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Isolation and functional characterization of three aquaporins from olive (Olea europaea L.)

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Abstract

To study the molecular bases of water transport in olive we characterized cDNAs from Olea europaea cv “Leccino” related to the aquaporin (AQP) gene family. A phylogenetic analysis of the corresponding polypeptides confirmed that they were part of water channel proteins localized in the plasma membrane and in the tonoplast. The full-length sequences were obtained by RACE-PCR and were named OePIP1.1, OePIP2.1 and OeTIP1.1. The OePIP2.1 and OeTIP1.1 encode functional water channel proteins, as indicated by expression assays in Xenopus laevis oocytes. OePIP1.1 and OePIP2.1 expression levels are high in roots and twigs and low in leaves. The highest hybridization signal of OeTIP1.1 was detected in twigs, while in roots and leaves the expression was low. To investigate the effect of abiotic stress on the transcript level of olive AQP genes, olive trees were subjected to drought treatment and the expression levels of the genes were measured by Northern-blot analysis. The transcript levels of each gene diminished strongly in plants submitted to drought stress, when soil moisture, twig water potential and twig hydraulic conductivity progressively decreased. The downregulation of AQP genes may result in reduced membrane water permeability and may limit loss of cellular water during periods of water stress. A possible role for AQPs on shoot embolism repair is discussed.

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Abbreviations

AQP:

Aquaporin

MIP:

Major intrinsic protein

PIP:

Plasma membrane intrinsic protein

TIP:

Tonoplast intrinsic protein

P f :

Osmotic permeability coefficient

PCR:

Polymerase chain reaction

K ss :

Specific twig hydraulic conductivity

References

  • Alexandersson E, Fraysse L, Sjovall-Larsen S, Gustavsson S, Fellert M, Karlsson M, Johanson U, Kjellbom P (2005) Whole gene family expression and drought stress regulation of aquaporins. Plant Mol Biol 59:469–484

    Article  PubMed  CAS  Google Scholar 

  • Baiges I, Schaffner AR, Affenzeller MJ, Mas A (2002) Plant aquaporins. Plant Physiol 115:175–182

    Article  CAS  Google Scholar 

  • Barone LM, Shih C, Wasserman P (1997) Mercury-induced conformational changes and identification of conserved surface loops in plasma membrane aquaporins from higher plants. J Biol Chem 272:30672–30677

    Article  PubMed  CAS  Google Scholar 

  • Biela A, Grote K, Otto B, Hoth S, Hedrich R, Kaldenhoff R (1999) The Nicotiana tabacum plasma membrane aquaporin NtAQP1 is mercury-insensitive and permeable for glycerol. Plant J 18:565–570

    Article  PubMed  CAS  Google Scholar 

  • Brito G, Costa A, Fonseca HMAC, Santos CV (2003) Response of Olea europaea ssp. maderensis in vitro shoots exposed to osmotic stress. Sci Hortic 97:411–417

    Article  CAS  Google Scholar 

  • Chang S, Puryear J, Cairney J (1993) A simple and efficient method for isolating RNA from pine tree. Plant Mol Biol Rep 11:113–116

    CAS  Google Scholar 

  • Chaumont F, Barrieu F, Jung R, Chrispeels MJ (2000) Plasma membrane intrinsic proteins from maize cluster in two sequence subgroups with differential aquaporin activity. Plant Physiol 122:1025–1034

    Article  PubMed  CAS  Google Scholar 

  • Chaumont F, Barrieu F, Wojcik E, Chrispeels MJ, Jung R (2001) Aquaporins constitute a large and highly divergent protein family in maize. Plant Physiol 125:1206–1215

    Article  PubMed  CAS  Google Scholar 

  • Chaumont F, Moshelion M, Daniels MJ (2005) Regulation of plant aquaporin activity. Biol Cell 97:749–764

    Article  PubMed  CAS  Google Scholar 

  • Chrispeels MJ, Maurel C (1994) Aquaporins: the molecular basis of facilitated water movement through living plant cells? Plant Physiol 105:9–13

    Article  PubMed  CAS  Google Scholar 

  • Daniels MJ, Chaumont F, Mirkov TE, Chrispeels J (1996) Characterization of a new vacuolar membrane aquaporin sensitive to mercury at a unique site. Plant Cell 8:587–599

    Article  PubMed  CAS  Google Scholar 

  • Frohman MA, Dush MK, Martin GR (1988) Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Biochemistry 85:8998–9002

    CAS  Google Scholar 

  • Holbrook NM, Zwieniecki MA (1999) Embolism repair and xylem tension: do we need a miracle? Plant Physiol 120:7–10

    Article  PubMed  CAS  Google Scholar 

  • Hukin D, Doering-Saad C, Thomas CR, Pritchard J (2002) Sensitivity of cell hydraulic conductivity to mercury is coincident with symplasmic isolation and expression of plasmalemma aquaporin genes in growing maize roots. Planta 215:1047–1056

