Skip to main content
Log in

PIP Aquaporin Gene Expression in Arbuscular Mycorrhizal Glycine max and Lactuca  sativa Plants in Relation to Drought Stress Tolerance

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Although the discovery of aquaporins in plants has resulted in a paradigm shift in the understanding of plant water relations, the relationship between aquaporins and plant responses to drought still remains elusive. Moreover, the contribution of aquaporin genes to the enhanced tolerance to drought in arbuscular mycorrhisal (AM) plants has never been investigated. Therefore, we studied, at a molecular level, whether the expression of aquaporin-encoding genes in roots is altered by the AM symbiosis as a mechanism to enhance host plant tolerance to water deficit. In this study, genes encoding plasma membrane aquaporins (PIPs) from soybean and lettuce were cloned and their expression pattern studied in AM and nonAM plants cultivated under well-watered or drought stressed conditions. Results showed that AM plants responded to drought stress by down-regulating the expression of the PIP genes studied and anticipating its down-regulation as compared to nonAM plants. The possible physiological implications of this down-regulation of PIP genes as a mechanism to decrease membrane water permeability and to allow cellular water conservation is further discussed.

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.

Similar content being viewed by others

References

  • R. Aharon Y. Shahak S. Wininger R. Bendov Y. Kapulnik G. Galili (2003) ArticleTitleOverexpression of a plasma membrane aquaporins in transgenic tobacco improves plant vigour under favourable growth conditions but not under drought or salt stress Plant Cell 15 439–447 Occurrence Handle10.1105/tpc.009225 Occurrence Handle1:CAS:528:DC%2BD3sXhtlOmtbg%3D Occurrence Handle12566583

    Article  CAS  PubMed  Google Scholar 

  • R. Aroca G. Amodeo S. Fernández-Illescas E.M. Herman F. Chaumont M.J. Chrispeels (2005) ArticleTitleThe role of aquaporins and membrane damage in chilling and hydrogen peroxide induced changes in the hydraulic conductance of maize roots Plant Physiol. 137 341–353 Occurrence Handle10.1104/pp.104.051045 Occurrence Handle1:CAS:528:DC%2BD2MXhtFOlsLY%3D Occurrence Handle15591439

    Article  CAS  PubMed  Google Scholar 

  • R.M. Augé (2001) ArticleTitleWater relations, drought and vesicular-arbuscular mycorrhizal symbiosis Mycorrhiza 11 3–42

    Google Scholar 

  • R.M. Augé (2004) ArticleTitleArbuscular mycorrhizae and soil/plant water relations Can. J. Soil Sci. 84 373–381

    Google Scholar 

  • F. Barrieu D. Marty-Mazars D. Thomas F. Chaumont M. Charbonnier F. Marty (1999) ArticleTitleDesiccation and osmotic stress increase the abundance of mRNA of the tonoplast aquaporin BobTIP26–1 in cauliflower cells Planta 209 77–86 Occurrence Handle1:CAS:528:DyaK1MXkvVCltbs%3D Occurrence Handle10467033

    CAS  PubMed  Google Scholar 

  • H.J. Bohnert D.E. Nelson R.G. Jensen (1995) ArticleTitleAdaptations to environmental stresses Plant Cell 7 1099–1111 Occurrence Handle10.1105/tpc.7.7.1099 Occurrence Handle1:CAS:528:DyaK2MXnt1Sgt7Y%3D Occurrence Handle12242400

    Article  CAS  PubMed  Google Scholar 

  • P. Bonfante S. Perotto (1995) ArticleTitleStrategies of arbuscular mycorrhizal fungi when infecting host plants New Phytol. 130 3–21

    Google Scholar 

  • M. Bots R. Feron N. Uehlein K. Weterings R. Kaldenhoff T. Mariani (2005) ArticleTitlePIP1 and PIP2 aquaporins are differentially expressed during tobacco anther and stigma development J. Exp. Bot. 56 113–121 Occurrence Handle1:CAS:528:DC%2BD2MXkt1Wmsg%3D%3D Occurrence Handle15520027

