Skip to main content
Log in

Fungal aquaporins: cellular functions and ecophysiological perspectives

  • Mini-Review
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Three aspects have to be taken into consideration when discussing cellular water and solute permeability of fungal cells: cell wall properties, membrane permeability, and transport through proteinaceous pores (the main focus of this review). Yet, characterized major intrinsic proteins (MIPs) can be grouped into three functional categories: (mainly) water transporting aquaporins, aquaglyceroporins that confer preferentially solute permeability (e.g., glycerol and ammonia), and bifunctional aquaglyceroporins that can facilitate efficient water and solute transfer. Two ancestor proteins, a water (orthodox aquaporin) and a solute facilitator (aquaglyceroporin), are supposed to give rise to today’s MIPs. Based on primary sequences of fungal MIPs, orthodox aquaporins/X-intrinsic proteins (XIPs) and FPS1-like/Yfl054-like/other aquaglyceroporins are supposed to be respective sister groups. However, at least within the fungal kingdom, no easy functional conclusion can be drawn from the phylogenetic position of a given protein within the MIP pedigree. In consequence, ecophysiological prediction of MIP relevance is not feasible without detailed functional analysis of the respective protein and expression studies. To illuminate the diverse MIP implications in fungal lifestyle, our current knowledge about protein function in two organisms, baker’s yeast and the Basidiomycotic Laccaria bicolor, an ectomycorrhizal model fungus, was exemplarily summarized in this review. MIP function has been investigated in such a depth in Saccharomyces cerevisiae that a system-wide view is possible. Yeast lifestyle, however, is special in many circumstances. Therefore, L. bicolor as filamentous Basidiomycete was added and allows insight into a very different way of life. Special emphasis was laid in this review onto ecophysiological interpretation of MIP function.

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.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Abascal F, Irisarri I, Zardoya R (2014) Diversity and evolution of membrane intrinsic proteins. Biochim Biophys Acta 1840(5):1468–1481

    PubMed  CAS  Google Scholar 

  • Abramson J, Vartanian AS (2013) Watch Water Flow. Science 340(6138):1294–1295

    PubMed  Google Scholar 

  • Agerer R (2001) Exploration types of ectomycorrhizae. Mycorrhiza 11(2):107–114

    Google Scholar 

  • Ahmadpour D, Geijer C, Tamás MJ, Lindkvist-Petersson K, Hohmann S (2014) Yeast reveals unexpected roles and regulatory features of aquaporins and aquaglyceroporins. Biochim Biophys Acta 1840(5):1482–1491

    PubMed  CAS  Google Scholar 

  • Al-Dagal M, Fung DY (1990) Aeromicrobiology-a review. Crit Rev Food Sci Nutr 29(5):333–40

    PubMed  CAS  Google Scholar 

  • Allen MF (2007) Mycorrhizal fungi: highways for water and nutrients in arid soils. Valdose Zone J 6(2):291–297

    Google Scholar 

  • Andreoli TE, Troutman SL (1971) An analysis of unstirred layers in series with “tight” and “porous” lipid bilayer membranes. J Gen Physiol 57(4):464–478

    PubMed  CAS  PubMed Central  Google Scholar 

  • Ashford AE, Peterson CA, Carpenter JL, Cairney JWG, Allaway WG (1988) Structure and permeability of the fungal sheath in the Pisonia mycorrhiza. Protoplasma 147(2–3):149–161

    Google Scholar 

  • Bago B, Pfeffer P, Shachar-Hill Y (2001) Could the urea cycle be translocating nitrogen in the arbuscular mycorrhizal symbiosis? New Phytol 149:4–8

  • Baltanás R, Bush A, Couto A, Durrieu L, Hohmann S, Colman-Lerner A (2013) Pheromone-induced morphogenesis improves osmoadaptation capacity by activating the HOG MAPK pathway, vol 6

  • Bauer H, Kasper-Giebl A, Löflund M, Giebl H, Hitzenberger R, Zibuschka F, Puxbaum H (2002) The contribution of bacteria and fungal spores to the organic carbon content of cloud water, precipitation and aerosols. Atmospher Res 64(1–4):109–119

    CAS  Google Scholar 

  • Beese SE, Negishi T, Levin DE (2009) Identification of positive regulators of the yeast Fps1 glycerol channel. PLoS Genet 5(11):e1000738

    PubMed  PubMed Central  Google Scholar 

  • Beese-Sims SE, Lee J, Levin DE (2011) Yeast Fps1 glycerol facilitator functions as a homotetramer. Yeast 28(12):815–819

    PubMed  CAS  PubMed Central  Google Scholar 

  • Beitz E, Wu B, Holm LM, Schultz JE, Zeuthen T (2006) Point mutations in the aromatic/arginine region in aquaporin 1 allow passage of urea, glycerol, ammonia, and protons. Proc Natl Acad Sci U S A 103(2):269–74

    PubMed  CAS  PubMed Central  Google Scholar 

  • Bienert G, Chaumont F (2011) Plant aquaporins: roles in water homeostasis, nutrition, and signaling processes. In: Geisler M, Venema K (eds) Transporters and pumps in plant signaling. Signaling and communication in plants, vol 7. Springer, Berlin, pp 3–36

    Google Scholar 

  • Birch E (2013) Aquaporins in Magnaporthe oryzae. University of, Oxford

    Google Scholar 

  • Bonhivers M, Carbrey JM, Gould SJ, Agre P (1998) Aquaporins in Saccharomyces: genetic and functional distinctions between laboratory and wild-type strains. J Biol Chem 273(42):27565–27572

    PubMed  CAS  Google Scholar 

  • Borgnia M, Nielsen S, Engel A, Agre P (1999) Cellular and molecular biology of the aquaporin water channels. Ann Rev Biochem 68(1):425–458

