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Premature progression of anther early developmental programs accompanied by comprehensive alterations in transcription during high-temperature injury in barley plants

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Abstract

High-temperature stress causes abortive male reproductive development in many plant species. Here, we report a putative mechanism of high-temperature injury during anther early development in barley plants (Hordeum vulgare L). Under high-temperature conditions (30°C day/25°C night), cell-proliferation arrest, increased vacuolization, over-development of chloroplasts, and certain abnormalities of the mitochondria, nuclear membrane, and rough endoplasmic reticulum (RER) were observed in developing anther cells, but not in developing ovule cells. Moreover, premature degradation of tapetum cells and premature progression to meiotic prophase in pollen mother cells (PMCs) were also observed. To monitor transcriptional alterations during high-temperature injury, we performed DNA microarray analysis using the 22K Barley1 GeneChip. Expression profiles were captured at four time points during the early development of panicles, and during vegetative growth of seedlings as a control, with or without high-temperature treatment. Abiotic or biotic stress related genes were equally or more dominantly up-regulated in the seedlings exposed to high temperatures compared with the panicles. In contrast, certain genes associated with histones, DNA replication initiation, mitochondria, and ribosomes were specifically repressed in the exposed panicles. In situ hybridization studies indicated that repression locally occurred on the developing anther cells exposed to high temperatures. Microarray analysis also indicated that a series of genes, including a meiosis-specific gene Asy1 and anther-specific lipid transfer protein genes, was prematurely up-regulated at an earlier stage under high-temperature conditions. Real-time quantitative RT-PCR analyses well confirmed the expression differences of certain key genes predicted by the DNA microarrays. These results suggest that high-temperature causes premature progression of anther early development program and fate, such as progression to meiosis of PMCs, cell-proliferation arrest and degradation in anther wall cells, accompanied by comprehensive alterations in transcription.

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Acknowledgments

We are very grateful to Drs. Tadashi Sato, Hideyuki Takahashi, Jun Hidema, Nobuharu Fujii, and Yutaka Miyazawa for helpful suggestions and discussions, and Dr. Ryuji Sugiyama for technical supports of in situ hybridization. We also thank Tadashi Sakai of the Ultrastructure Research Laboratories Inc., 5-8-27 Edaminami, Tsuzuki-ku, Yokohama 224-0007, Japan for preparations of TEM samples. This work was supported by a Grant-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science, and Technology and by the Program for Promotion of Basic Research Activities for Innovative Biosciences (PROBRAIN) to M. K-K.

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Author notes

  1. Mafumi Abiko

    Present address: Graduate School of Science, University of Tokyo, Hongo, Tokyo, 113-0033, Japan

  2. Rumiko Saito

    Present address: Graduate School of Medicine, Tohoku University, Sendai, 980-8574, Japan

Authors and Affiliations

  1. Graduate School of Life Sciences, Tohoku University, Sendai, 980-8577, Japan

    Takeshi Oshino, Mafumi Abiko & Atsushi Higashitani

  2. New Industry Creation Hatchery Center, NICHe, Tohoku University, Sendai, 980-8579, Japan

    Rumiko Saito & Eiichiro Ichiishi

  3. Biomedical Engineering Research Organization, Tohoku University, Sendai, 980-8579, Japan

    Eiichiro Ichiishi

  4. National Institute of Crop Science, NARO, Tsukuba, 305-8518, Japan

    Makoto Endo & Makiko Kawagishi-Kobayashi

Authors
  1. Takeshi Oshino
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  2. Mafumi Abiko
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  6. Makiko Kawagishi-Kobayashi
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  7. Atsushi Higashitani
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Corresponding author

Correspondence to Atsushi Higashitani.

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Communicated by K. Shirasu.

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Oshino, T., Abiko, M., Saito, R. et al. Premature progression of anther early developmental programs accompanied by comprehensive alterations in transcription during high-temperature injury in barley plants. Mol Genet Genomics 278, 31–42 (2007). https://doi.org/10.1007/s00438-007-0229-x

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  • DOI: https://doi.org/10.1007/s00438-007-0229-x

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