    CAS  PubMed  Google Scholar 

  • S.H. Burleigh T. Cavagnaro I. Jakobsen (2002) ArticleTitleFunctional diversity of arbuscular mycorrhizas extends to the expression of plant genes involved in P nutrition J. Exp. Bot. 53 1593–1601 Occurrence Handle10.1093/jxb/erf013 Occurrence Handle1:CAS:528:DC%2BD38XlsFSmsbw%3D Occurrence Handle12096098

    Article  CAS  PubMed  Google Scholar 

  • F. Chaumont F. Barrieu R. Jung M.J. Chrispeels (2000) ArticleTitlePlasma membrane intrinsic proteins from maize cluster in two sequence subgroups with differential aquaporin activity Plant Physiol. 122 1025–1034 Occurrence Handle10.1104/pp.122.4.1025 Occurrence Handle1:CAS:528:DC%2BD3cXktFSqtb4%3D Occurrence Handle10759498

    Article  CAS  PubMed  Google Scholar 

  • M.J. Chrispeels P. Agre (1994) ArticleTitleAquaporins: water channel proteins of plant and animal cells Trends Biochem. Sci. 19 421–425 Occurrence Handle10.1016/0968-0004(94)90091-4 Occurrence Handle1:CAS:528:DyaK2MXhvFWntL8%3D Occurrence Handle7529436

    Article  CAS  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 Handle1:CAS:528:DyaK2MXislensbo%3D Occurrence Handle7846153

    Article  CAS  PubMed  Google Scholar 

  • R.M. Dean R.L. Rivers M.L. Zeidel D.M. Roberts (1999) ArticleTitlePurification and functional reconstitution of soybean Nodulin 26. An aquaporin with water and glycerol transport properties Biochemistry 38 347–353 Occurrence Handle10.1021/bi982110c Occurrence Handle1:CAS:528:DyaK1cXnvValtrY%3D Occurrence Handle9890916

    Article  CAS  PubMed  Google Scholar 

  • D.B. Duncan (1955) ArticleTitleMultiple range and multiple F-tests Biometrics 11 1–42

    Google Scholar 

  • B.A. Faber R.J. Zasoski D.N. Munns (1991) ArticleTitleA method for measuring hyphal nutrient and water uptake in mycorrhizal plants Can. J. Bot. 69 87–94

    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 Handle1:CAS:528:DC%2BD2cXosVeksg%3D%3D Occurrence Handle14671024

    Article  CAS  PubMed  Google Scholar 

  • R.G. Fray A. Wallace D. Grierson G.W. Lycett (1994) ArticleTitleNucleotide sequence and expression of a ripening and water stress-related cDNA from tomato with homology to the MIP class of membrane channel proteins Plant Mol. Biol. 24 539–543 Occurrence Handle10.1007/BF00024122 Occurrence Handle1:CAS:528:DyaK2cXksFamt7s%3D Occurrence Handle7510135

    Article  CAS  PubMed  Google Scholar 

  • V. Gianinazzi-Pearson (1996) ArticleTitlePlant cell response to arbuscular mycorrhizal fungi: getting to the roots of the symbiosis Plant Cell 8 1871–1883 Occurrence Handle10.1105/tpc.8.10.1871 Occurrence Handle12239368

    Article  PubMed  Google Scholar 

  • M. Giovannetti B. Mosse (1980) ArticleTitleAn evaluation of techniques for measuring vesicular-arbuscular infection in roots New Phytol. 84 489–500

    Google Scholar 

  • N. Goicoechea M.C. Antolin M. Sánchez-Díaz (1997) ArticleTitleGas exchange is related to the hormone balance in mycorrhizal or nitrogen-fixing alfalfa subjected to drought Physiol. Plant. 100 989–997 Occurrence Handle10.1034/j.1399-3054.1997.1000427.x Occurrence Handle1:CAS:528:DyaK2sXlvFCiurk%3D

    Article  CAS  Google Scholar 

  • K. Grote P. Trzebiatovski R. Kaldenhoff (1998) ArticleTitleRNA levels of plasma membrane aquaporins in Arabidopsis  thaliana Protoplasma 204 139–144 Occurrence Handle10.1007/BF01280320 Occurrence Handle1:CAS:528:DyaK1MXitVeqsr8%3D

    Article  CAS  Google Scholar 

  • K. Hardie (1985) ArticleTitleThe effect of removal of extraradical hyphae on water uptake by vesicular-arbuscular mycorrhizal plants New Phytol. 101 677–684