    PubMed  CAS  Google Scholar 

  • Boyle CD, Hellenbrand KE (1991) Assessment of the effect of mycorrhizal fungi on drought tolerance of conifer seedlings. Can J Bot 69:1764–1771

    Google Scholar 

  • Brown JK, Hovmoller MS (2002) Aerial dispersal of pathogens on the global and continental scales and its impact on plant disease. Science 297(5581):537–41

    PubMed  CAS  Google Scholar 

  • Brownlee C, Duddridge JA, Malibari A, Read DJ (1983) The structure and function of mycelial systems of ectomycorrhizal roots with special reference to their role in assimilate and water transport. Plant Soil 71:433–443

    Google Scholar 

  • Bücking H, Kuhn AJ, Schröder WH, Heyser W (2002) The fungal sheath of ectomycorrhizal pine roots: an apoplastic barrier for the entry of calcium, magnesium, and potassium into root cortex? J Exp Bot 53(374):1659–1669

    PubMed  Google Scholar 

  • Carbrey JM, Bonhivers M, Boeke JD, Agre P (2001a) Aquaporins in Saccharomyces: characterization of a second functional water channel protein. Proc Natl Acad Sci U S A 98(3):1000–1005

    PubMed  CAS  PubMed Central  Google Scholar 

  • Carbrey JM, Cormack BP, Agre P (2001b) Aquaporin in Candida: characterization of a functional water channel protein. Yeast 18(15):1391–6

    PubMed  CAS  Google Scholar 

  • Chalot M, Blaudez D, Brun A (2006) Ammonia: a candidate for nitrogen transfer at the mycorrhizal interface. Trends Plant Sci 11(6):263–266

    PubMed  CAS  Google Scholar 

  • Cheng CK, Au CH, Wilke S, Stajich J, Zolan M, Pukkila P, Kwan HS (2013) 5′-serial analysis of gene expression studies reveal a transcriptomic switch during fruiting body development in Coprinopsis cinerea. BMC Genomics 14(1):195

    PubMed  CAS  PubMed Central  Google Scholar 

  • Chrispeels MJ, Agre P (1994) Aquaporins: water channel proteins of plant and animal cells. Trends Biochem Sci 19(10):421–5

    PubMed  CAS  Google Scholar 

  • Chrispeels MJ, Maurel C (1994) Aquaporins: the molecular basis of facilitated water movement through living plant cells? Plant Physiol 105(1):9–13

    PubMed  CAS  PubMed Central  Google Scholar 

  • Chu S, DeRisi J, Eisen M, Mulholland J, Botstein D, Brown PO, Herskowitz I (1998) The transcriptional program of sporulation in budding yeast. Science 282(5389):699–705

    PubMed  CAS  Google Scholar 

  • Coury LA, Hiller M, Mathai JC, Jones EW, Zeidel ML, Brodsky JL (1999) Water transport across yeast vacuolar and plasma membrane-targeted secretory vesicles occurs by passive diffusion. J Bact 181(14):4437–4440

    PubMed  CAS  PubMed Central  Google Scholar 

  • Danielson JA, Johanson U (2008) Unexpected complexity of the aquaporin gene family in the moss Physcomitrella patens. BMC Plant Biol 8:45

    PubMed  PubMed Central  Google Scholar 

  • De La Providencia IE, De Souza FA, Fernández F, Delmas NS, Declerck S (2005) Arbuscular mycorrhizal fungi reveal distinct patterns of anastomosis formation and hyphal healing mechanisms between different phylogenic groups. New Phytol 165(1):261–271

    PubMed  Google Scholar 

  • Dietz S (2010) Countertrade in ectomycorrhiza symbiosis—aquaporins and sugarporters in the model fungus Laccaria bicoclor. University of Tuebingen

  • Dietz S, von Bülow J, Beitz E, Nehls U (2011) The aquaporin gene family of the ectomycorrhizal fungus Laccaria bicolor: lessons for symbiotic functions. New Phytol 190(4):927–940

    PubMed  CAS  Google Scholar 

  • Duddridge JA, Malibari A, Read DJ (1980) Structure and function of mycorrizal rhizomorphs with special reference to their role in water transport. Nature 287:834–836

    Google Scholar 

  • Dumont F, Marechal PA, Gervais P (2004) Cell size and water permeability as determining factors for cell viability after freezing at different cooling rates. Appl Environ Microbiol 70(1):268–272

    PubMed  CAS  PubMed Central  Google Scholar 

  • Dynowski M, Mayer M, Moran O, Ludewig U (2008) Molecular determinants of ammonia and urea conductance in plant aquaporin homologs. FEBS Lett 582(16):2458–2462

    PubMed  CAS  Google Scholar 

  • Eddy AA, Barnett JA (2007) A history of research on yeasts 11. The study of solute transport: the first 90 years, simple and facilitated diffusion (1). Yeast 24(12):1023–59

    PubMed  CAS  Google Scholar 

  • Egerton-Warburton LM, Querejeta JI, Allen MF (2008) Efflux of hydraulically lifted water from mycorrhizal fungal hyphae during imposed drought. Plant Signal Behav 3(1):68–71

    PubMed  PubMed Central  Google Scholar 

  • Ekundayo J (1966) Further studies on germination of sporangiospores of Rhizopus arrhizus. J Gen Microbiol 42(2):283–291

    PubMed  CAS  Google Scholar 

  • Engel A, Stahlberg H (2002) Aquaglyceroporins: channel proteins with a conserved core, multiple functions, and variable surfaces. In: Thomas Zeuthen WDS (ed) International review of cytology, vol 215. Academic Press, pp. 75–104

  • Eriksson UK, Fischer G, Friemann R, Enkavi G, Tajkhorshid E, Neutze R (2013) Subangstrom resolution X-ray structure details aquaporin-water interactions. Science 340(6138):1346–1349

