Skip to main content
SpringerLink
Log in

Members of the aquaporin family in the developing pea seed coat include representatives of the PIP, TIP, and NIP subfamilies

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Water and nutrients required by developing seeds are mainly supplied by the phloem and have to be released from a maternal parenchyma tissue before being utilized by the filial tissues of embryo and endosperm. To identify aquaporins that could be involved in this process four full-length cDNAs were cloned and sequenced from a cDNA library of developing seed coats of pea (Pisum sativum L.). The cDNA of PsPIP1-1 appeared to be identical to that of clone 7a/TRG-31, a turgor-responsive gene cloned previously from pea roots. PsPIP1-1, PsPIP2-1, and PsTIP1-1, or their possible close homologues, were also expressed in cotyledons of developing and germinating seeds, and in roots and shoots of seedlings, but transcripts of PsNIP-1 were only detected in the seed coat. In mature dry seeds, high hybridization signals were observed with the probe for PsPIP1-1, but transcripts of PsPIP2-1, PsTIP1-1, and PsNIP-1 were not detected. Functional characterization after heterologous expression in Xenopus oocytes showed that PsPIP2-1 and PsTIP1-1 are aquaporins whereas PsNIP-1 is an aquaglyceroporin. PsNIP-1, like several other NIPs, contains a tryptophan residue corresponding with Trp-48 in GlpF (the glycerol facilitator of Escherichia coli) that borders the selectivity filter in the permeation channel. It is suggested that PsPIP1-1 and/or its possible close homologues could play a role in water absorption during seed imbibition, and that PsPIP2-1, possibly together with PsPIP1-1, could be involved in the release of phloem water from the seed coat symplast, which is intimately connected with the release of nutrients for the embryo. Abbreviations: MIPs, major intrinsic proteins; NIPs, nodulin 26-like intrinsic proteins; PIPs, plasma membrane intrinsic proteins; SIPs, small, basic intrinsic proteins; TIPs, tonoplast intrinsic proteins

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Agre, P., Bonhivers, M. and Borgnia, M.J. 1998. The aquaporins, blueprints for cellular plumbing systems. J. Biol. Chem. 273: 14659–14662.

    PubMed  Google Scholar 

  • Aharon, R., Shahak, Y., Wininger, S., Bendov, R., Kapulnik, Y. and Galili, G. 2003. Overexpression of a plasma membrane aquaporin in transgenic tobacco improves plant vigor under favorable growth conditions but not under drought or salt stress. Plant Cell 15: 439–447.

    PubMed  Google Scholar 

  • Altschul, S.F., Madden, T.L., Schäffer, A.A., Zhang, J., Zhang, Z., Miller, W. and Lipman DJ. 1997. Gapped BLAST and PSIBLAST: a new generation of protein database search programs. Nucl. Acids Res. 25: 3389–3402.

    PubMed  Google Scholar 

  • Barrieu, F., Chaumont, F. and Chrispeels, M.J. 1998. High expression of the tonoplast aquaporin ZmTIP1 in epidermal and conducting tissues of maize. Plant Physiol. 117: 1153–1163.

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Borgnia, M.J. and Agre, P. 2001. Reconstitution and functional comparison of purified GlpF and AqpZ, the glycerol and water channels from Escherichia coli. Proc. Natl. Acad. Sci. USA 98: 2888–2893.

    PubMed  Google Scholar 

  • Borstlap, A.C. 2002. Early diversification of plant aquaporins. Trends Plant Sci. 7: 529–530.

    PubMed  Google Scholar 

  • Bradford, K.J. 1994. Water stress and the water relations of seed development: a critical review. Crop Sci. 34: 1–11.

    Google Scholar 

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

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Chen, G., Wilson, I.D., Kim, S.H. and Grierson, D. 2001. Inhibiting expression of a tomato ripening-associated membrane protein increases organic acids and reduces sugar levels of fruit. Planta 212: 799–807.

