Thermospermine levels are controlled by an auxin-dependent feedback loop mechanism in Populus xylem

Authors

  • Ana Milhinhos,

    1. Instituto de Biologia Experimental e Tecnológica, Oeiras, Portugal
    2. Instituto de Tecnologia Química e Biológica, Universidade Nova de Lisboa, Oeiras, Portugal
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  • Jakob Prestele,

    1. Umeå Plant Science Centre, Department of Plant Physiology, Umeå University, Umeå, Sweden
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  • Benjamin Bollhöner,

    1. Umeå Plant Science Centre, Department of Plant Physiology, Umeå University, Umeå, Sweden
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  • Andreia Matos,

    1. Instituto de Biologia Experimental e Tecnológica, Oeiras, Portugal
    2. Instituto de Tecnologia Química e Biológica, Universidade Nova de Lisboa, Oeiras, Portugal
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  • Francisco Vera-Sirera,

    1. Instituto de Biología Molecular y Celular de Plantas, Universidad Politécnica de Valencia-Consejo Superior de Investigaciones Científicas, Valencia, Spain
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  • José L. Rambla,

    1. Instituto de Biología Molecular y Celular de Plantas, Universidad Politécnica de Valencia-Consejo Superior de Investigaciones Científicas, Valencia, Spain
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  • Karin Ljung,

    1. Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, Umeå, Sweden
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  • Juan Carbonell,

    1. Instituto de Biología Molecular y Celular de Plantas, Universidad Politécnica de Valencia-Consejo Superior de Investigaciones Científicas, Valencia, Spain
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  • Miguel A. Blázquez,

    1. Instituto de Biología Molecular y Celular de Plantas, Universidad Politécnica de Valencia-Consejo Superior de Investigaciones Científicas, Valencia, Spain
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  • Hannele Tuominen,

    1. Umeå Plant Science Centre, Department of Plant Physiology, Umeå University, Umeå, Sweden
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  • Célia M. Miguel

    Corresponding author
    1. Instituto de Tecnologia Química e Biológica, Universidade Nova de Lisboa, Oeiras, Portugal
    • Instituto de Biologia Experimental e Tecnológica, Oeiras, Portugal
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For correspondence (e-mail cmiguel@itqb.unl.pt).

Summary

Polyamines are small polycationic amines that are widespread in living organisms. Thermospermine, synthesized by thermospermine synthase ACAULIS5 (ACL5), was recently shown to be an endogenous plant polyamine. Thermospermine is critical for proper vascular development and xylem cell specification, but it is not known how thermospermine homeostasis is controlled in the xylem. We present data in the Populus model system supporting the existence of a negative feedback control of thermospermine levels in stem xylem tissues, the main site of thermospermine biosynthesis. While over-expression of the ACL5 homologue in Populus, POPACAULIS5, resulted in strong up-regulation of ACL5 expression and thermospermine accumulation in leaves, the corresponding levels in the secondary xylem tissues of the stem were similar or lower than those in the wild-type. POPACAULIS5 over-expression had a negative effect on accumulation of indole-3-acetic acid, while exogenous auxin had a positive effect on POPACAULIS5 expression, thus promoting thermospermine accumulation. Further, over-expression of POPACAULIS5 negatively affected expression of the class III homeodomain leucine zipper (HD-Zip III) transcription factor gene PttHB8, a homologue of AtHB8, while up-regulation of PttHB8 positively affected POPACAULIS5 expression. These results indicate that excessive accumulation of thermospermine is prevented by a negative feedback control of POPACAULIS5 transcript levels through suppression of indole-3-acetic acid levels, and that PttHB8 is involved in the control of POPACAULIS5 expression. We propose that this negative feedback loop functions to maintain steady-state levels of thermospermine, which is required for proper xylem development, and that it is dependent on the presence of high concentrations of endogenous indole-3-acetic acid, such as those present in the secondary xylem tissues.

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