    PubMed Central  Google Scholar 

  • Feofilova EP, Tereshina VM, Khokhlova NS, Memorskaya AS (2000) Different mechanisms of the biochemical adaptation of mycelial fungi to temperature stress: changes in the cytosol carbohydrate composition. Microbiol 69(5):504–508

    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 Online 16(1):215–228

    CAS  Google Scholar 

  • Fettiplace R, Haydon DA (1980) Water permeability of lipid membranes. Physiol Rev 60(2):510–50

    PubMed  CAS  Google Scholar 

  • Fettiplace R, Gordon LGM, Hladky SB, Requena J, Zingsheim HP, Haydon DA (1975) Techniques in the formation and examination of “black” lipid bilayer membranes. In: Korn E (ed) Biophysical Approaches. Springer, New York, US, pp 1–75

    Google Scholar 

  • Finkelstein A (1976) Water and nonelectrolyte permeability of lipid bilayer membranes. J Gen Physiol 68(2):127–135

    PubMed  CAS  Google Scholar 

  • Finkelstein A (1987) Water movement through lipid bilayers, pores, and plasma membranes. Theory and reality, vol 4. Wiley, New York

    Google Scholar 

  • Finlay RD, Frostegärd Ä, Sonnerfeldt A-M (1992) Utilisation of organic and inorganic nitrogen sources by ectomycorrhizal fungi in pure culture and in symbiosis with Pinus contorta Dougl. ex Loud. New Phytol 120:105–111

    Google Scholar 

  • Fischer G, Kosinska-Eriksson U, Aponte-Santamaría C, Palmgren M, Geijer C, Hedfalk K, Hohmann S, de Groot BL, Neutze R, Lindkvist-Petersson K (2009) Crystal structure of a yeast aquaporin at 1.15 Å reveals a novel gating mechanism. PLoS Biol 7(6):e1000130

    PubMed  PubMed Central  Google Scholar 

  • Fletcher J, Morton AG (1970) Physiology of germination of Penicillium griseofulvum conidia. Trans Br Mycol Soc 54(1):65–81

    CAS  Google Scholar 

  • Froger A, Thomas D, Delamarche C, Tallur B (1998) Prediction of functional residues in water channels and related proteins. Protein Sci 7(6):1458–1468

    PubMed  CAS  PubMed Central  Google Scholar 

  • Fujiyoshi Y, Mitsuoka K, de Groot BL, Philippsen A, Grubmüller H, Agre P, Engel A (2002) Structure and function of water channels. Curr Opin Struct Biol 12(4):509–515

    PubMed  CAS  Google Scholar 

  • Furukawa K, Sidoux-Walter F, Hohmann S (2009) Expression of the yeast aquaporin Aqy2 affects cell surface properties under the control of osmoregulatory and morphogenic signalling pathways. Mol Microbiol 74(5):1272–86

    PubMed  CAS  Google Scholar 

  • Gadgil RL, Gadgil PD (1971) Mycorrhiza and litter decomposition. Nature 233(5315):133

    PubMed  CAS  Google Scholar 

  • Gadgil RL, Gadgil PD (1975) Suppression of litter decomposition by mycorrhizal roots of Pinus radiata. N Z J For Sci 5:35–41

    Google Scholar 

  • Galagan JE, Calvo SE, Borkovich KA, Selker EU, Read ND, Jaffe D, FitzHugh W, Ma L-J, Smirnov S, Purcell S, Rehman B, Elkins T, Engels R, Wang S, Nielsen CB, Butler J, Endrizzi M, Qui D, Ianakiev P, Bell-Pedersen D, Nelson MA, Werner-Washburne M, Selitrennikoff CP, Kinsey JA, Braun EL, Zelter A, Schulte U, Kothe GO, Jedd G, Mewes W, Staben C, Marcotte E, Greenberg D, Roy A, Foley K, Naylor J, Stange-Thomann N, Barrett R, Gnerre S, Kamal M, Kamvysselis M, Mauceli E, Bielke C, Rudd S, Frishman D, Krystofova S, Rasmussen C, Metzenberg RL, Perkins DD, Kroken S, Cogoni C, Macino G, Catcheside D, Li W, Pratt RJ, Osmani SA, DeSouza CPC, Glass L, Orbach MJ, Berglund JA, Voelker R, Yarden O, Plamann M, Seiler S, Dunlap J, Radford A, Aramayo R, Natvig DO, Alex LA, Mannhaupt G, Ebbole DJ, Freitag M, Paulsen I, Sachs MS, Lander ES, Nusbaum C, Birren B (2003) The genome sequence of the filamentous fungus Neurospora crassa. Nature 422(6934):859–868

    PubMed  CAS  Google Scholar 

  • Geijer C, Ahmadpour D, Palmgren M, Filipsson C, Klein DM, Tamás MJ, Hohmann S, Lindkvist-Petersson K (2012) Yeast aquaglyceroporins use the transmembrane core to restrict glycerol transport. J Biol Chem 287(28):23562–23570

    PubMed  CAS  PubMed Central  Google Scholar 

  • Gena P, Pellegrini-Calace M, Biasco A, Svelto M, Calamita G (2011) Aquaporin membrane channels: biophysics, classification, functions, and possible biotechnological applications. Food Biophys 6(2):241–249

    Google Scholar 

  • Ghosh K, Cappiello CD, McBride SM, Occi JL, Cali A, Takvorian PM, McDonald TV, Weiss LM (2006) Functional characterization of a putative aquaporin from Encephalitozoon cuniculi, a microsporidia pathogenic to humans. Int J Parasit 36(1):57–62

