Skip to main content
Log in

Whole Gene Family Expression and Drought Stress Regulation of Aquaporins

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Since many aquaporins (AQPs) act as water channels, they are thought to play an important role in plant water relations. It is therefore of interest to study the expression patterns of AQP isoforms in order to further elucidate their involvement in plant water transport. We have monitored the expression patterns of all 35 Arabidopsis AQPs in leaves, roots and flowers by cDNA microarrays, specially designed for AQPs, and by quantitative real-time reverse transcriptase PCR (Q-RT-PCR). This showed that many AQPs are pre-dominantly expressed in either root or flower organs, whereas no AQP isoform seem to be leaf specific. Looking at the AQP subfamilies, most plasma membrane intrinsic proteins (PIPs) and some tonoplast intrinsic proteins (TIPs) have a high level of expression, while NOD26-like proteins (NIPs) are present at a much lower level. In addition, we show that PIP transcripts are generally down-regulated upon gradual drought stress in leaves, with the exception of AtPIP1;4 and AtPIP2;5, which are up-regulated. AtPIP2;6 and AtSIP1;1 are constitutively expressed and not significantly affected by the drought stress. The transcriptional down-regulation of PIP genes upon drought stress could also be observed on the protein level.

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

Access this article

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

Abbreviations

ABA:

abscisic acid

AQP:

aquaporin

MIP:

major intrinsic protein

NIP:

NOD26-like intrinsic protein

PIP:

plasma membrane intrinsic protein

Q-RT-PCR:

quantitative real-time reverse transcriptase PCR

SIP:

small basic intrinsic protein

TIP:

tonoplast intrinsic protein

UTR:

un-translated region

References

  • J.C. Bearden (1978) ArticleTitleQuantitation of submicrogram quantities of protein by an improved protein-dye binding assay Biochim. Biophys. Acta 533 525–529 Occurrence Handle647023

    PubMed  Google Scholar 

  • A. Biela K. Grote B. Otto S. Hoth R. Hedrich R. Kaldenhoff (1999) ArticleTitleThe Nicotiana tabacum plasma membrane aquaporin NtAQP1 is mercury-insensitive and permeable for glycerol Plant J. 18 565–570 Occurrence Handle10.1046/j.1365-313X.1999.00474.x Occurrence Handle10417707

    Article  PubMed  Google Scholar 

  • E.A. Bray (2004) ArticleTitleGenes commonly regulated by water-deficit stress in Arabidopsis thaliana J. Exp. Bot. 55 2331–2341 Occurrence Handle10.1093/jxb/erh270 Occurrence Handle15448178

    Article  PubMed  Google Scholar 

  • F. Chaumont F. Barrieu E. Wojcik M.J. Chrispeels R. Jung (2001) ArticleTitleAquaporins constitute a large and highly divergent protein family in maize Plant Physiol. 125 1206–1215 Occurrence Handle10.1104/pp.125.3.1206 Occurrence Handle11244102

    Article  PubMed  Google Scholar 

  • S.R. Cutler D.W. Ehrhardt J.S. Griffitts C.R. Somerville (2000) ArticleTitleRandom GFP:cDNA fusions enable visualization of subcellular structures in cells of Arabidopsis at a high frequency Proc. Natl. Acad. Sci. USA 97 3718–3723 Occurrence Handle10.1073/pnas.97.7.3718 Occurrence Handle10737809

    Article  PubMed  Google Scholar 

  • M.J. Daniels T.E. Mirkov M.J. Chrispeels (1994) ArticleTitleThe 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 Occurrence Handle10.1104/pp.106.4.1325 Occurrence Handle7846153

    Article  PubMed  Google Scholar 

  • C. Dordas M.J. Chrispeels P.H. Brown (2000) ArticleTitlePermeability and channel-mediated transport of boric acid across membrane vesicles isolated from squash roots Plant Physiol. 124 1349–1362 Occurrence Handle10.1104/pp.124.3.1349 Occurrence Handle11080310

    Article  PubMed  Google Scholar 

  • G.D. Farquhar J.R. Ehleringer K.T. Hubick (1989) ArticleTitleCarbon isotope discrimination and photosynthesis Annu. Plant Physiol. Plant Mol. Biol. 40 503–537 Occurrence Handle10.1146/annurev.pp.40.060189.002443

