Ethylene regulates fast apoplastic acidification and expansin A transcription during submergence-induced petiole elongation in Rumex palustris

Authors

  • Robert A.M. Vreeburg,

    1. Plant Ecophysiology, Faculty of Biology, Utrecht University, Sorbonnelaan 16, 3584 CA Utrecht, The Netherlands,
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    • Present address: Edinburgh Cell Wall Group, Institute of Molecular Plant Science, University of Edinburgh, Daniel Rutherford Building, The Kings Buildings, Edinburgh EH9 3JH, UK.

  • Joris J. Benschop,

    1. Plant Ecophysiology, Faculty of Biology, Utrecht University, Sorbonnelaan 16, 3584 CA Utrecht, The Netherlands,
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    • Present address: Molecular Genetics, Faculty of Biology, Utrecht University, Padualaan 8, 3584 CH Utrecht, The Netherlands.

  • Anton J.M. Peeters,

    1. Plant Ecophysiology, Faculty of Biology, Utrecht University, Sorbonnelaan 16, 3584 CA Utrecht, The Netherlands,
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  • Timothy D. Colmer,

    1. School of Plant Biology, Faculty of Natural and Agricultural Sciences, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia,
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  • Ankie H.M. Ammerlaan,

    1. Plant Ecophysiology, Faculty of Biology, Utrecht University, Sorbonnelaan 16, 3584 CA Utrecht, The Netherlands,
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  • Marten Staal,

    1. Department of Plant Biology, University of Groningen, PO Box 14, 9750 AA Haren, The Netherlands, and
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  • Theo M. Elzenga,

    1. Department of Plant Biology, University of Groningen, PO Box 14, 9750 AA Haren, The Netherlands, and
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  • Raymond H.J. Staals,

    1. Plant Ecophysiology, Faculty of Biology, Utrecht University, Sorbonnelaan 16, 3584 CA Utrecht, The Netherlands,
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  • Catherine P. Darley,

    1. Biology Department, University of York, PO Box 373, York, YO10 4 YW, UK
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  • Simon J. McQueen-Mason,

    1. Biology Department, University of York, PO Box 373, York, YO10 4 YW, UK
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  • Laurentius A.C.J. Voesenek

    Corresponding author
    1. Plant Ecophysiology, Faculty of Biology, Utrecht University, Sorbonnelaan 16, 3584 CA Utrecht, The Netherlands,
      (fax +31 302 518366; e-mail l.a.c.j.voesenek@bio.uu.nl).
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(fax +31 302 518366; e-mail l.a.c.j.voesenek@bio.uu.nl).

Summary

The semi-aquatic dicot Rumex palustris responds to complete submergence by enhanced elongation of young petioles. This elongation of petiole cells brings leaf blades above the water surface, thus reinstating gas exchange with the atmosphere and increasing survival in flood-prone environments. We already know that an enhanced internal level of the gaseous hormone ethylene is the primary signal for underwater escape in R. palustris. Further downstream, concentration changes in abscisic acid (ABA), gibberellin (GA) and auxin are required to gain fast cell elongation under water. A prerequisite for cell elongation in general is cell wall loosening mediated by proteins such as expansins. Expansin genes might, therefore, be important target genes in submergence-induced and plant hormone-mediated petiole elongation. To test this hypothesis we have studied the identity, kinetics and regulation of expansin A mRNA abundance and protein activity, as well as examined pH changes in cell walls associated with this adaptive growth. We found a novel role of ethylene in triggering two processes affecting cell wall loosening during submergence-induced petiole elongation. First, ethylene was shown to promote fast net H+ extrusion, leading to apoplastic acidification. Secondly, ethylene upregulates one expansin A gene (RpEXPA1), as measured with real-time RT-PCR, out of a group of 13 R. palustris expansin A genes tested. Furthermore, a significant accumulation of expansin proteins belonging to the same size class as RpEXPA1, as well as a strong increase in expansin activity, were apparent within 4–6 h of submergence. Regulation of RpEXPA1 transcript levels depends on ethylene action and not on GA and ABA, demonstrating that ethylene evokes at least three, parallel operating pathways that, when integrated at the whole petiole level, lead to coordinated underwater elongation. The first pathway involves ethylene-modulated changes in ABA and GA, these acting on as yet unknown downstream components, whereas the second and third routes encompass ethylene-induced apoplastic acidification and ethylene-induced RpEXPA1 upregulation.

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