    CAS  Google Scholar 

  • Glass NL, Rasmussen C, Roca MG, Read ND (2004) Hyphal homing, fusion and mycelial interconnectedness. Trends Microbiol 12(3):135–141

    PubMed  CAS  Google Scholar 

  • Gupta AB, Sankararamakrishnan R (2009) Genome-wide analysis of major intrinsic proteins in the tree plant Populus trichocarpa: characterization of XIP subfamily of aquaporins from evolutionary perspective. BMC Plant Biol 9:134

    PubMed  PubMed Central  Google Scholar 

  • Hacquard S, Tisserant E, Brun A, Legué V, Martin F, Kohler A (2013) Laser microdissection and microarray analysis of Tuber melanosporum ectomycorrhizas reveal functional heterogeneity between mantle and Hartig net compartments. Environ Microbiol 15(6):1853–1869

    PubMed  CAS  Google Scholar 

  • Hansen M, Kun JFJ, Schultz JE, Beitz E (2002) A bingle, bi-functional aquaglyceroporin in blood-stage Plasmodium falciparum malaria parasites. J Biol Chem 277(7):4874–4882

    PubMed  CAS  Google Scholar 

  • Harvengt P, Vlerick A, Fuks B, Wattiez R, Ruysschaert JM, Homble F (2000) Lentil seed aquaporins form a hetero-oligomer which is phosphorylated by a Mg2+-dependent and Ca2+-regulated kinase. Biochem J 352:183–90

    PubMed  CAS  PubMed Central  Google Scholar 

  • Heaton L, Obara B, Grau V, Jones N, Nakagaki T, Boddy L, Fricker MD (2012) Analysis of fungal networks. Fung Biol Rev 26(1):12–29

    Google Scholar 

  • Heller KB, Lin EC, Wilson TH (1980) Substrate specificity and transport properties of the glycerol facilitator of Escherichia coli. J Bact 144(1):274–278

    PubMed  CAS  PubMed Central  Google Scholar 

  • Henzler T, Steudle E (2000) Transport and metabolic degradation of hydrogen peroxide in Chara corallina: model calculations and measurements with the pressure probe suggest transport of H2O2 across water channels. J Exp Bot 51(353):2053–66

    PubMed  CAS  Google Scholar 

  • Hill AE, Shachar-Hill B, Shachar-Hill Y (2004) What are aquaporins for? J Membr Biol 197(1):1–32

    PubMed  CAS  Google Scholar 

  • Hobbie EA, Olszyk DM, Rygiewicz PT, Tingey DT, Johnson MG (2001) Foliar nitrogen concentrations and natural abundance of (15)N suggest nitrogen allocation patterns of Douglas-fir and mycorrhizal fungi during development in elevated carbon dioxide concentration and temperature. Tree Physiol 21(15):1113–22

  • Hohmann S, Krantz M, Nordlander B (2007) Yeast osmoregulation. In: Dieter H, Helmut S (eds) Methods enzymol, vol 428. Academic Press, pp. 29–45

  • Hooijmaijers C, Rhee JY, Kwak KJ, Chung GC, Horie T, Katsuhara M, Kang H (2012) Hydrogen peroxide permeability of plasma membrane aquaporins of Arabidopsis thaliana. J Plant Res 125(1):147–153

    PubMed  CAS  Google Scholar 

  • Howard RJ, Ferrari MA (1989) Role of melanin in appressorium function. Exp Mycol 13(4):403–418

    CAS  Google Scholar 

  • Hüsken D, Steudle E, Zimmermann U (1978) Pressure probe technique for measuring water relations of cells in higher plants. Plant Physiol 61(2):158–163

    PubMed  PubMed Central  Google Scholar 

  • Ishibashi K (2006) Aquaporin subfamily with unusual NPA boxes. BBA 1758(8):989–993

    PubMed  CAS  Google Scholar 

  • Jakobsen I (2004) Hyphal fusion to plant species connections—giant mycelia and community nutrient flow. New Phytol 164(1):4–7

    Google Scholar 

  • Jung JS, Preston GM, Smith BL, W.B. G, Agre P (1994) Molecular structure of the water channel through aquaporin CHIP. The hourglass model. J Biol Chem 269(20):14648–14654

    PubMed  CAS  Google Scholar 

  • Kleinhans FW (1998) Membrane permeability modeling: Kedem–Katchalsky vs a two-parameter formalism. Cryobiology 37(4):271–289

    PubMed  CAS  Google Scholar 

  • Koide RT, Wu T (2003) Ectomycorrhizas and retarded decomposition in a Pinus resinosa plantation. New Phytol 158:401–407

    Google Scholar 

  • Kosinska-Eriksson U, Fischer G, Friemann R, Enkavi G, Tajkhorshid E, Neutze R (2013) Subangström resolution X-ray structure details aquaporin-water interactions. Science 340(6138):1346–1349

    PubMed  CAS  Google Scholar 

  • Kottke I, Oberwinkler F (1986) Mycorrhiza of forest trees—structure and function. Trees 1:1–24

    Google Scholar 

  • Krane CM, Goldstein DL (2007) Comparative functional analysis of aquaporins/glyceroporins in mammals and anurans. Mamm Genome 18(6–7):452–462

    PubMed  CAS  PubMed Central  Google Scholar 

  • Krylov AV, Pohl P, Zeidel ML, Hill WG (2001) Water permeability of asymmetric planar lipid bilayers: leaflets of different composition offer independent and additive resistances to permeation. J Gen Physiol 118(4):333–340

    PubMed  CAS  PubMed Central  Google Scholar 

  • Kües U, Liu Y (2000) Fruiting body production in basidiomycetes. Appl Microbiol Biotech 54(2):141–152

    Google Scholar 

  • Lande MB, Donovan JM, Zeidel ML (1995) The relationship between membrane fluidity and permeabilities to water, solutes, ammonia, and protons. J Gen Physiol 106(1):67–84

