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Stress signaling in response to polycyclic aromatic hydrocarbon exposure in Arabidopsis thaliana involves a nucleoside diphosphate kinase, NDPK-3

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Abstract

Main conclusion

The study is the first to reveal the proteomic response in plants to a single PAH stress, and indicates that NDPK3 is a positive regulator in the Arabidopsis response to phenanthrene stress.

Abstract

Polycyclic aromatic hydrocarbons (PAHs) are highly carcinogenic pollutants that are byproducts of carbon-based fuel combustion, and tend to persist in the environment for long periods of time. PAHs elicit complex, damaging responses in plants, and prior research at the physiological, biochemical, and transcriptional levels has indicated that reactive oxygen species (ROS) and oxidative stress play major roles in the PAH response. However, the proteomic response has remained largely unexplored. This study hypothesized that the proteomic response in Arabidopsis thaliana to phenanthrene, a model PAH, would include a strong oxidative stress signature, and would provide leads to potential signaling molecules involved. To explore that proteomic signature, we performed 2D-PAGE experiments and identified 30 proteins levels that were significantly altered including catalases (CAT), ascorbate peroxidase (APX), peroxiredoxins (POD), glutathione-S-transferase, and glutathione reductase. Also upregulated was nucleoside diphosphate kinase 3 (NDPK-3), a protein known to have metabolic and stress signaling functions. To address whether NDPK-3 functions upstream of the oxidative stress response, we measured levels of stress-responsive enzymes in NDPK-3 overexpressor, loss-of-function knockout, and wild-type plant lines. In the NDPK-3 overexpressor, the enzyme activities of APX, CAT, POD, as well as superoxide dismutase were all increased compared to wild type; in the NDPK-3 knockout line, these enzymes had reduced activity. This pattern occurred in untreated as well as phenanthrene-treated plants. These data support a model in which NDPK-3 is a positive regulator of the Arabidopsis stress response to PAHs.

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Abbreviations

APX:

Ascorbate peroxidase

CAT:

Catalases

MDA:

Malondialdehyde

NDPK-3:

Nucleoside diphosphate kinase 3

PAH:

Polycyclic aromatic hydrocarbons

PCD:

Programmed cell death

POD:

Peroxiredoxins

ROS:

Reactive oxygen species

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Acknowledgments

We thank Dr. Chentao Lin at University Of California, Riverside for generous donation of the vector pFGC5941 used in this study, and Dr. Yuejun Yang at Hunan University for assistance in proteomics and MALDI-TOF/TOF. We also thank Dr. Airong Wang and Guodong Lu at Agriculture and Forestry University, Fuzhou, and Jessica Redfern, Kristophe Diaz, Tsering Gesar, James Stark at University of Massachusetts Boston for helpful discussions and review. This work was supported by National Nature Science Foundation of China (Grant No. 30970532), Key Program for the Construction of the Economic Zone on the Western Side of the Taiwan Straits, Fujian Province (Grant No. 0b08b005) and Nature Science Foundation of Fujian (Grant No. 2014J01089) to HL.

Conflict of interest

The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. College of Resources and Environment, Fujian Agriculture and Forestry University, Fuzhou, 350002, China

    Hong Liu, Long Tan & Yan-he Huang

  2. Department of Biology, University of Massachusetts, 100 Morrissey Blvd, Boston, MA, 02125-3393, USA

    David Weisman & Adán Colón-Carmona

  3. The School of Life Sciences, Fujian Agriculture and Forestry University, Fuzhou, 350002, China

    Ling Tang, Wen-ke Zhang, Zong-hua Wang & Wen-xiong Lin

  4. Department of Life Science, College of Biology, Hunan University, Changsha, 410082, China

    Xuan-ming Liu

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  1. Hong Liu
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  2. David Weisman
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  3. Ling Tang
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  4. Long Tan
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  5. Wen-ke Zhang
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  7. Yan-he Huang
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  8. Wen-xiong Lin
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  9. Xuan-ming Liu
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  10. Adán Colón-Carmona
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Correspondence to Hong Liu or Adán Colón-Carmona.

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H. Liu and D. Weisman contributed equally to this work.

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Liu, H., Weisman, D., Tang, L. et al. Stress signaling in response to polycyclic aromatic hydrocarbon exposure in Arabidopsis thaliana involves a nucleoside diphosphate kinase, NDPK-3. Planta 241, 95–107 (2015). https://doi.org/10.1007/s00425-014-2161-8

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