    Google Scholar 

  • D.L. Herrin G.W. Schmidt (1988) ArticleTitleRapid, reversible staining of northern blot prior to hybridization Biotechniques 6 196 Occurrence Handle1:CAS:528:DyaL1cXitVWjsbk%3D Occurrence Handle2483319

    CAS  PubMed  Google Scholar 

  • Hewitt, E.J. 1952. Sand and water culture methods used in the study of plant nutrition. Technical Communication 22, Farnham Royal, Commonwealth Agricultural Bureaux, Bucks

  • J. Ingram D. Bartels (1996) ArticleTitleThe molecular basis of dehydration tolerance in plants Annu. Rev. Plant Physiol. Plant Mol. Biol. 47 377–403 Occurrence Handle10.1146/annurev.arplant.47.1.377 Occurrence Handle1:CAS:528:DyaK28XjtlWgtr0%3D Occurrence Handle15012294

    Article  CAS  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 Handle1:CAS:528:DC%2BD2cXptlCrtLg%3D Occurrence Handle15356390

    Article  CAS  PubMed  Google Scholar 

  • H. Javot V. Lauvergeat V. Santoni F. Martin-Laurent J. Guclu J. Vinh J. Heyes K.I. Franck A.R. Schaffner 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 Handle1:CAS:528:DC%2BD3sXhtlOmur8%3D Occurrence Handle12566588

    Article  CAS  PubMed  Google Scholar 

  • H. Javot C. Maurel (2002) ArticleTitleThe role of aquaporins in root water uptake Ann. Bot. 90 301–313 Occurrence Handle10.1093/aob/mcf199 Occurrence Handle1:CAS:528:DC%2BD38XnvVOhu7k%3D Occurrence Handle12234142

    Article  CAS  PubMed  Google Scholar 

  • I. Johanson 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

    Google Scholar 

  • U. Johanson M. Karlsson I. Johanson S. Gustavsson S. Sjövall L. Fraysse A.R. Weigh 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 Handle1:CAS:528:DC%2BD3MXlvFOjtbk%3D Occurrence Handle11500536

    Article  CAS  PubMed  Google Scholar 

  • K.D. Johnson H. Höftem M.J. Chrispeels (1990) ArticleTitleAn intrinsic tonoplast protein of proteins storage vacuoles in seeds is structurally related to a bacterial solute transporter (GlpF) Plant Cell 2 525–532 Occurrence Handle10.1105/tpc.2.6.525 Occurrence Handle1:CAS:528:DyaK3MXitlCi Occurrence Handle2152174

    Article  CAS  PubMed  Google Scholar 

  • W. Kammerloher U. Fischer G.P. Pienchottka 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 Handle1:CAS:528:DyaK2MXhtlGntL8%3D Occurrence Handle7920711

    Article  CAS  PubMed  Google Scholar 

  • R. Kay A. Chau M. Daly (1987) ArticleTitleDuplication of CaMV 35S promoter sequences creates a strong enhancer for plants genes Science 236 1299–1302 Occurrence Handle1:CAS:528:DyaL2sXksFeisrw%3D

    CAS  Google Scholar 

  • P. Kjelbom C. Larsson I. Johansson M. Karlsson U. Johanson (1999) ArticleTitleAquaporins and water homeostasis in plants Trends Plant Sci. 4 308–314

    Google Scholar 

  • F. Krajinski A. Biela D. Schubert V. Gianinazzi-Pearson R. Kaldenhoff P. Franken (2000) ArticleTitleArbuscular mycorrhiza development regulates the mRNA abundance of Mtaqp1 encoding a mercury-insensitive aquaporin of Medicago  truncatula Planta 211 85–90 Occurrence Handle10.1007/s004250000263 Occurrence Handle1:CAS:528:DC%2BD3cXjvVyhsLs%3D Occurrence Handle10923707

    Article  CAS  PubMed  Google Scholar 

  • P.J. Kramer J.S. Boyer (1997) Water Relations of Plants and Soils Academic Press San Diego

    Google Scholar 

  • H.L. Lian X. Yu Q. Ye X.S. Ding Y. Kitagawa S.S. Swak W.A. Su Z.C. Tang (2004) ArticleTitleThe role of aquaporin RWC3 in drought avoidance in rice Plant Cell Physiol. 15 481–489