    PubMed  CAS  Google Scholar 

  • Landhäusser SM, Muhsin TM, Zwiazek J (2002) The effect of ectomycorrhizae on water relations in aspen (Populus tremuloides) and white spruce (Picea glauca) at low soil temperatures. Can J Bot 80(6):684–689

    Google Scholar 

  • Lee J, Reiter W, Dohnal I, Gregori C, Beese-Sims S, Kuchler K, Ammerer G, Levin DE (2013) MAPK Hog1 closes the S. cerevisiae glycerol channel Fps1 by phosphorylating and displacing its positive regulators. Genes Dev 27(23):2590–2601

    PubMed  CAS  PubMed Central  Google Scholar 

  • Lehto T, Zwiazek JJ (2011) Ectomycorrhizas and water relations of trees: a review. Mycorrhiza 21(2):71–90

    PubMed  Google Scholar 

  • Li T, Hu Y-J, Hao Z-P, Li H, Wang Y-S, Chen B-D (2013) First cloning and characterization of two functional aquaporin genes from an arbuscular mycorrhizal fungus Glomus intraradices. New Phytol 197(2):617–630

    PubMed  CAS  Google Scholar 

  • Lindahl BD, Ihrmark K, Boberg J, Trumbore SE, Högberg P, Stenlid J, Finlay RD (2007) Spatial separation of litter decomposition and mycorrhizal nitrogen uptake in a boreal forest. New Phytol 173(3):611–620

    PubMed  CAS  Google Scholar 

  • Linder MB, Szilvay GR, Nakari-Setälä T, Penttilä ME (2005) Hydrophobins: the protein-amphiphiles of filamentous fungi. FEMS Microbiol Rev 29(5):877–896

    PubMed  CAS  Google Scholar 

  • Loewe A, Einig W, Shi L, Dizengremel P, Hampp R (2000) Mycorrhiza formation and elevated CO2 both increase the capacity for sucrose synthesis in source leaves of spruce and aspen. New Phytol 145(3):565–574

    CAS  Google Scholar 

  • Lopez D, Bronner G, Brunel N, Auguin D, Bourgerie S, Brignolas F, Carpin S, Tournaire-Roux C, Maurel C, Fumanal B, Martin F, Sakr S, Label P, Julien JL, Gousset-Dupont A, Venisse JS (2012) Insights into Populus XIP aquaporins: evolutionary expansion, protein functionality, and environmental regulation. J Exp Bot 63(5):2217–2230

    PubMed  CAS  Google Scholar 

  • Lucic E, Fourrey C, Kohler A, Martin F, Chalot M, Brun-Jacob A (2008) A gene repertoire for nitrogen transporters in Laccaria bicolor. New Phytol 180(2):343–364

    PubMed  CAS  Google Scholar 

  • Ludewig U, Dynowski M (2009) Plant aquaporin selectivity: where transport assays, computer simulations and physiology meet. Cell Mol Life Sci 66(19):3161–3175

    PubMed  CAS  Google Scholar 

  • Luu D-T, Maurel C (2005) Aquaporins in a challenging environment: molecular gears for adjusting plant water status. Plant Cell Environ 28(1):85–96

    CAS  Google Scholar 

  • Luyten K, Albertyn J, Skibbe WF, Prior B, Ramos J, Thevelein J, Hohmann S (1995) Fps1, a yeast member of the MIP family of channel proteins, is a facilitator for glycerol uptake and efflux and is inactive under osmotic stress. EMBO J 14(7):1360

    PubMed  CAS  PubMed Central  Google Scholar 

  • Macey RL, Farmer REL (1970) Inhibition of water and solute permeability in human red cells. BBA 211(1):104–106

    PubMed  CAS  Google Scholar 

  • Macey R, Karan D, Farmer RL (1972) Properties of water channels in human red cells. In: Kreuzer F, Slegers JFG (eds) Biomembranes: passive permeability of cell membranes. Biomembranes, vol 3. Springer, New York, US, pp 331–340

    Google Scholar 

  • Marchant R, White MF (1967) The carbon metabolism and swelling of Fusarium culmorum conidia. J Gen Microbiol 48(1):65–77

    CAS  Google Scholar 

  • Marjanovic Z, Nehls U, Hampp R (2005a) Mycorrhiza formation enhances adaptive response of hybrid poplar to drought. Ann NY Acad Sci 1048:496–499

    PubMed  CAS  Google Scholar 

  • Marjanovic Z, Uehlein N, Kaldenhoff R, Zwiazek JJ, Weiss M, Hampp R, Nehls U (2005b) Aquaporins in poplar: what a difference a symbiont makes! Planta 222:258–268

    PubMed  CAS  Google Scholar 

  • Maurel C, Reizer J, Schroeder JI, Chrispeels MJ, Saier MH (1994) Functional characterization of the Escherichia coli glycerol facilitator, GlpF, in Xenopus oocytes. J Biol Chem 269:11869–11872

    PubMed  CAS  Google Scholar 

  • Melin E, Nilsson H (1952) Transport of labelled nitrogen from an ammonium source to pine seedlings through mycorrhizal mycelium. Svensk Bot Tidskr 46:281–285

    CAS  Google Scholar 

  • Mexal J, Reid CPP (1973) The growth of selected mycorrhizal fungi in response to induced water stress. Can J Bot 51:1579–1588

    Google Scholar 

  • Meyrial V, Laize V, Gobin R, Ripoche P, Hohmann S, Tacnet F (2001) Existence of a tightly regulated water channel in Saccharomyces cerevisiae. Eur J Biochem 268(2):334–343