    PubMed  Google Scholar 

  • Ciavatta, V.T., Morillon, R., Pullman, G.S., Chrispeels, M.J. and Cairney, J. 2001. An aquaglyceroporin is abundantly expressed early in the development of the suspensor and the embryo proper of loblolly pine. Plant Physiol. 127: 1556–1567.

    PubMed  Google Scholar 

  • Corpet, F. 1988. Multiple sequence alignment with hierarchical clustering. Nucl. Acids Res. 16: 10881–10890.

    PubMed  Google Scholar 

  • Daniels, M.J., Mirkov, T.E. and Chrispeels, M.J. 1994. The plasma membrane of Arabidopsis thaliana contains a mercuryinsensitive aquaporin that is a homolog of the tonoplast water channel protein TIP. Plant Physiol. 106: 1325–1333.

    PubMed  Google Scholar 

  • Dean, R.M., Rivers, R.L., Zeidel, M.L. and Roberts, D.M. 1999. Purification and functional reconstitution of soybean nodulin 26. An aquaporin with water and glycerol transport properties. Biochemistry 38: 347–353.

    PubMed  Google Scholar 

  • de Jong, A., Koerselman-Kooij, J.W. Schuurmans, J.A.M.J. and Borstlap, A.C. 1997. The mechanism of amino acid efflux from seed coats of developing pea seeds as revealed by uptake experiments. Plant Physiol. 114: 731–736.

    PubMed  Google Scholar 

  • de Jong, A. and Wolswinkel, P. 1995. Differences in release of endogenous sugars and amino acids from attached and detached seed coats of developing pea seeds. Physiol. Plant. 94: 78–86.

    Google Scholar 

  • Doering-Saad, C., Newbury, H.J., Bale, J.S. and Pritchard, J. 2002. Use of aphid stylectomy and RT-PCR for the detection of transporter mRNAs in sieve elements. J. Exp. Bot. 53: 631–637.

    PubMed  Google Scholar 

  • Dordas, C., Chrispeels, M.J. and Brown, P.H. 2000. Permeability and channel-mediated transport of boric acid across membrane vesicles isolated from squash roots. Plant Physiol. 124: 1349–1361.

    PubMed  Google Scholar 

  • Dumont, J.N. 1972. Oogenesis in Xenopus laevis. J. Morphol. 136: 153–180.

    PubMed  Google Scholar 

  • Feinberg, A.P. and Vogelstein, G. 1983. A technique for radiolabelling DNA restriction fragments to high specific activity. Anal. Biochem. 132: 6–13.

    PubMed  Google Scholar 

  • Fisher, D.B. 2000. Long-distance transport. In: B.B. Buchanan, W. Gruissem and R.L. Jones (Eds.) Biochemistry & Molecular Biology of Plants, American Society of Plant Physiologists, Rockville, MD, pp. 730–784.

    Google Scholar 

  • Frangne, N., Maeshima, M., Schäffner, A.R., Mandel, T., Martinoia, E. and Bonnemain, J.-L. 2001. Expression and distribution of a vacuolar aquaporin in young and mature leaf tissues of Brassica napus in relation to water fluxes. Planta 212: 270–278.

    PubMed  Google Scholar 

  • Froger, A., Tallur, B., Thomas, D. and Delamarche, C. 1998. Prediction of functional residues in water channels and related proteins. Prot. Sci. 7: 1458–1468.

    Google Scholar 

  • Fu, D., Libson, A., Miercke, L.J.W., Weitzman, C., Nollert, P., Krucinski, J. and Stroud, R.M. 2000. Structure of a glycerolconducting channel and the basis for its selectivity. Science 290: 481–486.

    PubMed  Google Scholar 

  • Gao, Y.-P., Young, L., Bonham-Smith, P. and Gusta, L.V. 1999. Characterization and expression of plasma and tonoplast membrane aquaporins in primed seed of Brassica napus during germination under stress conditions. Plant Mol. Biol. 40: 635–644.