    Article  PubMed  CAS  Google Scholar 

  • Jang JK, Kim DG, Kim YO, Kim JS, Kang H (2004) An expression analysis of a gene family encoding plasma membrane aquaporins in response to abiotic stresses in Arabidopsis thaliana. Plant Mol Biol 54:713–725

    Article  PubMed  CAS  Google Scholar 

  • Johanson U, Gustavsson S (2002) A new subfamily of major intrinsic proteins in plants. Mol Biol Evol 19:456–461

    PubMed  CAS  Google Scholar 

  • Johanson U, Karlsson M, Johansson I, Gustavsson S, Sjovall S, Fraysse L, Weig AR, Kjellbom P (2001) The complete set of genes encoding major intrinsic proteins in Arabidopsis provides a framework for a new nomenclature for major intrinsic proteins in plants. Plant Physiol 126:1358–1369

    Article  PubMed  CAS  Google Scholar 

  • Johansson I, Larsson C, Ek B, Kjellbom P (1996) The major integral proteins of spinach leaf plasma membranes are putative aquaporins and are phosphorylated in response to Ca2+ and apoplastic water potential. Plant Cell 8:1181–1191

    Article  PubMed  CAS  Google Scholar 

  • Johansson I, Karlsson M, Shukla VK, Chrispeels MJ, Larsson C, Kjellbom P (1998) Water transport activity of the plasma membrane aquaporin PM28A is regulated by phosphorylation. Plant Cell 10:451–459

    Article  PubMed  CAS  Google Scholar 

  • Johansson I, Karlsson M, Johanson U, Larsson C, Kjellbom P (2000) The role of aquaporins in cellular and whole plant water balance. Biochim Biophys Acta 1465:324–342

    Article  PubMed  CAS  Google Scholar 

  • Jones HG (2004) Irrigation scheduling: advantages and pitfalls of plant-based methods. J Exp Bot 55:2427–2436

    Article  PubMed  CAS  Google Scholar 

  • Kolb KJ, Sperry JS, Lamont BB (1996) A method for measuring xylem hydraulic conductance and embolism in entire root and shoot systems. J Exp Bot 47:1805–1810

    CAS  Google Scholar 

  • Li L, Li S, Tao Y, Kitagawa Y (2000) Molecular cloning of a novel water channel from rice: its products expression in Xenopus oocytes and involvement in chilling tolerance. Plant Sci 154:43–51

    Article  PubMed  CAS  Google Scholar 

  • Liman ER, Tytgat J, Hess P (1992) Subunit stoichiometry of a mammalian K+ channel determined by construction of multimeric cDNAs. Neuron 9:861–871

    Article  PubMed  CAS  Google Scholar 

  • Lo Gullo MA, Salleo S, Rosso R, Trifilò P (2003) Drought resistance of 2-year-old saplings of Mediterranean forest trees in the field: relations between water relations, hydraulics and productivity. Plant Soil 250:259–272

    Article  CAS  Google Scholar 

  • Lovisolo C, Hartung W, Schubert A (2002) Whole-plant hydraulic conductance and root-to-shoot flow of abscisic acid are independently affected by water stress in grapevines. Funct Plant Biol 29:1349–1356

    Article  CAS  Google Scholar 

  • Ludevid D, Hofte H, Himelblau E, Chrispeels MJ (1992) The expression pattern of the tonoplast intrinsic protein γTIP in Arabidopsis thaliana is correlated with cell enlargement. Plant Physiol 100:1633–1639

    Article  PubMed  CAS  Google Scholar 

  • Luu DT, Maurel C (2005) Aquaporins in a challenging environment: molecular gears for adjusting plant water status. Plant Cell Environ 28:85–96

    Article  CAS  Google Scholar 

  • Moshelion M, Becker D, Biela A, Uehlein N, Hedrich R, Otto B, Levi H, Moran N, Kaldenhoff R (2002) Plasma membrane aquaporins in the motor cells of Samanea saman: diurnal and circadian regulation. Plant Cell 14:727–739

    Article  PubMed  CAS  Google Scholar 

  • North GB, Martre P, Nobel PS (2004) Aquaporins account for variations in hydraulic conductance for metabolically active root regions of Agave deserti in wet, dry, and rewetted soil. Plant Cell Environ 27:219–228

    Article  CAS  Google Scholar 

  • Preston GM, Carroll TP, Guggino WB, Agree P (1992) Appearance of water channels in Xenopus oocytes expressing red cell CHIP28 protein. Science 256:385–387

    Article  PubMed  CAS  Google Scholar 

  • Sakr S, Alves G, Morillon R, Maurel K, Decourteix M, Guilliot A, Fleurat-Lessard P, Julien JL, Chrispeels MJ (2003) Plasma membrane aquaporins are involved in winter embolism recovery in walnut tree. Plant Physiol 133:630–641

    Article  PubMed  CAS  Google Scholar 

  • Sakurai J, Ishikawa F, Yamaguchi T, Uemura M, Maeshima M (2005) Identification of 33 rice aquaporin genes and analysis of their expression and function. Plant Cell Physiol l46:1568–1577