    Google Scholar 

  • K.J. Livak T.D. Schmittgen (2001) ArticleTitleAnalysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCt method Methods 25 402–408 Occurrence Handle10.1006/meth.2001.1262 Occurrence Handle1:CAS:528:DC%2BD38XhtFelt7s%3D Occurrence Handle11846609

    Article  CAS  PubMed  Google Scholar 

  • D.T. Luu C. Maurel (2005) ArticleTitleAquaporins in a challenging environment: molecular gears for adjusting plant water status Plant Cell Environ. 28 85–96 Occurrence Handle10.1111/j.1365-3040.2004.01295.x Occurrence Handle1:CAS:528:DC%2BD2MXhsVGqtLY%3D

    Article  CAS  Google Scholar 

  • J.B. Mariaux C. Bockel F. Salamini D. Bartels (1998) ArticleTitleDesiccation- and abscisic acid-responsive genes encoding major intrinsic proteins (MIPs) from the resurrection plant Craterostigma  plantagineum Plant Mol. Biol. 38 1089–1099 Occurrence Handle10.1023/A:1006013130681 Occurrence Handle1:CAS:528:DyaK1MXksVClsA%3D%3D Occurrence Handle9869415

    Article  CAS  PubMed  Google Scholar 

  • Marjanovic, Z., Uehlein, N., Kaldenhoff, R., Zwiazek, J.J., Weiß, M., Hampp, R. and Nehls, U. 2005. Aquaporins in poplar: what a difference a simbiont makes! Planta (DOI: 10.1007/s00425–005–1539-z)

  • P. Martre R. Morillon F. Barrieu G.B. North P.S. Nobel M.J. Chrispeels (2002) ArticleTitlePlasma membrane aquaporins play a significant role during recovery from water deficit Plant Physiol. 130 2101–2110 Occurrence Handle10.1104/pp.009019 Occurrence Handle1:CAS:528:DC%2BD3sXktlyh Occurrence Handle12481094

    Article  CAS  PubMed  Google Scholar 

  • A. Marulanda R. Azcón J.M. Ruiz-Lozano (2003) ArticleTitleContribution of six arbuscular mycorrhizal fungal isolates to water uptake by Lactuca  sativa L. plants under drought stress Physiol. Plant. 119 526–533 Occurrence Handle10.1046/j.1399-3054.2003.00196.x Occurrence Handle1:CAS:528:DC%2BD3sXpslShtbY%3D

    Article  CAS  Google Scholar 

  • C. Maurel (1997) ArticleTitleAquaporins and water permeability of plant membranes Annu. Rev. Plant Physiol. Plant Mol. Biol. 48 399–429 Occurrence Handle10.1146/annurev.arplant.48.1.399 Occurrence Handle1:CAS:528:DyaK2sXjs1ems7w%3D Occurrence Handle15012269

    Article  CAS  PubMed  Google Scholar 

  • C. Maurel H. Javot V. Lauvergeat P. Gerbeau C. Tournaire V. Santoni J. Heyes (2002) ArticleTitleMolecular physiology of aquaporins in plants Inter. Revi. Cytol. 215 105–148 Occurrence Handle1:CAS:528:DC%2BD38XjsFCrt74%3D

    CAS  Google Scholar 

  • C.M. Niemietz S.D. Tyerman (2000) ArticleTitleChannel-mediated permeation of ammonia gas through the peribacteroid membrane of soybean nodules FEBS Lett. 465 110–114 Occurrence Handle10.1016/S0014-5793(99)01729-9 Occurrence Handle1:CAS:528:DC%2BD3cXjtV2qtg%3D%3D Occurrence Handle10631315

    Article  CAS  PubMed  Google Scholar 

  • J.H. Numberg D.K. Wright G.E. Cole E.A. Petrovskis L.E. Post T. Compton J.H. Gilbert (1989) ArticleTitleIdentification of the thymidine kinase gene of feline herpesvirus: use of degenerate oligonucleotides in the polymerase chain reaction to isolate herpesvirus gene homologs J. Virol. 63 3240–3249

