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Implication of reactive oxygen species and mitochondrial dysfunction in the early stages of plant programmed cell death induced by ultraviolet-C overexposure

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Abstract

Recent studies have suggested that ultraviolet-C (UV-C) overexposure induces programmed cell death (PCD) in Arabidopsis thaliana (L.) Heynh, and this process includes participation of caspase-like proteases, DNA laddering as well as fragmentation of the nucleus. To investigate possible early signal events, we used microscopic observations to monitor in vivo the behaviour of mitochondria, as well as the production and localization of reactive oxygen species (ROS) during protoplast PCD induced by UV-C. A quick burst of ROS was detected when the protoplasts were kept in continuous light after UV-C exposure, which was restricted in chloroplasts and the adjacent mitochondria. Pre-incubation with ascorbic acid (AsA, antioxidant molecule) or 3-(3, 4-dichlorophenyl)-1, 1-dimethylurea (DCMU, an inhibitor of photosynthetic electron transport) decreased the ROS production and partially protected protoplasts from PCD. A mitochondrial transmembrane potential (MTP) loss occurred prior to cell death; thereafter, the mitochondria irregularly clumped around chloroplasts or aggregated in other places within the cytoplasm, and the movement of mitochondria was concomitantly blocked. Pre-treatment with an inhibitor of mitochondrial permeability transition pores (MPTP), cyclosporine (CsA), effectively retarded the decrease of MTP and reduced the percentage of protoplasts undergoing PCD after UV-C overexposure. Our results suggest that the MTP loss and the changes in distribution and mobility of mitochondria, as well as the production of ROS play important roles during UV-induced plant PCD, which is in good accordance with what has been reported in many types of apoptotic cell death, both in animals and plants.

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Abbreviations

AsA:

Ascorbic acid

CsA:

Cyclosporine A

DCMU:

3-(3, 4-dichlorophenyl)-1, 1-dimethylurea

FDA:

Fluorescein diacetate

H2DCFDA:

2′, 7′-Dichlorodihydrofluorescein diacetate

HR:

Hypersensitive response

MPTP:

Mitochondrial permeability transitions pore

MTP:

Mitochondrial transmembrane potential

PCD:

Programmed cell death

Rh123:

Rhodamine 123

ROS:

Reactive oxygen species

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Acknowledgments

We are grateful to Dr. David C. Logan (St Andrews, UK) for kindly providing transgenic Arabidopsis seeds harboring GFP-labeled mitochondria. We thank Yonghong Tang for her help in using laser scanning confocal microscope in our research group, anonymous reviewers for their constructive comments, Prof. Wei R. Chen for critical reading of the manuscript, and members of our group for helpful discussions. This research is supported by the National Natural Science Foundation of China (30670507; 30600128; 30470494) and the Natural Science Foundation of Guangdong Province (015012).

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  1. MOE Key Laboratory of Laser Life Science and Institute of Laser Life Science, South China Normal University, Guangzhou, 510631, People’s Republic of China

    Caiji Gao, Da Xing, Lingling Li & Lingrui Zhang

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  1. Caiji Gao
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  2. Da Xing
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  3. Lingling Li
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Correspondence to Da Xing.

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Gao, C., Xing, D., Li, L. et al. Implication of reactive oxygen species and mitochondrial dysfunction in the early stages of plant programmed cell death induced by ultraviolet-C overexposure. Planta 227, 755–767 (2008). https://doi.org/10.1007/s00425-007-0654-4

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