    Article  CAS  Google Scholar 

  • Salleo S, Lo Gullo MA, Trifio’ P, Nardini A (2004) New evidence for a role of vessel-associated cells and phloem in the rapid xylem refilling of cavitated stems of Laurus nobilis L. Plant Cell Environ 27:1065–1076

    Article  Google Scholar 

  • Schaffner AR (1998) Aquaporin function, structure, and expression: are there more surprises to surface in water relations? Planta 204:131–139

    Article  PubMed  CAS  Google Scholar 

  • Siefritz F, Tyree MT, Lovisolo C, Schubert A, Kaldenhoff R (2002) PIP1 plasma membrane aquaporins in tobacco: from cellular effects to function in plants. Plant Cell 14:869–876

    Article  PubMed  CAS  Google Scholar 

  • Smart LB, Moskal WA, Cameron KD, Bennett AB (2001) MIP genes are down-regulated under drought stress in Nicotiana glauca. Plant Cell Physiol 42:686–693

    Article  PubMed  CAS  Google Scholar 

  • Sui H, Han BG, Lee JK, Wallan P, Jap B (2001) Structural basis of water-specific transport through the AQP1 water channel. Nature 414:872–878

    Article  PubMed  CAS  Google Scholar 

  • Tognetti R, D’Andria R, Morelli G, Calandrelli D, Fragnito F (2004) Irrigation effects on daily and seasonal variations of trunk sap flow and leaf water relations in olive trees. Plant Soil 263:249–264

    Article  CAS  Google Scholar 

  • Törnroth-Horsefield S, Wang Y, Hedfalk K, Johanson U, Karlsson M, Tajkhorshid E, Neutze R, Kjellbom P (2005) Structural mechanism of plant aquaporin gating. Nature 439:688–694

    Article  PubMed  CAS  Google Scholar 

  • Tournaire-Roux C, Sutka M, Javot H, Gout E, Gerbeau P, Luu DT, Bligny R, Maurel C (2003) Cytosolic pH regulates root water transport during anoxic stress through gating of aquaporins. Nature 425:393–397

    Article  PubMed  CAS  Google Scholar 

  • Tyerman SD, Niemietz CM, Bramley H (2002) Plant aquaporins: multifunctional water and solute channels with expanding roles. Plant Cell Environ 25:173–194

    Article  PubMed  CAS  Google Scholar 

  • Vandeleur R, Niemietz C, Tilbrook J, Tyerman SD (2005) Roles of aquaporins in root responses to irrigation. Plant Soil 274:141–161

    Article  CAS  Google Scholar 

  • Vera-Estrella R, Barkla BJ, Bohnert HJ, Pantoja O (2004) Novel regulation of aquaporins during osmotic stress. Plant Physiol 135:2318–2329

    Article  PubMed  CAS  Google Scholar 

  • Yamada S, Katsuhara M, Kelly WB, Michalowski CB, Bohnert HJ (1995) A family of transcripts encoding water channel proteins: tissue-specific expression in the common ice plant. Plant Cell 7:1129–1142

    Article  PubMed  CAS  Google Scholar 

  • Yamada S, Komori T, Myers PN, Kuwata S, Kubo T, Imaseki H (1997) Expression of plasma membrane water channel genes under water stress in Nicotiana excelsior. Plant Cell Physiol 38:1226–1231

    PubMed  CAS  Google Scholar 

  • Zardoya R (2005) Phylogeny and evolution of the major intrinsic protein family. Biol Cell 97:397–414

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This study was financed by the Italian Ministry of Education and Research—PRIN MIUR “The control of vegetative growth in olive (O. europaea L.) by the rootstock: ecophysiological, histo-anatomical and molecular aspects.” FS was funded by the Vigoni-DAAD program: “CO2 in plants: from the atmosphere towards chloroplasts. A coupled intercellular and transmembrane pathway, involving aquaporins” for oocyte-swelling assays in Darmstadt. Our particular thanks are due to A. Carra for his advices on molecular biology and to S. Bragagnolo for his help with physiological measurements.

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Authors and Affiliations

  1. Department of Arboriculture and Pomology, University of Turin, Via Leonardo da Vinci 44, Grugliasco, 10095, Turin, Italy

    Francesca Secchi, Claudio Lovisolo & Andrea Schubert

  2. Applied Plant Sciences, Institute of Botany, Darmstadt University of Technology, Schnittspahnstr 10, 64287, Darmstadt, Germany

    Norbert Uehlein & Ralf Kaldenhoff

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  1. Francesca Secchi
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  2. Claudio Lovisolo
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  3. Norbert Uehlein
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  4. Ralf Kaldenhoff
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  5. Andrea Schubert
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Correspondence to Francesca Secchi.

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Secchi, F., Lovisolo, C., Uehlein, N. et al. Isolation and functional characterization of three aquaporins from olive (Olea europaea L.). Planta 225, 381–392 (2007). https://doi.org/10.1007/s00425-006-0365-2

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  • DOI: https://doi.org/10.1007/s00425-006-0365-2

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