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Production of reactive oxygen species and induction of signaling pathways for the ACO gene expressions in tomato plants triggered by the volatile organic compound ether

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Abstract

Diethyl ether (ether), a volatile organic compound, is widely used as an industrial solvent and easily released to the environment. Acute exposure of tomato plants to high concentrations of ether caused young leaves to curl. Histochemical analyses revealed that superoxide anion (•O2 −) and hydrogen peroxide were formed sequentially by ether, and that •O2 − was the major ROS produced in response to ether exposure. We observed cell death by microscopic inspection of Evans blue-stained samples, following fumigation with ether for 6 h. The ethylene biosynthetic gene, 1-aminocyclopropane-1-carboxylic acid oxidase (ACO), was induced as early as 15–30 min after ether fumigation and could be activated at ether concentration as low as 1 μL/L. Induction of ACO gene expression occurred simultaneously with ROS accumulation and coincided with the occurrence of cell death. Simultaneous treatment of tomato plants with mechanical wounding and ether induced differential expression of the ACO gene family. Ether strongly induced ACO4 and moderately induced ACO1, whereas mechanical wounding strongly induced ACO1 and slightly induced ACO4. Induction of the ACO gene family by ether occurred via different signaling pathways. While the ACO1 gene was induced via protein phosphorylation, the ACO4 gene was induced through protein dephosphorylation. Induction of ACO1 and ACO4 might be through MPK1, MPK2, MPK3, and PP2Ac1. These results suggest that the cellular responses of tomato plants to ether are different from the plant responses to ozone, and that tomato plants respond to different air pollutants through different perceptions and downstream signaling pathways.

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Abbreviations

GAPDH:

Glyceraldehyde-3-phosphate dehydrogenase

ACO:

1-Aminocyclopropane-1-carboxylic acid oxidase

AOS:

Allene oxide synthase

APX1:

Cytosolic ascorbate peroxidase 1

ER5:

Ethylene-responsive gene 5

ICS:

Isochorismate synthase

LOXD:

Lipoxygenase D

MEK:

Mitogen-activating protein kinase kinase

MKP1:

MAP kinase phosphatase 1

MPK:

Mitogen-activating protein kinase

RBOH1:

NADPH oxidase

PAL:

Phenylalanine ammonia lyase

PP1:

Phosphoprotein phosphatase 1

PP2Ac1:

Protein phosphatase 2Ac1

PP2C:

Metal ion-dependent protein phosphatase 2C

PP5:

Protein phosphatase 5

Ptpkis1:

Phosphotyrosine phosphatase 1

SOD:

Superoxide dismutase

PR:

Pathogenesis-related protein

ROS:

Reactive oxygen species

VOC:

Volatile organic compound

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Acknowledgments

We thank Yi-Jyun Jheng and Yu-Jhen Hsu for expert technical assistance and Drs. David Shiuan and Kuo-Wei Lin for careful reading of the manuscript.

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Authors and Affiliations

  1. Department of Life Science and Institute of Biotechnology, National Dong Hwa University, Hualien, 974, Taiwan

    Kuo-Chih Lin, Pi-Chi Sun & Pei-Lan Lin

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  1. Kuo-Chih Lin
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  2. Pi-Chi Sun
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Correspondence to Kuo-Chih Lin.

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Communicated by A. Altman.

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Lin, KC., Sun, PC. & Lin, PL. Production of reactive oxygen species and induction of signaling pathways for the ACO gene expressions in tomato plants triggered by the volatile organic compound ether. Plant Cell Rep 30, 599–611 (2011). https://doi.org/10.1007/s00299-010-0976-8

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