    PubMed  CAS  Google Scholar 

  • Mitani-Ueno N, Yamaji N, Zhao F-J, Ma JF (2011) The aromatic/arginine selectivity filter of NIP aquaporins plays a critical role in substrate selectivity for silicon, boron, and arsenic. J Exp Bot 62(12):4391–4398

    PubMed  CAS  PubMed Central  Google Scholar 

  • Mollapour M, Piper PW (2007) Hog1 mitogen-activated protein kinase phosphorylation targets the yeast Fps1 aquaglyceroporin for endocytosis, thereby rendering cells resistant to acetic acid. Mol Cell Biol 27(18):6446–6456

    PubMed  CAS  PubMed Central  Google Scholar 

  • Muhsin TM, Zwiazek JJ (2002a) Ectomycorrhizae increase water conductance and protect white spruce (Picea glauca) seedlings against salt stress. Plant Soil 238:217–225

    CAS  Google Scholar 

  • Muhsin TM, Zwiazek JJ (2002b) Ectomycorrhizas increase apoplastic water transport and root hydraulic conductivity in Ulmus americana seedlings. New Phytol 153:153–158

    Google Scholar 

  • Navarro-Ródenas A, Ruíz-Lozano JM, Kaldenhoff R, Morte A (2011) The aquaporin TcAQP1 of the desert truffle Terfezia claveryi is a membrane pore for water and CO2 transport. Molec Plant Micobe Interact 25(2):259–266

    Google Scholar 

  • Nehls U (2008) Mastering ectomycorrhizal symbiosis: the impact of carbohydrates. J Exp Bot 59(5):1097–1108

    PubMed  CAS  Google Scholar 

  • Neves L, Oliveira R, Lucas C (2004) Yeast orthologues associated with glycerol transport and metabolism. FEMS Yeast Res 5(1):51–62

    PubMed  CAS  Google Scholar 

  • Oliva R, Calamita G, Thornton JM, Pellegrini-Calace M (2010) Electrostatics of aquaporin and aquaglyceroporin channels correlates with their transport selectivity. Proc Natl Acad Sci 107(9):4135–4140

    PubMed  CAS  PubMed Central  Google Scholar 

  • Oliveira R, Lages F, Silva-Graça M, Lucas C (2003) Fps1p channel is the mediator of the major part of glycerol passive diffusion in Saccharomyces cerevisiae: artefacts and re-definitions. BBA 1613(1–2):57–71

    PubMed  CAS  Google Scholar 

  • Otto B, Uehlein N, Sdorra S, Fischer M, Ayaz M, Belastegui-Macadam X, Heckwolf M, Lachnit M, Pede N, Priem N, Reinhard A, Siegfart S, Urban M, Kaldenhoff R (2010) Aquaporin tetramer composition modifies the function of tobacco aquaporins. J Biol Chem 285(41):31253–31260

    PubMed  CAS  PubMed Central  Google Scholar 

  • Pareek M, Cole L, Ashford AE (2001) Variations in structure of aerial and submerged rhizomorphs of Armillaria luteobubalina indicate that they may be organs of absorption. Mycol Res 105(11):1377–1387

    Google Scholar 

  • Payyavula RS, Tay KHC, Tsai C-J, Harding SA (2011) The sucrose transporter family in Populus: the importance of a tonoplast PtaSUT4 to biomass and carbon partitioning. Plant J 65(5):757–770

    PubMed  CAS  Google Scholar 

  • Perez Di Giorgio J, Soto G, Alleva K, Jozefkowicz C, Amodeo MJP, Ayub ND (2014) Prediction of aquaporin function by integrating evolutionary and functional analyses. J Membr Biol 247(2):107–125

    PubMed  CAS  Google Scholar 

  • Pettersson N, Filipsson C, Becit E, Brive L, Hohmann S (2005) Aquaporins in yeasts and filamentous fungi. Biol Cell 97:487–500

    PubMed  CAS  Google Scholar 

  • Philips J, Herskowitz I (1997) Osmotic balance regulates cell fusion during mating in Saccharomyces cerevisiae. J Cell Biol 138(5):961–974

    PubMed  CAS  PubMed Central  Google Scholar 

  • Querejeta JI, Egerton-Warburton LM, Allen MF (2003) Direct nocturnal water transfer from oaks to their mycorrhizal symbionts during severe soil drying. Oecologia 134(1):55–64

    PubMed  Google Scholar 

  • Ramahaleo T, Morillon R, Alexandre J, Lassalles JP (1999) Osmotic water permeability of isolated protoplasts. Modifications during development. Plant Physiol 119(3):885–96

    PubMed  CAS  PubMed Central  Google Scholar 

  • Redwood WR, Haydon DA (1969) Influence of temperature and membrane composition on the water permeability of lipid bilayers. J Theoret Biol 22(1):1–8

    CAS  Google Scholar 

  • Reizer J, Reizer A, Saier MH (1993) The MIP family of integral membrane channel proteins: squence comparisons, evolutionary relationships, reconstructed pathway of evolution, and proposed functional differentiation of the two repeated halves of the proteins. CRC Crit Rev Biochem Molec Biol 28(3):235–257

    CAS  Google Scholar 

  • Rhind N, Chen Z, Yassour M, Thompson DA, Haas BJ, Habib N, Wapinski I, Roy S, Lin MF, Heiman DI, Young SK, Furuya K, Guo Y, Pidoux A, Chen HM, Robbertse B, Goldberg JM, Aoki K, Bayne EH, Berlin AM, Desjardins CA, Dobbs E, Dukaj L, Fan L, FitzGerald MG, French C, Gujja S, Hansen K, Keifenheim D, Levin JZ, Mosher RA, Müller CA, Pfiffner J, Priest M, Russ C, Smialowska A, Swoboda P, Sykes SM, Vaughn M, Vengrova S, Yoder R, Zeng Q, Allshire R, Baulcombe D, Birren BW, Brown W, Ekwall K, Kellis M, Leatherwood J, Levin H, Margalit H, Martienssen R, Nieduszynski CA, Spatafora JW, Friedman N, Dalgaard JZ, Baumann P, Niki H, Regev A, Nusbaum C (2011) Comparative functional genomics of the fission yeasts. Science 332(6032):930–936

