Skip to main content
SpringerLink
Log in

Intracellular pH sensing is altered by plasma membrane PIP aquaporin co-expression

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

The plant plasma membrane barrier can express aquaporins (PIP1 and PIP2) that show two intriguing aspects: (1) the potential of modulating whole membrane water permeability by co-expression of both types, which have recently been distinguished for showing a different capacity to reach the plasma membrane; and (2) the faculty to reduce water permeation through the pore after cytosolic acidification, as a consequence of a gating process. Our working hypothesis is that these two key features might enhance plasticity of the membrane water transport capacity if they jointly trigger any cooperative interaction. In previous work, we proved by biophysical approaches that the plasma membrane of the halophyte Beta vulgaris storage root presents highly permeable aquaporins that can be shut down by acidic pH. Root Beta vulgaris PIPs were therefore subcloned and expressed in Xenopus oocytes. Co-expression of BvPIP1;1 and BvPIP2;2 not only enhances oocyte plasma membrane water permeability synergistically but also reinforces pH inhibitory response from partial to complete shut down after cytosolic pH acidification. This pH dependent behavior shows that PIP1–PIP2 co-expression accounts for a different pH sensitivity in comparison with PIP2 expression. These results prove for the first time that PIP co-expression modulates the membrane water permeability through a pH regulatory response, enhancing in this way membrane versatility to adjust its water transfer capacity.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Abbreviations

AQP:

Aquaporin

P f :

Osmotic water permeability

PIP:

Plasma membrane intrinsic protein (aquaporin)

PM:

Plasma membrane

ARCA:

Anti-reverse cap analog

References

  • Agre P, Mathai JC, Smith BL, Preston GM (1999) Functional analyses of aquaporin water channel proteins. Methods Enzymol 294:550–572

    Article  PubMed  CAS  Google Scholar 

  • Alleva K, Niemietz CM, Sutka M, Maurel C, Parisi M, Tyerman SD, Amodeo G (2006) Plasma membrane of Beta vulgaris storage root shows high water channel activity regulated by cytoplasmic pH and a dual range of calcium concentrations. J Exp Bot 57:609–621

    Article  PubMed  CAS  Google Scholar 

  • Alleva K, Chara O, Sutka MR, Amodeo G (2009) Analysis of the source of heterogeneity in the osmotic response of plant membrane vesicles. Eu Biophys J 38(2):175–184

    Article  Google Scholar 

  • Amodeo G, Dorr R, Vallejo A, Sutka M, Parisi M (1999) Radial and axial water transport in sugar beet storage root. J Exp Bot 50:509–516

    Article  CAS  Google Scholar 

  • Amodeo G, Sutka M, Dorr R, Parisi M (2002) Protoplasmic pH modifies water and solute transfer in Beta vulgaris root vacuoles. J Membr Biol 187:175–184

    Article  PubMed  CAS  Google Scholar 

  • Azad AK, Katsuhara M, Sawa Y, Ishikawa T, Shibata H (2008) Characterization of four plasma membrane aquaporins in tulip petals: a putative homolog is regulated by phosphorylation. Plant Cell Physiol 49:1196–1208

    Article  PubMed  CAS  Google Scholar 

  • Barone LM, Shih C, Wasserman BP (1997) Mercury-induced conformational changes and identification of conserved surface loops in plasma membrane aquaporins from higher plants. Topology of PMIP31 from Beta vulgaris L. J Biol Chem 272:30672–30677

    Article  PubMed  CAS  Google Scholar 

  • Barone LM, Mu HH, Shih CJ, Kashlan KB, Wasserman BP (1998) Distinct biochemical and topological properties of the 31- and 27- kilodalton plasma membrane intrinsic protein subgroups from red beet. Plant Physiol 118:315–322

    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 

  • Boursiac Y, Boudet J, Postaire O, Luu DT, Tournaire-Roux C, Maurel C (2008) Stimulus-induced downregulation of root water transport involves reactive oxygen species-activated cell signalling and plasma membrane intrinsic protein internalization. Plant J 56:207–218

