Downregulation of high-isoelectric-point extracellular superoxide dismutase mediates alterations in the metabolism of reactive oxygen species and developmental disturbances in hybrid aspen

Authors

  • Vaibhav Srivastava,

    Corresponding author
    1. Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, 901 83 Umeå, Sweden,
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  • Helga Schinkel,

    Corresponding author
    1. Fraunhofer Institute for Molecular Biology and Applied Ecology (IME), Forckenbeckstr.6, 52074 Aachen, Germany,
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  • Johanna Witzell,

    1. Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, 901 83 Umeå, Sweden,
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  • Magnus Hertzberg,

    1. Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, 901 83 Umeå, Sweden,
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  • Mikaela Torp,

    1. Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, 901 83 Umeå, Sweden,
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  • Manoj Kumar Srivastava,

    Corresponding author
    1. Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, 901 83 Umeå, Sweden,
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  • Barbara Karpinska,

    1. Department of Botany, Stockholm University, Lilla Frescativ. 5, SE-10691 Stockholm, Sweden, and
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  • Michael Melzer,

    1. Department of Molecular Cell Biology, Institute of Plant Genetics and Crop Plant Research, 06466 Gatersleben, Germany
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  • Gunnar Wingsle

    Corresponding author
    1. Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, 901 83 Umeå, Sweden,
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(fax +46 90 786 5901; e-mail gunnar.wingsle@genfys.slu.se).

Joint first authors.

Present address: Department of Biochemistry, JC Bose Institute of Life Sciences, Bundelkhand University, Jhansi (UP) 284 128, India.

Summary

Transgenic hybrid aspen (Populus tremula L. × P. tremuloides Michx.) plants expressing a high-isoelectric-point superoxide dismutase (hipI-SOD) gene in antisense orientation were generated to investigate its function. Immunolocalization studies showed the enzyme to be localized extracellularly, in the secondary cell wall of xylem vessels and phloem fibers. The antisense lines of hipI-SOD exhibited a distinct phenotype; growth rate was reduced, stems were thinner and leaves smaller than in wild-type (WT) plants. The abundance of hipI-SOD was reduced in the bark and xylem of plants from these antisense lines. The vascular tissue of transgenic lines became lignified earlier than in WT plants and also showed an increased accumulation of reactive oxygen species (ROS). Xylem fibers and vessels were shorter and thinner in the transgenic lines than in WT plants. The total phenolic content was enhanced in the antisense lines. Furthermore, microarray analysis indicated that several enzymes involved in cell signaling, lignin biosynthesis and stress responses were upregulated in apical vascular tissues of transgenic plants. The upregulation of selected genes involved in lignin biosynthesis was also verified by real-time PCR. The results suggest that, in the transgenic plants, a premature transition into maturation occurs and the process is discussed in terms of the effects of increased accumulation of ROS due to reduced expression of hipI-SOD during development and differentiation.

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