    Article  Google Scholar 

  • K. Fetter V. Wilder ParticleVan M. Moshelion F. Chaumont (2004) ArticleTitleInteractions between plasma membrane aquaporins modulate their water channel activity Plant Cell 16 215–228 Occurrence Handle10.1105/tpc.017194 Occurrence Handle14671024

    Article  PubMed  Google Scholar 

  • L.C. Fraysse B. Wells M.C. McCann P. Kjellbom (2005) ArticleTitleSpecific plasma membrane aquaporins of the PIP1 subfamily are expressed in sieve elements and guard cells Biol Cell 97 519–534 Occurrence Handle15898953

    PubMed  Google Scholar 

  • M. Gaspar A. Bousser I. Sissoëff O. Roche J. Hoarau A. Mahé (2003) ArticleTitleCloning and characterization of ZmPIP1-5b, an aquaporin transporting water and urea Plant Sci. 165 21–31 Occurrence Handle10.1016/S0168-9452(03)00117-1

    Article  Google Scholar 

  • P. Gerbeau J. Guclu P. Ripoche C. Maurel (1999) ArticleTitleAquaporin Nt-TIPa can account for the high permeability of tobacco cell vacuolar membrane to small neutral solutes Plant J. 18 577–587 Occurrence Handle10.1046/j.1365-313x.1999.00481.x Occurrence Handle10417709

    Article  PubMed  Google Scholar 

  • T. Henzler R.N. Waterhouse A.J. Smyth M. Carvajal D.T. Cooke A.R. Schäffner E. Steudle D.T. Clarkson (1999) ArticleTitleDiurnal variations in hydraulic conductivity and root pressure can be correlated with the expression of putative aquaporins in the roots of lotus japonicus Planta 210 50–60 Occurrence Handle10.1007/s004250050653 Occurrence Handle10592032

    Article  PubMed  Google Scholar 

  • A.E. Hill B. Shachar-Hill Y. Shachar-Hill (2004) ArticleTitleWhat are aquaporins for? J. Membr. Biol. 197 1–32 Occurrence Handle10.1007/s00232-003-0639-6 Occurrence Handle15014915

    Article  PubMed  Google Scholar 

  • E. Huala A.W. Dickerman M. Garcia-Hernandez D. Weems L. Reiser F. LaFond D. Hanley D. Kiphart M. Zhuang W. Huang L.A. Mueller D. Bhattacharyya D. Bhaya B.W. Sobral W. Beavis D.W. Meinke C.D. Town C. Somerville S.Y. Rhee (2001) ArticleTitleThe Arabidopsis Information Resource (TAIR): a comprehensive database and web-based information retrieval, analysis, and visualization system for a model plant Nucleic Acids Res. 29 102–105 Occurrence Handle10.1093/nar/29.1.102 Occurrence Handle11125061

    Article  PubMed  Google Scholar 

  • T.P. Jahn A.L. Moller T. Zeuthen L.M. Holm D.A. Klaerke B. Mohsin W. Kuhlbrandt J.K. Schjoerring (2004) ArticleTitleAquaporin homologues in plants and mammals transport ammonia FEBS Lett. 574 31–36 Occurrence Handle10.1016/j.febslet.2004.08.004 Occurrence Handle15358535

    Article  PubMed  Google Scholar 

  • J.Y. Jang D.G. Kim Y.O. Kim J.S. Kim H. Kang (2004) ArticleTitleAn expression analysis of a gene family encoding plasma membrane aquaporins in response to abiotic stresses in Arabidopsis thaliana Plant Mol. Biol. 54 713–725 Occurrence Handle10.1023/B:PLAN.0000040900.61345.a6 Occurrence Handle15356390

    Article  PubMed  Google Scholar 

  • H. Javot V. Lauvergeat V. Santoni F. Martin-Laurent J. Guclu J. Vinh J. Heyes K.I. Franck A.R. Schäffner D. Bouchez C. Maurel (2003) ArticleTitleRole of a single aquaporin isoform in root water uptake Plant Cell 15 509–522 Occurrence Handle10.1105/tpc.008888 Occurrence Handle12566588

    Article  PubMed  Google Scholar 

  • U. Johanson M. Karlsson I. Johansson S. Gustavsson S. Sjovall L. Fraysse A.R. Weig P. Kjellbom (2001) ArticleTitleThe 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 Occurrence Handle10.1104/pp.126.4.1358 Occurrence Handle11500536