    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 

  • Daniels MJ, Mirkov TE, Chrispeels MJ (1994) The plasma membrane of Arabidopsis thaliana contains a mercury-insensitive aquaporin that is a homolog of the tonoplast water channel protein TIP. Plant Physiol 106:1325–1333

    Article  PubMed  CAS  Google Scholar 

  • Dordas C, Chrispeels MJ, Brown PH (2000) Permeability and channel-mediated transport of boric acid across membrane vesicles isolated from squash roots. Plant Physiol 124:1349–1362

    Article  PubMed  CAS  Google Scholar 

  • Fetter K, Van Wilder V, Moshelion M, Chaumont F (2004) Interactions between plasma membrane aquaporins modulate their water channel activity. Plant Cell 16:215–228

    Article  PubMed  CAS  Google Scholar 

  • Finkelstein A (1987) Water movement through lipid bilayers, pores, and plasma membranes: theory and reality. In: Distinguished lecture series of the society of general physiologists, Vol. 4. Wiley, New York, pp 1–228

  • Fischer M, Kaldenhoff R (2008) On the pH regulation of plant aquaporins. J Biol Chem 283:33889–33892

    Article  PubMed  CAS  Google Scholar 

  • Gerbeau P, Amodeo G, Henzler T, Santoni V, Ripoche P, Maurel C (2002) The water permeability of Arabidopsis plasma membrane is regulated by divalent cations and pH. Plant J 30:71–81

    Article  PubMed  CAS  Google Scholar 

  • Gouet P, Courcelle E, Stuart DI, Metoz F (1999) ESPript: multiple sequence alignments in PostScript. Bioinformatics 15:305–308

    Article  PubMed  CAS  Google Scholar 

  • Graber ML, DiLillo DC, Friedman BL, Pastoriza-Munoz E (1986) Characteristics of fluoroprobes for measuring intracellular pH. Anal Biochem 156(1):202–212

    Article  PubMed  CAS  Google Scholar 

  • Hachez C, Zelazny E, Chaumont F (2006) Modulating the expression of aquaporin genes in planta: a key to understand their physiological functions? Biochim Biophys Acta 1758:1142–1156

    Article  PubMed  CAS  Google Scholar 

  • Hachez C, Heinen RB, Draye X, Chaumont F (2008) The expression pattern of plasma membrane aquaporins in maize leaf highlights their role in hydraulic regulation. Plant Mol Biol 68:337–353

    Article  PubMed  CAS  Google Scholar 

  • Hu CG, Hao HJ, Honda C, Kita M, Moriguchi T (2003) Putative PIP1 genes isolated from apple: expression analyses during fruit development and under osmotic stress. J Exp Bot 54:2193–2194

    Article  PubMed  CAS  Google Scholar 

  • Javot H, Lauvergeat V, Santoni V, Martin-Laurent F, Güçlü J, Vinh J, Heyes J, Franck KI, Schäffner AR, Bouchez D, Maurel C (2003) Role of a single aquaporin isoform in root water uptake. Plant Cell 15:509–522

    Article  PubMed  CAS  Google Scholar 

  • Johanson U, Karlsson M, Johansson I, Gustavsson S, Sjövall 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, 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 

  • Kammerloher W, Fischer U, Piechottka GP, Schaffner AR (1994) Water channels in the plant plasma membrane cloned by immunoselection from a mammalian expression system. Plant J 6:187–199

    Article  PubMed  CAS  Google Scholar 

  • Karlsson M, Fotiadis D, Sjövall S, Johansson I, Hedfalk K, Engel A, Kjellbom P (2003) Reconstitution of water channel function of an aquaporin overexpressed and purified from Pichia pastoris. FEBS Lett 537:68–72

    Article  PubMed  CAS  Google Scholar 

  • Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163

    Article  PubMed  CAS  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) ClustalW and ClustalX version 2. Bioinformatics 23:2947–2948

    Article  PubMed  CAS  Google Scholar 

  • Maurel C, Tacnet F, Güclü J, Guern J, Ripoche P (1997) Purified vesicles of tobacco cell vacuolar and plasma membranes exhibit dramatically different water permeability and water channel activity. Proc Natl Acad Sci USA 94:7103–7108