    PubMed  Google Scholar 

  • Gerbeau, P., Güçlü, J., Ripoche, P. and Maurel, C. 1999. Aquaporin Nt-TIPa can account for the high permeability of tobacco cell vacuolar membrane to small neutral solutes. Plant J. 18: 577–587.

    PubMed  Google Scholar 

  • Guenther, J.F. and Roberts, D.M. 2000. Water-selective and multifunctional aquaporins from Lotus japonicus nodules. Planta 210: 741–748.

    PubMed  Google Scholar 

  • Guerrero, F.D. and Crossland, L. 1993. Tissue-specific expression of a plant turgor-responsive gene with amino acid sequence homology to transport-facilitating proteins. Plant Mol. Biol. 21: 929–935.

    PubMed  Google Scholar 

  • Guerrero, F.D., Jones, J.T. and Mullet, J.E. 1990. Turgor-responsive gene transcription and RNA levels increase rapidly when pea shoots are wilted. Sequence and expression of three inducible genes. Plant Mol. Biol. 15: 11–26.

    PubMed  Google Scholar 

  • Hakman, I. and Oliviusson, P. 2002. High expression of putative aquaporin genes in cells with transporting and nutritive functions during seed development in Norway spruce (Picea abies). J. Exp. Bot. 53: 639–649.

    PubMed  Google Scholar 

  • Heller, K.B., Lin, E.C.C. and Wilson, T.H. 1980. Substrate specificity and transport properties of the glycerol facilitator of Escherichia coli. J. Bacteriol. 144: 274–278.

    PubMed  Google Scholar 

  • Heymann, J.B. and Engel, A. 1999. Aquaporins: phylogeny, structure, and physiology of water channels. News Physiol. Sci. 14: 187–193.

    PubMed  Google Scholar 

  • Ikeda, M., Beitz, E., Kozono, D., Guggino, W.B., Agre, P. and Yasui, M. 2002. Characterization of aquaporin-6 as a nitrate channel in mammalian cells. Requirement of pore-lining residue threonine 63. J. Biol. Chem. 277: 39873–39879.

    PubMed  Google Scholar 

  • Jauh, G.-Y., Phillips, T.E. and Rogers, J.C. 1999. Tonoplast intrinsic protein isoforms as markers of vacuolar functions. Plant Cell 11: 1867–1882.

    PubMed  Google Scholar 

  • Johanson, U., Karlsson, M., Johansson, I., Gustavsson, S., Sjövall, S., Fraysse, L., Weig, A.R. and Kjellbom, P. 2001. The complete set of genes encoding major intrinsic proteins in Arabidopsis provides a frame work for a new nomenclature for major intrinsic proteins in plants. Plant Physiol. 126: 1358–1369.

    PubMed  Google Scholar 

  • Jones, J.T. and Mullet, J.E. 1995. Developmental expression of a turgor-responsive gene that encodes an intrinsic membrane protein. Plant Mol. Biol. 28: 983–996.

    PubMed  Google Scholar 

  • Krieg, P.A. and Melton, D.A. 1984. Functional messenger RNAs are produced by SP6 in vitro transcription of cloned cDNAs. Nucl. Acids Res. 12: 7057–7070.

    PubMed  Google Scholar 

  • Lagrée, V., Froger, A., Deschamps, S., Hubert, J.-F., Delamarche, C., Bonnec, G., Thomas, D., Gouranton, J. and Pellerin, I. 1999. Switch from an aquaporin to a glycerol channel by two amino acid substitutions. J. Biol. Chem. 274: 6817–6819.

    PubMed  Google Scholar 

  • Leggewie, G., Willmitzer, L. and Riesmeier, J.W. 1995. Molecular approaches towards the isolation and characterisation of plant phosphate transporters. 10th International Workshop on Plant Membrane Biology, 6–11 August 1995, Regensburg, p. R32.