    Article  PubMed  Google Scholar 

  • I. Johansson C. Larsson B. Ek P. Kjellbom (1996) ArticleTitleThe 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 Occurrence Handle10.1105/tpc.8.7.1181 Occurrence Handle8768376

    Article  PubMed  Google Scholar 

  • I. Johansson M. Karlsson V.K. Shukla M.J. Chrispeels C. Larsson P. Kjellbom (1998) ArticleTitleWater transport activity of the plasma membrane aquaporin PM28A is regulated by phosphorylation Plant Cell 10 451–459 Occurrence Handle10.1105/tpc.10.3.451 Occurrence Handle9501117

    Article  PubMed  Google Scholar 

  • R. Kaldenhoff K. Grote J.J. Zhu U. Zimmermann (1998) ArticleTitleSignificance of plasmalemma aquaporins for water-transport in Arabidopsis thaliana Plant J. 14 121–128 Occurrence Handle10.1046/j.1365-313X.1998.00111.x Occurrence Handle9681029

    Article  PubMed  Google Scholar 

  • R. Kaldenhoff A. Kolling J. Meyers U. Karmann G. Ruppel G. Richter (1995) ArticleTitleThe blue light-responsive AthH2 gene of Arabidopsis thaliana is primarily expressed in expanding as well as in differentiating cells and encodes a putative channel protein of the plasmalemma Plant J. 7 87–95 Occurrence Handle10.1046/j.1365-313X.1995.07010087.x Occurrence Handle7534555

    Article  PubMed  Google Scholar 

  • W. Kammerloher U. Fischer G.P. Piechottka A.R. Schäffner (1994) ArticleTitleWater channels in the plant plasma membrane cloned by immunoselection from a mammalian expression system Plant J. 6 187–199 Occurrence Handle10.1046/j.1365-313X.1994.6020187.x Occurrence Handle7920711

    Article  PubMed  Google Scholar 

  • R. Kawaguchi T. Girke E.A. Bray J. Bailey-Serres (2004) ArticleTitleDifferential mRNA translation contributes to gene regulation under non-stress and dehydration stress conditions in Arabidopsis thaliana Plant J. 38 823–839 Occurrence Handle10.1111/j.1365-313X.2004.02090.x Occurrence Handle15144383

    Article  PubMed  Google Scholar 

  • F. Klebl M. Wolf N. Sauer (2003) ArticleTitleA defect in the yeast plasma membrane urea transporter Dur3p is complemented by CpNIP1, a Nod26-like protein from zucchini (Cucurbita pepo L.), and by Arabidopsis thaliana delta-TIP or gamma-TIP FEBS Lett. 547 69–74 Occurrence Handle10.1016/S0014-5793(03)00671-9 Occurrence Handle12860388

    Article  PubMed  Google Scholar 

  • J.A. Kreps Y. Wu H.S. Chang T. Zhu X. Wang J.F. Harper (2002) ArticleTitleTranscriptome changes for Arabidopsis in response to salt, osmotic, and cold stress Plant Physiol. 130 2129–2141 Occurrence Handle10.1104/pp.008532 Occurrence Handle12481097

    Article  PubMed  Google Scholar 

  • U.K. Laemmli (1970) ArticleTitleCleavage of structural proteins during the assembly of the head of bacteriophage T4 Nature 227 680–685 Occurrence Handle10.1038/227680a0 Occurrence Handle5432063

    Article  PubMed  Google Scholar 

  • V. Lång E. Mantyla B. Welin B. Sundberg E.T. Palva (1994) ArticleTitleAlterations in Water Status, Endogenous Abscisic Acid Content, and Expression of rab18 Gene during the Development of Freezing Tolerance in Arabidopsis thaliana Plant Physiol. 104 1341–1349 Occurrence Handle12232173

    PubMed  Google Scholar 

  • L.H. Liu U. Ludewig B. Gassert W.B. Frommer N. Wiren Particlevon (2003) ArticleTitleUrea transport by nitrogen-regulated tonoplast intrinsic proteins in Arabidopsis Plant Physiol. 133 1220–1228 Occurrence Handle10.1104/pp.103.027409 Occurrence Handle14576283