    Article  PubMed  CAS  Google Scholar 

  • Maurel C, Verdoucq L, Luu DT, Santoni V (2008) Plant aquaporins: membrane channels with multiple integrated functions. Annu Rev Plant Biol 59:595–624

    Article  PubMed  CAS  Google Scholar 

  • Meyer MM, Verkman AS (1986) Human platelet osmotic water and nonelectrolyte transport. Am J Physiol 251:C549–C557

    PubMed  CAS  Google Scholar 

  • Moshelion M, Moran N, Chaumont F (2004) Dynamic changes in the osmotic water permeability of protoplast plasma membrane. Plant Physiol 135:2301–2317

    Article  PubMed  CAS  Google Scholar 

  • Mut P, Bustamante C, Martínez G, Alleva K, Sutka M, Civello M, Amodeo G (2008) A fruit- specific plasma membrane aquaporin subtype PIP1;1 is regulated during strawberry (Fragaria x ananassa) fruit ripening. Physiol Plant 132:538–551

    Article  PubMed  CAS  Google Scholar 

  • Niemietz CM, Tyerman SD (1997) Characterization of water channels in wheat root membrane vesicles. Plant Physiol 115:561–567

    PubMed  CAS  Google Scholar 

  • Peng ZH, Sharma V, Singleton SF, Gerson PD (2002) Synthesis and application of chain-terminating dinucleotide mRNA cap analog. Organic Lett 4:161–164

    Article  CAS  Google Scholar 

  • Peracchia C, Peracchia LL (2005) Inversion of both gating polarity and CO2 sensitivity of voltage gating with D3 N mutation of Cx50. Am J Physiol Cell Physiol 288(6):C1381–C1389

    Article  PubMed  CAS  Google Scholar 

  • Picaud S, Becq F, Dédaldéchamp F, Ageorges A, Derot S (2003) Cloning and expression of two plasma membrane aquaporins expressed during the ripening of grape berry. Funct Plant Biol 30:621–630

    Article  CAS  Google Scholar 

  • Postaire O, Tournaire-Roux C, Grondin A, Boursiac Y, Morillon R, Schaffner AR, Maurel C (2010) A PIP1 aquaporin contributes to hydrostatic pressure-induced water transport in both the root and rosette of Arabidopsis. Plant Physiol 152(3):1418–1430

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Qi X, Tai CY, Wasserman BP (1995) Plasma membrane intrinsic proteins of Beta vulgaris L. Plant Physiol 108:387–392

    Article  PubMed  CAS  Google Scholar 

  • Sasaki S, Ishibashi K, Nagai T, Marumo F (1992) Regulation mechanisms of intracellular pH of Xenopus laevis oocyte. Biochim Biophys Acta 1137(1):45–51

    Article  PubMed  CAS  Google Scholar 

  • Stepinsky J, Waddell C, Stolarski R, Darzynkiewicz E, Rhoads RE (2001) Synthesis and properties of mRNAs containing the novel “anti-reverse” cap analog 7-methyl(3′O-methyl)GpppG and 7-methyl(3′deoxy)GpppG. RNA 7:1486–1495

    Google Scholar 

  • Sutka M, Alleva K, Parisi M, Amodeo G (2005) Tonoplast vesicles of Beta vulgaris storage root show functional aquaporins regulated by protons. Biol Cell 97:837–846

    Article  PubMed  CAS  Google Scholar 

  • Temmei Y, Uchida S, Hoshino D, Kanzawa N, Kuwahara M, Sasaki S, Tsuchiya T (2005) Water channel activities of Mimosa pudica plasma membrane intrinsic proteins are regulated by direct interaction and phosphorylation. FEBS Lett 579:4417–4422

    Article  PubMed  CAS  Google Scholar 

  • Törnroth-Horsefield S, Wang Y, Hedfalk K, Johanson U, Karlsson M, Tajkhorshid E, Neutze R, Kjellbom P (2006) 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 

  • Vandeleur RK, Mayo G, Shelden MC, Gilliham M, Kaiser BN, Tyerman SD (2009) The role of PIP aquaporins in water transport through roots: diurnal and drought stress responses reveal different strategies between isohydric and anisohydric cultivars of grapevine. Plant Physiol 149:445–460

