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Impact of mitochondrial alternative oxidase expression on the response of Nicotiana tabacum to cold temperature

Authors

  • Jia Wang,

    1. Department of Biological Sciences, University of Toronto Scarborough, 1265 Military Trail, Toronto, ON M1C 1A4, Canada
    2. Department of Cell and Systems Biology, University of Toronto Scarborough, 1265 Military Trail, Toronto, ON M1C 1A4, Canada
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  • Nirusan Rajakulendran,

    1. Department of Biological Sciences, University of Toronto Scarborough, 1265 Military Trail, Toronto, ON M1C 1A4, Canada
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  • Sasan Amirsadeghi,

    1. Department of Biological Sciences, University of Toronto Scarborough, 1265 Military Trail, Toronto, ON M1C 1A4, Canada
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  • Greg C. Vanlerberghe

    Corresponding author
    1. Department of Biological Sciences, University of Toronto Scarborough, 1265 Military Trail, Toronto, ON M1C 1A4, Canada
    2. Department of Cell and Systems Biology, University of Toronto Scarborough, 1265 Military Trail, Toronto, ON M1C 1A4, Canada
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e-mail: gregv@utsc.utoronto.ca

Abstract

The plant mitochondrial electron transport chain (ETC) includes a non-energy conserving alternative oxidase (AOX) thought to dampen reactive oxygen species (ROS) generation by the ETC and/or facilitate carbon metabolism by uncoupling it from ATP turnover. When wild-type (WT) Nicotiana tabacum grown at 28°C/22°C (light/dark) were transferred to 12°C/5°C, they showed a large induction of leaf Aox1a mRNA and AOX protein within 24 h. Transfer to cold also resulted in a large accumulation of monosaccharides, an increase in transcript level of genes encoding important ROS-scavenging enzymes and a moderate increase in lipid peroxidation. Transgenic plants with suppressed AOX level showed less cold-induced sugar accumulation than WT while transgenic plants with enhanced AOX levels showed enhanced sugar accumulation. This is inconsistent with the hypothesis that AOX acts to burn excess carbohydrate, but rather suggests a role for AOX to aid sugar accumulation, at least during cold stress. At 28°C/22°C, plants with suppressed AOX had elevated levels of lipid peroxidation compared with WT, while plants with enhanced AOX had reduced lipid peroxidation. This is consistent with the hypothesis that AOX dampens ROS generation and oxidative damage. However, this inverse relationship between AOX level and lipid peroxidation did not hold upon shift to cold. Under this stress condition, plants with strong suppression of AOX show enhanced induction of ROS-scavenging enzymes compared with WT and decline in lipid peroxidation. These data suggest that, under stress conditions, the lack of AOX enhances a mitochondrial stress-signaling pathway able to increase the ROS-scavenging capacity of the cell.

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