    Article  PubMed  Google Scholar 

  • F. Lopez A. Bousser I. Sissoeff M. Gaspar B. Lachaise J. Hoarau A. Mahe (2003) ArticleTitleDiurnal regulation of water transport and aquaporin gene expression in maize roots: contribution of PIP2 proteins Plant Cell Physiol. 44 1384–1395 Occurrence Handle10.1093/pcp/pcg168 Occurrence Handle14701934

    Article  PubMed  Google Scholar 

  • D. Loque U. Ludewig L. Yuan N. Wiren Particlevon (2005) ArticleTitleTonoplast intrinsic proteins AtTIP2;1 and AtTIP2;3 facilitate NH3 transport into the vacuole Plant Physiol. 137 671–680 Occurrence Handle10.1104/pp.104.051268 Occurrence Handle15665250

    Article  PubMed  Google Scholar 

  • F.J. Maathuis V. Filatov P. Herzyk G.C. Krijger K.B. Axelsen S. Chen B.J. Green Y. Li K.L. Madagan R. Sanchez-Fernandez B.G. Forde M.G. Palmgren P.A. Rea L.E. Williams D. Sanders A. Amtmann (2003) ArticleTitleTranscriptome analysis of root transporters reveals participation of multiple gene families in the response to cation stress Plant J 35 675–692 Occurrence Handle10.1046/j.1365-313X.2003.01839.x Occurrence Handle12969422

    Article  PubMed  Google Scholar 

  • C. Maurel R.T. Kado J. Guern M.J. Chrispeels (1995) ArticleTitlePhosphorylation regulates the water channel activity of the seed-specific aquaporin alpha-TIP Embo. J. 14 3028–3035 Occurrence Handle7542585

    PubMed  Google Scholar 

  • M. Moshelion D. Becker A. Biela N. Uehlein R. Hedrich B. Otto H. Levi N. Moran R. Kaldenhoff (2002) ArticleTitlePlasma membrane aquaporins in the motor cells of Samanea saman: diurnal and circadian regulation Plant Cell 14 727–739 Occurrence Handle10.1105/tpc.010351 Occurrence Handle11910017

    Article  PubMed  Google Scholar 

  • M. Nylander J. Svensson E.T. Palva B.V. Welin (2001) ArticleTitleStress-induced accumulation and tissue-specific localization of dehydrins in Arabidopsis thaliana Plant Mol. Biol. 45 263–279 Occurrence Handle10.1023/A:1006469128280 Occurrence Handle11292073

    Article  PubMed  Google Scholar 

  • Y. Oono M. Seki T. Nanjo M. Narusaka M. Fujita R. Satoh M. Satou T. Sakurai J. Ishida K. Akiyama K. Iida K. Maruyama S. Satoh K. Yamaguchi-Shinozaki K. Shinozaki (2003) ArticleTitleMonitoring expression profiles of Arabidopsis gene expression during rehydration process after dehydration using ca 7000 full-length cDNA microarray Plant J. 34 868–887 Occurrence Handle10.1046/j.1365-313X.2003.01774.x Occurrence Handle12795706

    Article  PubMed  Google Scholar 

  • G.M. Preston T.P. Carroll W.B. Guggino P. Agre (1992) ArticleTitleAppearance of water channels in Xenopus oocytes expressing red cell CHIP28 protein Science 256 385–387 Occurrence Handle1373524

    PubMed  Google Scholar 

  • A.R. Schäffner (1998) ArticleTitleAquaporin function, structure, and expression: are there more surprises to surface in water relations? Planta 204 131–139 Occurrence Handle10.1007/s004250050239 Occurrence Handle9487723

    Article  PubMed  Google Scholar 

  • M. Seki M. Narusaka H. Abe M. Kasuga K. Yamaguchi-Shinozaki P. Carninci Y. Hayashizaki K. Shinozaki (2001) ArticleTitleMonitoring the expression pattern of 1300 Arabidopsis genes under drought and cold stresses by using a full-length cDNA microarray Plant Cell 13 61–72 Occurrence Handle10.1105/tpc.13.1.61 Occurrence Handle11158529

    Article  PubMed  Google Scholar 

  • M. Seki M. Narusaka J. Ishida T. Nanjo M. Fujita Y. Oono A. Kamiya M. Nakajima A. Enju T. Sakurai M. Satou K. Akiyama T. Taji K. Yamaguchi-Shinozaki P. Carninci J. Kawai Y. Hayashizaki K. Shinozaki (2002a) ArticleTitleMonitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray Plant J. 31 279–292 Occurrence Handle10.1046/j.1365-313X.2002.01359.x