    Article  PubMed  CAS  Google Scholar 

  • Verdoucq L, Grondin A, Maurel C (2008) Structure-function analysis of plant aquaporin AtPIP2;1 gating by divalent cations and protons. Biochem J 415:409–416

    Article  PubMed  CAS  Google Scholar 

  • Verkman AS, Van Hoek AN, Ma T, Frigeri A, Skach WR, Mitra A, Tamarappoo BK, Farinas J (1996) Water transport across mammalian cell membranes. Am J Physiol 270:C12–C30

    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 

  • Zardoya R, Villalba S (2001) A phylogenetic framework for the aquaporin family in eukaryotes. J Mol Evol 52:391–404

    PubMed  CAS  Google Scholar 

  • Zelazny E, Borst JW, Muylaert M, Batoko H, Hemminga MA, Chaumont F (2007) FRET imaging in living maize cells reveals that plasma membrane aquaporins interact to regulate the subcellular localization. Proc Natl Acad Sci USA 104:12359–12364

    Article  PubMed  CAS  Google Scholar 

  • Zelazny E, Miecielica U, Borst JW, Hemminga MA, Chaumont F (2009) An N-terminal diacidic motif is required for the trafficking of maize aquaporins ZmPIP2;4 and ZmPIP2;5 to the plasma membrane. Plant J 57:346–355

    Article  PubMed  CAS  Google Scholar 

  • Zhang RB, Verkman AS (1991) Water and urea permeability properties of Xenopus oocytes: expression of mRNA from toad urinary bladder. Am J Physiol 260:C26–C34

    PubMed  CAS  Google Scholar 

  • Zhou Y, Setz N, Niemietz C, Qu H, Offler CE, Tyerman SD, Patrick JW (2007) Aquaporins and unloading of phloem-imported water in coats of developing bean seeds. Plant Cell Environ 30:1566–1577

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Our particular thanks are due to Noel Danjou who improved AMCAP program (version 9.20; http://noeld.com/programs.asp?cat=video#AMCap) to allow acquisition of still images as requested; Alex Paladini (INGEBI, CONICET) who designed and provided us with built-in chambers for oocyte experiments; Christophe Maurel (INRA, France) for kindly providing us with AtPIP2;2 (wild type and the H197D mutant); Mark Daniels (UCSD, USA) for the kindly gift of AtPIP2;3 cDNA; Victoria Espelt and Cora Alvarez for their invaluable contribution with the fluorimetric measurements and Alejandro C. Paladini for helpful comments in the ms. This work was financed by the PRESTAMO BID PICT04 949, UBACyT0810 and CONICET PIP5154, grants to GA and PRESTAMO BID PICT06 01804 grant to KA. KA and GA are Career Research Members of CONICET.

Author information

Authors and Affiliations

  1. Laboratorio de Biomembranas, Departamento de Fisiología, Facultad de Medicina, Universidad de Buenos Aires, Buenos Aires, Argentina

    Jorge Bellati, Karina Alleva, Victoria Vitali, Cintia Jozefkowicz & Gabriela Amodeo

  2. Instituto de Ingeniería Genética y Biología Molecular (INGEBI-CONICET), Buenos Aires, Argentina

    Gabriela Soto

  3. Departamento de Biodiversidad y Biología Experimental, Facultad de Ciencias Exactas y Naturales, UBA, Pabellón II Piso 4 Ciudad Universitaria, C1428EHA, Buenos Aires, Argentina

    Gabriela Amodeo

Authors
  1. Jorge Bellati
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Karina Alleva
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gabriela Soto
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Victoria Vitali
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Cintia Jozefkowicz
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Gabriela Amodeo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gabriela Amodeo.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bellati, J., Alleva, K., Soto, G. et al. Intracellular pH sensing is altered by plasma membrane PIP aquaporin co-expression. Plant Mol Biol 74, 105–118 (2010). https://doi.org/10.1007/s11103-010-9658-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-010-9658-8

Keywords

Search

Navigation