorgey P, Sheen J, Ausubel FM (2000) Fumonisin B1-induced cell death in arabidopsis protoplasts requires jasmonate-, ethylene-, and salicylate-dependent signaling pathways. Plant Cell 12:1823–1836Google Scholar
  4. Atta-Aly M (1992) Effect of high temperature on ethylene biosynthesis by tomato fruit. Postharvest Biol Technol 2:19–24Google Scholar
  5. De Jong AJ, Hoeberichts FA, Yakimova ET, Maximova E, Woltering EJ (2000) Chemical-induced apoptotic cell death in tomato cells: involvement of caspase-like proteases. Planta 211:656–662CrossRefPubMedGoogle Scholar
  6. De Jong AJ, Yakimova ET, Kapchina VM, Woltering EJ (2002) A critical role for ethylene in hydrogen peroxide release during programmed cell death in tomato suspension cells. Planta 214:537–545PubMedGoogle Scholar
  7. Hanania U, Furman-Matarasso N, Ron M, Avni A (1999) Isolation of a novel SUMO protein from tomato that suppresses EIX-induced cell death. Plant J 19:533–541CrossRefPubMedGoogle Scholar
  8. He C-J, Morgan PW, Drew MC (1996) Transduction of an ethylene signal is required for cell death and lysis in the root cortex of maize during aerenchyma formation induced by hypoxia. Plant Physiol 112:463–472PubMedGoogle Scholar
  9. Iwai S, Kishi C, Nakata K, Kawashima N (1986) Production of Nicotiana tabacum × Nicotiana acuminata hybrid by ovule culture. Plant Cell Rep 5:403–404Google Scholar
  10. Jones AM (2001) Programmed cell death in development and defence. Plant Physiol 125:94–97CrossRefPubMedGoogle Scholar
  11. Lloyd R (1975) Tissue culture as a means of circumventing lethality in an interspecific Nicotiana hybrid. Tob Sci XIX:4–6Google Scholar
  12. Lund ST, Stall RE, Klee HJ (1998) Ethylene regulates the susceptible response to pathogen infection in tomato. Plant Cell 10:371–382PubMedGoogle Scholar
  13. Lurie S, Handros A, Fallik E, Shapira R (1996) Reversible inhibition of tomato fruit gene expression at high temperature. Plant Physiol 110:1207–1214PubMedGoogle Scholar
  14. Marubashi W, Kobayashi M (2002) Temperature-dependent apoptosis detected in hybrid between Nicotiana debneyi and N. tabacum expressing lethality. Plant Biotechnol 19: 267–270Google Scholar
  15. Marubashi W, Yamada T, Niwa M (1999) Apoptosis detected in hybrids between Nicotiana glutinosa and N. repanda expressing lethality. Planta 210:168–171CrossRefPubMedGoogle Scholar
  16. Mayr E (1963) Animal species and evolution. Belknap Cambridge, MAGoogle Scholar
  17. Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497Google Scholar
  18. Oka H-I, Doida Y (1962) Phylogenetic differentiation of cultivated rice, XX. Analysis of the genetic basis of hybrid breakdown in rice. Jpn J Genet 37:24–35Google Scholar
  19. Orzáez D, Granell A (1997) The plant homologue of the defender against apoptotic death gene is down-regulated during senescence of flower petals. FEBS Lett 404:275–278PubMedGoogle Scholar
  20. Overmyer K, Tuominen H, Kettunen R, Betz C, Langebartels C, Sandermann Jr H, Kangasjärvi J (2000) Ozone-sensitive Arabidopsis rcd1 mutant reveals opposite roles for ethylene and jasmonate signaling pathways in regulating superoxide-dependent cell death. Plant Cell 12:1849–1862PubMedGoogle Scholar
  21. Phillips LL (1977) Interspecific incompatibility in Gossypium. IV. Temperature-conditional lethality in hybrids of G. klotzschianum. Am J Bot 64:914–915Google Scholar
  22. Provine WB (1991) Alfred Henry Sturtevant and crosses between Drosophila melanogaster and Drosophila simulans. Genetics 129:1–5PubMedGoogle Scholar
  23. Samora PJ, Stelly DM, Kohel RJ (1994) Localization and mapping of the Le 1 and Gl 2 loci of cotton (Gossypium hirsutum L.). J Hered 85:152-157Google Scholar
  24. Sharma HC, Ohm HW (1990) Crossability and embryo rescue enhancement in wide crosses between wheat and three Agropyron species. Euphytica 49:209–214Google Scholar
  25. Stebbins GL (1966) Reproductive isolation and the origin of species. In: Processes of organic evolution. Prentice-Hall, New Jersey, pp 85–112Google Scholar
  26. Woltering EJ, De Jong AJ, Yakimova ET (1999) Apoptotic cell death in plants: the role of ethylene. In: AK Kanellis (ed) Biology and biotechnology of the plant hormone ethylene II. Kluwer, Dordrecht, pp 209–216Google Scholar
  27. 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 49:203–210Google Scholar
  28. Yamada T, Marubashi W, Niwa M (2000) Apoptotic cell death induces temperature-sensitive lethality in hybrid seedlings and calli derived from the cross of Nicotiana suaveolens × N. tabacum. Planta 211:614–622CrossRefPubMedGoogle Scholar
  29. Yamada T, Marubashi W, Nakamura T, Niwa M (2001a) Possible involvement of auxin-induced ethylene in an apoptotic cell death during temperature-sensitive lethality expressed by hybrid between Nicotiana glutinosa and N. repanda. Plant Cell Physiol 42:923–930CrossRefPubMedGoogle Scholar
  30. Yamada T, Takatsu Y, Kasumi M, Manabe T, Hayashi M, Marubashi W, Niwa M (2001b) Novel evaluation method of flower senescence in freesia (Freesia hybrida) based on apoptosis as an indicator. Plant Biotech 18:215–218Google Scholar
  31. Yang SF, Hoffman NE (1984) Ethylene biosynthesis and its regulation in higher plants. Annu Rev Plant Physiol 35:155–189Google Scholar
  32. Young TE, Gallie DR (2000) Regulation of programmed cell death in maize endosperm by abscisic acid. Plant Mol Biol 42:397–414PubMedGoogle Scholar
  33. Zeven AC (1981) Eighth supplementary list of wheat varieties classified according to their genotype for hybrid necrosis. Euphytica 30:521–539Google Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  1. 1.School of AgricultureIbaraki UniversityIbarakiJapan
  2. 2.Plant Biotechnology InstituteIbaraki Agricultural CenterIbarakiJapan
  3. 3.National Institute of Floricultural ScienceNational Agricultural Research OrganizationIbaraki Japan

Personalised recommendations