  • Lewis, O.A.M. and Pate, J.S. 1973. The significance of transpirationally derived nitrogen in protein synthesis in fruiting plants of pea (Pisum sativum L.). J. Exp. Bot. 24: 596–606.

    Google Scholar 

  • Liu, Q., Umeda, M. and Uchimiya, H. 1994. Isolation and expression analysis of two rice genes encoding the major intrinsic protein. Plant Mol. Biol. 26: 2003–2007.

    PubMed  Google Scholar 

  • Logemann, J., Schell, J. and Willmitzer, L. 1987. Improved method for the isolation of RNA from plant tissue. Anal. Biochem. 163: 16–20.

    PubMed  Google Scholar 

  • Ludevid, D., Höfte, H., Himelblau, E. and Chrispeels, M.J. 1992. The expression pattern of the tonoplast intrinsic protein β-TIP in Arabidopsis thaliana is correlated with cell enlargement. Plant Physiol. 100: 1633–1639.

    Google Scholar 

  • Martre, P., Morillon, R., Barrieu, F., North, G.B., Nobel, P.S. and Chrispeels, M.J. 2002. Plasma membrane aquaporins play a significant role during recovery from water deficit. Plant Physiol. 130: 2101–2110.

    PubMed  Google Scholar 

  • Maurel, C., Chrispeels, M., Lurin, C., Tacnet, F., Geelen, D., Ripoche, P. and Guern, J. 1997. Function and regulation of seed aquaporins. J. Exp. Bot. 48: 421–430.

    Google Scholar 

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

    PubMed  Google Scholar 

  • Münch, E. 1930. Die Stoffbewegungen in der Pflanze. Gustav Fischer, Jena.

    Google Scholar 

  • Opperman, C., Taylor, C.G. and Conkling, M.A. 1994. Rootknot nematode-directed expression of a plant root-specific gene. Science 263: 221–223.

    Google Scholar 

  • Ouyang, L.J., Whelan, J., Weaver, C.D., Roberts, D.M. and Day, D.A. 1991. Protein phosphorylation stimulates the rate of malate uptake across the peribacteroid membrane of soybean nodules. FEBS Lett. 293: 188–190.

    PubMed  Google Scholar 

  • Patrick, J.W. and Offler, C.E. 2001. Compartmentation of transport and transfer events in developing seeds. J. Exp. Bot. 52: 551–564.

    PubMed  Google Scholar 

  • Patrick, J.W., Zhang, W., Tyerman, S.D., Offler, C.E. and Walker, N.A. 2001. Role of membrane transport in phloem translocation of assimilates and water. Aust. J. Plant Physiol. 28: 695–707.

    Google Scholar 

  • Sambrook, J., Fritsch, E.F. and Maniatis, T. 1989. Molecular Cloning: A Laboratory Manual, 2nd ed. Cold Spring Harbor Laboratory Press, Plainview, NY.

    Google Scholar 

  • Shackel, K.A. and Turner, N.C. 2000. Seed coat cell turgor in chickpea is independent of changes in plant and pod water potential. J. Exp. Bot. 51: 895–900.

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Silberberg, S.D. and Magleby, K.L. 1997. Voltage-induced slow activation and deactivation of mechanosensitive channels in Xenopus oocytes. J. Physiol. (London) 505: 551–569.

    PubMed  Google Scholar 

  • Suga, S., Imagawa, S. and Maeshima, M. 2001. Specificity of the accumulation of mRNAs and protein of the plasma membrane and tonoplast aquaporins in radish organs. Planta 212: 294–304.

    PubMed  Google Scholar 

  • Sui, H., Han, B.-G., Lee, J.K., Walian, P. and Jap, B.K. 2001. Structural basis of water-specific transport through the AQP1 water channel. Nature 414: 872–878.