    Article  Google Scholar 

  • M. Seki J. Ishida M. Narusaka M. Fujita T. Nanjo T. Umezawa A. Kamiya M. Nakajima A. Enju T. Sakurai M. Satou K. Akiyama K. Yamaguchi-Shinozaki P. Carninci J. Kawai Y. Hayashizaki K. Shinozaki (2002b) ArticleTitleMonitoring the expression pattern of around 7000 Arabisopsis genes under ABA treatments using a full-length cDNA microarray Funct. Integr. Genomics 2 282–291 Occurrence Handle10.1007/s10142-002-0070-6

    Article  Google Scholar 

  • F. Siefritz M.T. Tyree C. Lovisolo A. Schubert R. Kaldenhoff (2002) ArticleTitlePIP1 plasma membrane aquaporins in tobacco: from cellular effects to function in plants Plant Cell 14 869–876 Occurrence Handle10.1105/tpc.000901 Occurrence Handle11971141

    Article  PubMed  Google Scholar 

  • C. Tournaire-Roux M. Sutka H. Javot E. Gout P. Gerbeau D.T. Luu R. Bligny C. Maurel (2003) ArticleTitleCytosolic pH regulates root water transport during anoxic stress through gating of aquaporins Nature 425 393–397 Occurrence Handle10.1038/nature01853 Occurrence Handle14508488

    Article  PubMed  Google Scholar 

  • S.D. Tyerman C.M. Niemietz H. Bramley (2002) ArticleTitlePlant aquaporins: multifunctional water and solute channels with expanding roles Plant Cell Environ. 25 173–194 Occurrence Handle10.1046/j.0016-8025.2001.00791.x Occurrence Handle11841662

    Article  PubMed  Google Scholar 

  • N. Uehlein C. Lovisolo F. Siefritz R. Kaldenhoff (2003) ArticleTitleThe tobacco aquaporin NtAQP1 is a membrane CO2 pore with physiological functions Nature 425 734–737 Occurrence Handle10.1038/nature02027 Occurrence Handle14520414

    Article  PubMed  Google Scholar 

  • A. Weig C. Deswarte M.J. Chrispeels (1997) ArticleTitleThe major intrinsic protein family of Arabidopsis has 23 members that form three distinct groups with functional aquaporins in each group Plant Physiol 114 1347–1357 Occurrence Handle10.1104/pp.114.4.1347 Occurrence Handle9276952

    Article  PubMed  Google Scholar 

  • A.R. Weig C. Jakob (2000) ArticleTitleFunctional identification of the glycerol permease activity of Arabidopsis thaliana NLM1 and NLM2 proteins by heterologous expression in Saccharomyces cerevisiae FEBS Lett. 481 293–298 Occurrence Handle10.1016/S0014-5793(00)02027-5 Occurrence Handle11007982

    Article  PubMed  Google Scholar 

  • R. Vera-Estrella B.J. Barkla H.J. Bohnert O. Pantoja (2004) ArticleTitleNovel regulation of aquaporins during osmotic stress Plant Physiol. 135 2318–2329 Occurrence Handle10.1104/pp.104.044891 Occurrence Handle15299122

    Article  PubMed  Google Scholar 

  • W. Xu S. Bak A. Decker S.M. Paquette R. Feyereisen D.W. Galbraith (2001) ArticleTitleMicroarray-based analysis of gene expression in very large gene families: the cytochrome P450 gene superfamily of Arabidopsis thaliana Gene 272 61–74 Occurrence Handle10.1016/S0378-1119(01)00516-9 Occurrence Handle11470511

    Article  PubMed  Google Scholar 

  • P. Zimmermann M. Hirsch-Hoffmann L. Hennig W. Gruissem (2004) ArticleTitleGENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox Plant Physiol. 136 2621–2632 Occurrence Handle10.1104/pp.104.046367 Occurrence Handle15375207

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Erik Alexandersson.

Electronic Supplementary Material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Alexandersson, E., Fraysse, L., Sjövall-Larsen, S. et al. Whole Gene Family Expression and Drought Stress Regulation of Aquaporins. Plant Mol Biol 59, 469–484 (2005). https://doi.org/10.1007/s11103-005-0352-1

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-005-0352-1

Key words

Navigation