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First published online August 5, 2009; 10.1104/pp.109.140228

Plant Physiology 151:843-856 (2009)
© 2009 American Society of Plant Biologists

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SYSTEMS BIOLOGY, MOLECULAR BIOLOGY, AND GENE REGULATION

Involvement of HbPIP2;1 and HbTIP1;1 Aquaporins in Ethylene Stimulation of Latex Yield through Regulation of Water Exchanges between Inner Liber and Latex Cells in Hevea brasiliensis1,[C],[W]

Kessarin Tungngoen, Panida Kongsawadworakul, Unchera Viboonjun, Maki Katsuhara, Nicole Brunel, Soulaiman Sakr, Jarunya Narangajavana2 and Hervé Chrestin2,*

Department of Biotechnology, Faculty of Science, Mahidol University, Bangkok 10400, Thailand (K.T., J.N.); Department of Plant Science, Faculty of Science, Mahidol University, Bangkok 10400, Thailand (P.K., U.V., H.C.); Research Institute for Bioresources, Okayama University, Kurashiki 710–0046, Japan (M.K.); UMR 547 Physiologie Intégrée de l'Arbre Fruitier et Forestier, Université Blaise Pascal, 63177 Aubière cedex, France (N.B.); Agrocampus Ouest Centre d'Angers, UMR Sciences Agronomiques Appliquées à l'Horticulture, Institut Fédératif de Recherche Qualité et Santé du Végétal 149, 17 49045 Angers cedex, France (S.S.); and Institut de Recherche pour le Développement, UR 060 Climat et Fonctionnement des Agro-écosystèmes, Centre d'Ecologie Fonctionnelle et Evolutive-CNRS, F–34293 Montpellier cedex 5, France (H.C.)

Natural rubber is synthesized in specialized articulated cells (laticifers) located in the inner liber of Hevea brasiliensis. Upon bark tapping, the laticifer cytoplasm (latex) is expelled due to liber tissue turgor pressure. In mature virgin (untapped) trees, short-term kinetic studies confirmed that ethylene, the rubber yield stimulant used worldwide, increased latex yield, with a concomitant decrease in latex total solid content, probably through water influx in the laticifers. As the mature laticifers are devoid of plasmodesmata, the rapid water exchanges with surrounding liber cells probably occur via the aquaporin pathway. Two full-length aquaporin cDNAs (HbPIP2;1 and HbTIP1;1, for plasma membrane intrinsic protein and tonoplast intrinsic protein, respectively) were cloned and characterized. The higher efficiency of HbPIP2;1 than HbTIP1;1 in increasing plasmalemma water conductance was verified in Xenopus laevis oocytes. HbPIP2;1 was insensitive to HgCl2. In situ hybridization demonstrated that HbPIP2;1 was expressed in all liber tissues in the young stem, including the laticifers. HbPIP2;1 was up-regulated in both liber tissues and laticifers, whereas HbTIP1;1 was down-regulated in liber tissues but up-regulated in laticifers in response to bark Ethrel treatment. Ethylene-induced HbPIP2;1 up-regulation was confirmed by western-blot analysis. The promoter sequences of both genes were cloned and found to harbor, among many others, ethylene-responsive and other chemical-responsive (auxin, copper, and sulfur) elements known to increase latex yield. Increase in latex yield in response to ethylene was emphasized to be linked with water circulation between the laticifers and their surrounding tissues as well as with the probable maintenance of liber tissue turgor, which together favor prolongation of latex flow.

1 This work was supported by the Franco-Thai Cooperation Program in Higher Education and Research 2005–2008, and a grant under an agreement between the Institut de Recherche pour le Développement and a consortium from the private sector (the Institut Français du Caoutchouc, the Société de Technologie Michelin, the Société Internationale des Plantations d'Hévéa, and the Société Financière des Caoutchoucs Consultant Services). K.T. was supported by the Royal Golden Jubilee Ph.D. program (grant no. PHD/0217/2547) of the Thailand Research Fund.

2 These authors contributed equally to the article.

The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Hervé Chrestin (chrestin{at}ird.fr).

[C] Some figures in this article are displayed in color online but in black and white in the print edition.

[W] The online version of this article contains Web-only data.

www.plantphysiol.org/cgi/doi/10.1104/pp.109.140228

* Corresponding author; e-mail chrestin{at}ird.fr.

Received April 26, 2009; accepted July 24, 2009; published August 5, 2009.


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