    PubMed  CAS  PubMed Central  Google Scholar 

  • Richards JH, Caldwell MM (1987) Hydraulic lift: substantial nocturnal water transport between soil layers by Artemisia tridentata roots. Oecologia 73(4):486–489

    Google Scholar 

  • Robinson CH (2001) Cold adaptation in Arctic and Antarctic fungi. New Phytol 151(2):341–353

    CAS  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

  • Savage DF, Egea PF, Robles-Colmenares Y, O’Connell JD 3rd, Stroud RM (2003) Architecture and selectivity in aquaporins: 2.5 Å X-ray structure of aquaporin Z. PLoS Biol 1(3):E72

    PubMed  PubMed Central  Google Scholar 

  • Schnurbusch T, Hayes J, Hrmova M, Baumann U, Ramesh SA, Tyerman SD, Langridge P, Sutton T (2010) Boron toxicity tolerance in barley through reduced expression of the multifunctional aquaporin HvNIP2;1. Plant Physiol 153(4):1706–1715

    PubMed  CAS  PubMed Central  Google Scholar 

  • Selle A, Willmann M, Grunze N, Geßler A, Weiß M, Nehls U (2005) The high-affinity poplar ammonium importer PttAMT1.2 and its role in ectomycorrhizal symbiosis. New Phytol 168:697–706

    PubMed  CAS  Google Scholar 

  • Sidoux-Walter F, Pettersson N, Hohmann S (2004) The Saccharomyces cerevisiae aquaporin Aqy1 is involved in sporulation. Proc Natl Acad Sci U S A 101(50):17422–17427

    PubMed  CAS  PubMed Central  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic, London

    Google Scholar 

  • Sousa-Lopes A, Antunes F, Cyrne L, Marinho HS (2004) Decreased cellular permeability to H2O2 protects Saccharomyces cerevisiae cells in stationary phase against oxidative stress. FEBS Lett 578(1–2):152–156

    PubMed  CAS  Google Scholar 

  • Soveral G, Veiga A, Loureiro-Dias MC, Tanghe A, Van Dijck P, Moura TF (2006) Water channels are important for osmotic adjustments of yeast cells at low temperature. Microbiol 152(5):1515–1521

    CAS  Google Scholar 

  • Soveral G, Madeira A, Loureiro-Dias MC, Moura TF (2008) Membrane tension regulates water transport in yeast. BBA 1778(11):2573–2579

    PubMed  CAS  Google Scholar 

  • Soveral G, Prista C, Moura TF, Loureiro-Dias MC (2011) Yeast water channels: an overview of orthodox aquaporins. Biol Cell 103(1):35–54

    CAS  Google Scholar 

  • Steudle E (1989) Water flow in plants and its coupling to other processes: an overview. Methods Enzymol 174:183–225

    CAS  Google Scholar 

  • Steudle E (1994) Water transport across roots. Plant Soil 167:79–90

    CAS  Google Scholar 

  • Straatsma G, Sonnenberg AS, Van Griensven LJ (2013) Development and growth of fruit bodies and crops of the button mushroom, Agaricus bisporus. Fungal Biology 117(10):697–707

    PubMed  Google Scholar 

  • Sussman AS, Halvorson HO (1966) Spores: their dormancy and germination. Harper and Row, New York

    Google Scholar 

  • Tajkhorshid E, Nollert P, Jensen MO, Miercke LJ, O’Connell J, Stroud RM, Schulten K (2002) Control of the selectivity of the aquaporin water channel family by global orientational tuning. Science 296(5567):525–30

    PubMed  CAS  Google Scholar 

  • Tamás MJ, Luyten K, Sutherland FCW, Hernandez A, Albertyn J, Valadi H, Li H, Prior BA, Kilian SG, Ramos J, Gustafsson L, Thevelein JM, Hohmann S (1999) Fps1p controls the accumulation and release of the compatible solute glycerol in yeast osmoregulation. Molec Microbiol 31(4):1087–1104

    Google Scholar 

  • Tanghe A, Van Dijck P, Dumortier F, Teunissen A, Hohmann S, Thevelein JM (2002) Aquaporin expression correlates with freeze tolerance in Baker’s yeast, and overexpression improves freeze tolerance in industrial strains. Appl Environ Microbiol 68(12):5981–5989

    PubMed  CAS  PubMed Central  Google Scholar 

  • Tanghe A, Van Dijck P, Thevelein JM (2003) Determinants of freeze tolerance in microorganisms, physiological importance, and biotechnological applications. Adv Appl Microbiol 53:129–76

    PubMed  CAS  Google Scholar 

  • Tanghe A, Carbrey JM, Agre P, Thevelein JM, Van Dijck P (2005a) Aquaporin expression and freeze tolerance in Candida albicans. Appl Environ Microbiol 71(10):6434–7

    PubMed  CAS  PubMed Central  Google Scholar 

  • Tanghe A, Kayingo G, Prior BA, Thevelein JM, Van Dijck P (2005b) Heterologous aquaporin (AQY2-1) expression strongly enhances freeze tolerance of Schizosaccharomyces pombe. J Mol Microbiol Biotechnol 9(1):52–6

    PubMed  CAS  Google Scholar 

  • Tanghe A, Van Dijck P, Thevelein JM (2006) Why do microorganisms have aquaporins? Trends Microbiol 14(2):78–85