    PubMed  Google Scholar 

  • Tsukaguchi, H., Shayakul, C., Berger, U.V., Mackenzie, B., Devidas, S., Guggino, W.B., van Hoek, A.N. and Hediger, M.A. 1998. Molecular characterization of a broad selectivity neutral solute channel. J. Biol. Chem. 273: 24737–24743.

    PubMed  Google Scholar 

  • Udvardi, M.K. and Day, D.A. 1997. Metabolite transport across symbiotic membranes of legume nodules. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48: 493–523.

    PubMed  Google Scholar 

  • van Dongen, J.T., Ammerlaan, A.M.H., Wouterlood, M., van Aelst, A.C. and Borstlap, A.C. 2003. Structure of the developing pea seed coat and the post-phloem transport pathway of nutrients. Ann. Bot. 91: 729–737.

    PubMed  Google Scholar 

  • van Dongen, J.T. and Borstlap, A.C. 2003. Aquaporins: structure, function and phylogenetic analysis. In: A.R. Hemsley and I. Poole (Eds.) The Evolution of Plant Physiology, Academic Press, London, pp. 109–120.

    Google Scholar 

  • van Dongen, J.T., Laan, R.G.W., Wouterlood, M. and Borstlap, A.C. 2001. Electrodiffusional uptake of organic cations by pea seed coats. Further evidence for poorly selective pores in the plasma membrane of seed coat parenchyma cells. Plant Physiol. 126: 1688–1697.

    PubMed  Google Scholar 

  • Wallace, I.S., Wills, D.M., Guenther, J.F. and Roberts, D.M. 2002. Functional selectivity for glycerol of the nodulin 26 subfamily of plant membrane intrinsic proteins. FEBS Lett. 523: 109–112.

    PubMed  Google Scholar 

  • Weig, A.R. and Jakob, C. 2000. Functional identification of the glycerol permease activity of Arabidopsis thaliana NLM1 and NLM2 proteins by heterologous expression in Saccharomyces cerevisiae. FEBS Lett. 481: 293–298.

    PubMed  Google Scholar 

  • Wienkoop, S. and Saalbach, G. 2003. Proteome analysis. Novel proteins identified at the peribacteroid membrane from Lotus japonicus root nodules. Plant Physiol. 131: 1080–1090.

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Transport Physiology, Utrecht University, Sorbonnelaan 16, 3584 CA, Utrecht, Netherlands

    Jolanda A.M.J. Schuurmans, Joost T. van Dongen, Bas P.W. Rutjens, Alex Boonman & Adrianus C. Borstlap

  2. Molecular Plant Physiology, Utrecht University, Padualaan 8, 3584 CH, Utrecht, Netherlands

    Jolanda A.M.J. Schuurmans & Bas P.W. Rutjens

  3. Max Planck Institute of Molecular Plant Physiology, Am Mü:hlenberg 1, 14476, Golm, Germany

    Joost T. van Dongen

  4. Plant Ecophysiology Group, Utrecht University, Sorbonnelaan 16, 3584 CA, Utrecht, Netherlands

    Alex Boonman

  5. Section of Phytopathology, Utrecht University, Sorbonnelaan 16, 3584 CA, Utrecht, Netherlands

    Corné M.J. Pieterse

Authors
  1. Jolanda A.M.J. Schuurmans
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Joost T. van Dongen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bas P.W. Rutjens
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Alex Boonman
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Corné M.J. Pieterse
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Adrianus C. Borstlap
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Adrianus C. Borstlap.

Additional information

these authors contributed equally to the work

these authors contributed equally to the work

Rights and permissions

Reprints and permissions

About this article

Cite this article

Schuurmans, J.A., van Dongen, J.T., Rutjens, B.P. et al. Members of the aquaporin family in the developing pea seed coat include representatives of the PIP, TIP, and NIP subfamilies. Plant Mol Biol 53, 655–667 (2003). https://doi.org/10.1023/B:PLAN.0000019070.60954.77

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/B:PLAN.0000019070.60954.77

Search

Navigation