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

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.

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Similar content being viewed by others Explore related subjectsDiscover the latest articles and news from researchers in related subjects, suggested using machine learning. Abbreviations
AOA:

amino-oxyacetic acid

AVG:

amino-ethoxyvinyl glycine

CTAB:

cetyltrimethylammonium bromide

DAG:

days after germination

PCD:

programmed cell death

RIMs:

reproductive isolation mechanisms

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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.

Author information Author notes
  1. Tetsuya Yamada

    Present address: National Institute of Floricultural Science, National Agricultural Research Organization, 305-8519, Ibaraki , Japan

Authors and Affiliations
  1. School of Agriculture, Ibaraki University, 300-0393, Ibaraki, Japan

    Wataru Marubashi

  2. Plant Biotechnology Institute, Ibaraki Agricultural Center, 319-0292, Ibaraki, Japan

    Tetsuya Yamada

Authors
  1. Tetsuya Yamada
  2. Wataru Marubashi
Corresponding author

Correspondence to Wataru Marubashi.

Additional information

T. Yamada is a Domestic Research Fellow at the National Institute of Floricultural Science

About this article Cite this article

Yamada, T., Marubashi, W. Overproduced ethylene causes programmed cell death leading to temperature-sensitive lethality in hybrid seedlings from the cross Nicotiana suaveolens × N. tabacum . Planta 217, 690–698 (2003). https://doi.org/10.1007/s00425-003-1035-2

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