    PubMed  Google Scholar 

  • Theodorou C (1978) Soil moisture and the mycorrhizal association of Pinus radiata. Soil Biol Biochem 10:33–37

    CAS  Google Scholar 

  • Theodorou C, Bowen GD (1970) Mycorrhizal responses of radiata pine in experiments with different fungi. Austr Forestr Res 34:182–191

    Google Scholar 

  • Thines E, Weber RWS, Talbot NJ (2000) MAP kinase and protein kinase A-dependent mobilization of triacylglycerol and glycogen during appressorium turgor generation by Magnaporthe grisea. Plant Cell Online 12(9):1703–1718

    CAS  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl Acids Res 22:4673–4680

  • Tibbett M, Cairney JWG (2007) The cooler side of mycorrhizas: their occurrence and functioning at low temperatures. Can J Bot 85:51–62

    Google Scholar 

  • Tibbett M, Sanders F, Cairney J (2002) Low-temperature-induced changes in trehalose, mannitol and arabitol associated with enhanced tolerance to freezing in ectomycorrhizal basidiomycetes (Hebeloma spp.). Mycorrhiza 12(5):249–255

    PubMed  CAS  Google Scholar 

  • Uhlig SK (1972) Investigations on the drought resistance of mycorrhiza-forming fungi. Zentralblatt für Bakteriologie, Parasitenkunde, Infectionskrankheiten und Hygiene 127(2):124–33

    CAS  Google Scholar 

  • Unestam T (1991) Water repellency, mat formation, and leaf-stimulated growth of some ectomycorrhizal fungi. Mycorrhiza 1(1):13–20

    Google Scholar 

  • Unestam T, Sun Y-P (1995) Extramatrical structures of hydrophobic and hydrophilic ectomycorrhizal fungi. Mycorrhiza 5(5):301–311

    Google Scholar 

  • Vesk PA, Ashford AE, Markovina AL, Allaway WG (2000) Apoplasmic barriers and their significance in the exodermis and sheath of Eucalyptus pilularisPisolithus tinctorius ectomycorrhizas. New Phytol 145(2):333–346

    Google Scholar 

  • Wang Y, Schulten K, Tajkhorshid E (2005) What makes an aquaporin a glycerol channel? A comparative study of AqpZ and GlpF. Structure 13(8):1107–1118

    PubMed  CAS  Google Scholar 

  • Wang M, Gu B, Huang J, Jiang S, Chen Y, Yin Y, Pan Y, Yu G, Li Y, Wong BHC, Liang Y, Sun H (2013) Transcriptome and proteome exploration to provide a resource for the study of Agrocybe aegerita. PLoS One 8(2):e56686

    PubMed  CAS  PubMed Central  Google Scholar 

  • Wessels JGH (1997) Hydrophobins: proteins that change the nature of the fungal surface. Adv Microb Physiol 38:1–45

    PubMed  CAS  Google Scholar 

  • Will JL, Kim HS, Clarke J, Painter JC, Fay JC, Gasch AP (2010) Incipient balancing selection through adaptive loss of aquaporins in natural Saccharomyces cerevisiae populations. PLoS Genet 6(4):e1000893

    PubMed  PubMed Central  Google Scholar 

  • Willmann A, Thomfohrde S, Haensch R, Nehls U (2014) The poplar NRT2 gene family of high affinity nitrate importers: impact of nitrogen nutrition and ectomycorrhiza formation. Environmental and Experimental Botany(0)

  • Wösten HAB, Willey JM (2000) Surface-active proteins enable microbial aerial hyphae to grow into the air. Microbiol 146(4):767–773

    Google Scholar 

  • Wösten HAB, Richter M, Willey JM (1999) Structural proteins involved in emergence of microbial aerial hyphae. Fungal Genet Biol 27(2–3):153–160

    PubMed  Google Scholar 

  • Wysocki R, Chéry CC, Wawrzycka D, Van Hulle M, Cornelis R, Thevelein JM, Tamás MJ (2001) The glycerol channel Fps1p mediates the uptake of arsenite and antimonite in Saccharomyces cerevisiae. Molec Microbiol 40(6):1391–1401

    CAS  Google Scholar 

  • Xu H, Cooke JEK, Zwiazek JJ (2013) Phylogenetic analysis of fungal aquaporins provides insight into their possible role in water transport of mycorrhizal associations. Botany 91(8):495–504

    CAS  Google Scholar 

  • Young N, Ashford AE (1995) Apoplastic permeability of sclerotia of Sclerotium rolfsii, Sclerotium cepivorum and Rhizoctonia solani. New Phytol 131(1):33–40

    Google Scholar 

  • Zeidel ML, Ambudkar SV, Smith BL, Agre P (1992) Reconstitution of functional water channels in liposomes containing purified red cell CHIP28 protein. Biochem 31(33):7436–40

    CAS  Google Scholar 

  • Zhang Y, Lamm R, Pillonel C, Lam S, Xu J-R (2002) Osmoregulation and fungicide resistance: the Neurospora crassa os-2 gene encodes a HOG1 mitogen-activated protein kinase homologue. Appl Environ Microbiol 68(2):532–538

    PubMed  CAS  PubMed Central  Google Scholar 

  • Zhao F-J, Ago Y, Mitani N, Li R-Y, Su Y-H, Yamaji N, McGrath SP, Ma JF (2010) The role of the rice aquaporin Lsi1 in arsenite efflux from roots. New Phytol 186(2):392–399

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We are indebted to the anonymous reviewers for their helpful suggestions and Arpita Das for critical reading of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Uwe Nehls.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nehls, U., Dietz, S. Fungal aquaporins: cellular functions and ecophysiological perspectives. Appl Microbiol Biotechnol 98, 8835–8851 (2014). https://doi.org/10.1007/s00253-014-6049-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-014-6049-0

Keywords

Navigation