    Google Scholar 

  • Ouziad, F., Wilde, P., Schmelzer, E., Hildebrandt, U. and Bothe, H. 2005. Analysis of expression of aquaporins and Na+/H+ transporters in tomato colonized by arbuscular mycorrhizal fungi and affected by salt stress. Environ. Exp. Bot. (doi: 10.1016/j.envexpbot.2005.05.011)

  • J.M. Phillips D.S. Hayman (1970) ArticleTitleImproved procedure of clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection Trans. Brit. Mycol. Soc. 55 159–161

    Google Scholar 

  • R. Porcel R. Azcón J.M. Ruiz-Lozano (2004) ArticleTitleEvaluation of the role of genes encoding for Δ1-pyrroline−5-carboxylate synthetase (P5CS) during drought stress in arbuscular mycorrhizal Glycine max and Lactuca  sativa plants Physiol. Mol. Plant Pathol. 65 211–221 Occurrence Handle10.1016/j.pmpp.2005.02.003

    Article  Google Scholar 

  • R. Porcel R. Azcón J.M. Ruiz-Lozano (2005b) ArticleTitleEvaluation of the role of genes encoding for dehydrin proteins (LEA D−11) during drought stress in arbuscular mycorrhizal Glycine max and Lactuca  sativa plants J. Exp. Bot. 56 1933–1942 Occurrence Handle10.1093/jxb/eri188 Occurrence Handle1:CAS:528:DC%2BD2MXpvFKntbw%3D

    Article  CAS  Google Scholar 

  • R. Porcel J.M. Barea J.M. Ruiz-Lozano (2003) ArticleTitleAntioxidant activities in mycorrhizal soybean plants under drought stress and their possible relationship to the process of nodule senescence New Phytol. 157 135–143 Occurrence Handle10.1046/j.1469-8137.2003.00658.x Occurrence Handle1:CAS:528:DC%2BD3sXht1Siu74%3D

    Article  CAS  Google Scholar 

  • R. Porcel M. Gómez R. Kaldenhoff J.M. Ruiz-Lozano (2005a) ArticleTitleImpairment of NtAQP1 gene expression in tobacco plants does not affect root colonization pattern by arbuscular mycorrhizal fungi but decreases their symbiotic efficiency under drought Mycorrhiza 15 417–423 Occurrence Handle10.1007/s00572-005-0346-5 Occurrence Handle1:CAS:528:DC%2BD2MXos1Gisro%3D

    Article  CAS  Google Scholar 

  • R. Porcel J.M. Ruiz-Lozano (2004) ArticleTitleArbuscular mycorrhizal influence on leaf water potential, solute accumulation and oxidative stress in soybean plants subjected to drought stress J. Exp. Bot. 55 1743–1750 Occurrence Handle10.1093/jxb/erh188 Occurrence Handle1:CAS:528:DC%2BD2cXntValt7s%3D Occurrence Handle15208335

    Article  CAS  PubMed  Google Scholar 

  • H. Roussel S. Bruns V. Gianinazzi-Pearson K. Hahlbrock P. Franken (1997) ArticleTitleInduction of a membrane intrinsic protein-encoding mRNA in arbuscular mycorrhiza and elicitor-stimulated cell suspension cultures of parsley Plant Sci. 126 203–210 Occurrence Handle10.1016/S0168-9452(97)00106-4 Occurrence Handle1:CAS:528:DyaK2sXkvVWit7Y%3D

    Article  CAS  Google Scholar 

  • J.M. Ruiz-Lozano (2003) ArticleTitleArbuscular mycorrhizal symbiosis and alleviation of osmotic stress. New perspectives for molecular studies Mycorrhiza 13 309–317 Occurrence Handle10.1007/s00572-003-0237-6 Occurrence Handle12690537

    Article  PubMed  Google Scholar 

  • J.M. Ruiz-Lozano R. Azcón (1995) ArticleTitleHyphal contribution to water uptake in mycorrhizal plants as affected by the␣fungal species and water status Physiol. Plant. 95 472–478 Occurrence Handle10.1034/j.1399-3054.1995.950320.x Occurrence Handle1:CAS:528:DyaK28XltFKi

    Article  CAS  Google Scholar 

  • J.M. Ruiz-Lozano R. Azcón (1997) ArticleTitleEffect of calcium application on the tolerance of mycorrhizal lettuce plants to␣polyethylene glycol-induced water stress Symbiosis 23 9–22

    Google Scholar 

  • J.M. Ruiz-Lozano C. Collados R. Porcel R. Azcón J.M. Barea (2002) ArticleTitleIdentification of a cDNA from the arbuscular mycorrhizal fungus Glomus intraradices which is expressed during symbiosis and up-regulated by N fertilization Mol. Plant-Microbe Interact. 15 360–367 Occurrence Handle1:CAS:528:DC%2BD38XivV2mt7g%3D Occurrence Handle12026174

    CAS  PubMed  Google Scholar 

  • J. Sambrook E.F. Fritsch T.A. Maniatis (1989) Molecular Cloning: A Laboratory Manual EditionNumber2 Cold Spring Harbor Laboratory Press Cold Spring Harbor, NY

    Google Scholar 

  • F. Sanger S. Nicklen A.R. Coulsen (1977) ArticleTitleDNA sequencing with chain terminating inhibitors Proc. Natl. Acad. Sci. USA 74 5463–5467 Occurrence Handle1:CAS:528:DyaE1cXhtlaru7Y%3D Occurrence Handle271968

    CAS  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 Handle9487723

    PubMed  Google Scholar 

  • G. Sheng M. Sagi S. Weining T. Krugman T. A.B. Fahima Korol E. Nevo (2004) ArticleTitleWild barley eibi1 mutation identifies a gene essential for leaf water conservation Planta 219 684–693

    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 Handle1:CAS:528:DC%2BD38XjsFWktrw%3D Occurrence Handle11971141

    Article  CAS  PubMed  Google Scholar 

  • L.B. Smart W.A. Moskal K.D. Cameron A.B. Bennett (2001) ArticleTitleMip genes are down-regulated under drought stress in Nicotiana glauca Plant Cell Physiol. 42 686–693 Occurrence Handle10.1093/pcp/pce085 Occurrence Handle1:CAS:528:DC%2BD3MXlsVeqtr0%3D Occurrence Handle11479374

    Article  CAS  PubMed  Google Scholar 

  • S.E. Smith D.J. Read (1997) Mycorrhizal Symbiosis Academic Press San Diego, CA

    Google Scholar 

  • R.M. Tobar R. Azcón J.M. Barea (1994a) ArticleTitleThe improvement of plant N acquisition from an ammonium-treated, drought-stressed soil by the fungal symbiont in arbuscular mycorrhizae Mycorrhiza 4 105–108 Occurrence Handle10.1007/BF00203769

    Article  Google Scholar 

  • R.M. Tobar R. Azcón J.M. Barea (1994b) ArticleTitleImproved nitrogen uptake and transport from 15N-labelled nitrate by external hyphae of arbuscular mycorrhiza under water-stressed conditions New Phytol. 126 119–122

    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 Handle1:CAS:528:DC%2BD38Xhslaktbk%3D Occurrence Handle11841662

    Article  CAS  PubMed  Google Scholar 

  • S. Yamada M. Katsuhara W.B. Kelly C.B. Michalowski H.J. Bonhert (1995) ArticleTitleA family of transcripts encoding water channel proteins: tissue-specific expression in common ice plant Plant Cell 7 1129–1142 Occurrence Handle10.1105/tpc.7.8.1129 Occurrence Handle1:CAS:528:DyaK2MXnvVWntbk%3D Occurrence Handle7549476

    Article  CAS  PubMed  Google Scholar 

  • S. Yamada T. Komori P.N. Myers S. Kuwata T. Kubo H. Imaschi (1997) ArticleTitleExpression of plasma membrane water channel genes under water stress in Nicotiana excelsior Plant Cell Physiol. 38 1226–1231 Occurrence Handle1:CAS:528:DyaK2sXnsFWqsb8%3D Occurrence Handle9435139

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Juan Manuel Ruiz-Lozano.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Porcel, R., Aroca, R., Azcón, R. et al. PIP Aquaporin Gene Expression in Arbuscular Mycorrhizal Glycine max and Lactuca  sativa Plants in Relation to Drought Stress Tolerance. Plant Mol Biol 60, 389–404 (2006). https://doi.org/10.1007/s11103-005-4210-y

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-005-4210-y

Key words

Navigation