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.
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
Abramson J, Vartanian AS (2013) Watch Water Flow. Science 340(6138):1294–1295
Agerer R (2001) Exploration types of ectomycorrhizae. Mycorrhiza 11(2):107–114
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
Al-Dagal M, Fung DY (1990) Aeromicrobiology-a review. Crit Rev Food Sci Nutr 29(5):333–40
Allen MF (2007) Mycorrhizal fungi: highways for water and nutrients in arid soils. Valdose Zone J 6(2):291–297
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
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
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
Beese SE, Negishi T, Levin DE (2009) Identification of positive regulators of the yeast Fps1 glycerol channel. PLoS Genet 5(11):e1000738
Beese-Sims SE, Lee J, Levin DE (2011) Yeast Fps1 glycerol facilitator functions as a homotetramer. Yeast 28(12):815–819
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
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
Birch E (2013) Aquaporins in Magnaporthe oryzae. University of, Oxford
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
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
Boyle CD, Hellenbrand KE (1991) Assessment of the effect of mycorrhizal fungi on drought tolerance of conifer seedlings. Can J Bot 69:1764–1771
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
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
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
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
Carbrey JM, Cormack BP, Agre P (2001b) Aquaporin in Candida: characterization of a functional water channel protein. Yeast 18(15):1391–6
Chalot M, Blaudez D, Brun A (2006) Ammonia: a candidate for nitrogen transfer at the mycorrhizal interface. Trends Plant Sci 11(6):263–266
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
Chrispeels MJ, Agre P (1994) Aquaporins: water channel proteins of plant and animal cells. Trends Biochem Sci 19(10):421–5
Chrispeels MJ, Maurel C (1994) Aquaporins: the molecular basis of facilitated water movement through living plant cells? Plant Physiol 105(1):9–13
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
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
Danielson JA, Johanson U (2008) Unexpected complexity of the aquaporin gene family in the moss Physcomitrella patens. BMC Plant Biol 8:45
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
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
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
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
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
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
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
Ekundayo J (1966) Further studies on germination of sporangiospores of Rhizopus arrhizus. J Gen Microbiol 42(2):283–291
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
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
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
Fettiplace R, Haydon DA (1980) Water permeability of lipid membranes. Physiol Rev 60(2):510–50
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
Finkelstein A (1976) Water and nonelectrolyte permeability of lipid bilayer membranes. J Gen Physiol 68(2):127–135
Finkelstein A (1987) Water movement through lipid bilayers, pores, and plasma membranes. Theory and reality, vol 4. Wiley, New York
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
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
Fletcher J, Morton AG (1970) Physiology of germination of Penicillium griseofulvum conidia. Trans Br Mycol Soc 54(1):65–81
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
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
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
Gadgil RL, Gadgil PD (1971) Mycorrhiza and litter decomposition. Nature 233(5315):133
Gadgil RL, Gadgil PD (1975) Suppression of litter decomposition by mycorrhizal roots of Pinus radiata. N Z J For Sci 5:35–41
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
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
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
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
Glass NL, Rasmussen C, Roca MG, Read ND (2004) Hyphal homing, fusion and mycelial interconnectedness. Trends Microbiol 12(3):135–141
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
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
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
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
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
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
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
Hill AE, Shachar-Hill B, Shachar-Hill Y (2004) What are aquaporins for? J Membr Biol 197(1):1–32
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
Howard RJ, Ferrari MA (1989) Role of melanin in appressorium function. Exp Mycol 13(4):403–418
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
Ishibashi K (2006) Aquaporin subfamily with unusual NPA boxes. BBA 1758(8):989–993
Jakobsen I (2004) Hyphal fusion to plant species connections—giant mycelia and community nutrient flow. New Phytol 164(1):4–7
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
Kleinhans FW (1998) Membrane permeability modeling: Kedem–Katchalsky vs a two-parameter formalism. Cryobiology 37(4):271–289
Koide RT, Wu T (2003) Ectomycorrhizas and retarded decomposition in a Pinus resinosa plantation. New Phytol 158:401–407
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
Kottke I, Oberwinkler F (1986) Mycorrhiza of forest trees—structure and function. Trees 1:1–24
Krane CM, Goldstein DL (2007) Comparative functional analysis of aquaporins/glyceroporins in mammals and anurans. Mamm Genome 18(6–7):452–462
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
Kües U, Liu Y (2000) Fruiting body production in basidiomycetes. Appl Microbiol Biotech 54(2):141–152
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
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
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
Lehto T, Zwiazek JJ (2011) Ectomycorrhizas and water relations of trees: a review. Mycorrhiza 21(2):71–90
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
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
Linder MB, Szilvay GR, Nakari-Setälä T, Penttilä ME (2005) Hydrophobins: the protein-amphiphiles of filamentous fungi. FEMS Microbiol Rev 29(5):877–896
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
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
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
Ludewig U, Dynowski M (2009) Plant aquaporin selectivity: where transport assays, computer simulations and physiology meet. Cell Mol Life Sci 66(19):3161–3175
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
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
Macey RL, Farmer REL (1970) Inhibition of water and solute permeability in human red cells. BBA 211(1):104–106
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
Marchant R, White MF (1967) The carbon metabolism and swelling of Fusarium culmorum conidia. J Gen Microbiol 48(1):65–77
Marjanovic Z, Nehls U, Hampp R (2005a) Mycorrhiza formation enhances adaptive response of hybrid poplar to drought. Ann NY Acad Sci 1048:496–499
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
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
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
Mexal J, Reid CPP (1973) The growth of selected mycorrhizal fungi in response to induced water stress. Can J Bot 51:1579–1588
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
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
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
Muhsin TM, Zwiazek JJ (2002a) Ectomycorrhizae increase water conductance and protect white spruce (Picea glauca) seedlings against salt stress. Plant Soil 238:217–225
Muhsin TM, Zwiazek JJ (2002b) Ectomycorrhizas increase apoplastic water transport and root hydraulic conductivity in Ulmus americana seedlings. New Phytol 153:153–158
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
Nehls U (2008) Mastering ectomycorrhizal symbiosis: the impact of carbohydrates. J Exp Bot 59(5):1097–1108
Neves L, Oliveira R, Lucas C (2004) Yeast orthologues associated with glycerol transport and metabolism. FEMS Yeast Res 5(1):51–62
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
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
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
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
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
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
Pettersson N, Filipsson C, Becit E, Brive L, Hohmann S (2005) Aquaporins in yeasts and filamentous fungi. Biol Cell 97:487–500
Philips J, Herskowitz I (1997) Osmotic balance regulates cell fusion during mating in Saccharomyces cerevisiae. J Cell Biol 138(5):961–974
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
Ramahaleo T, Morillon R, Alexandre J, Lassalles JP (1999) Osmotic water permeability of isolated protoplasts. Modifications during development. Plant Physiol 119(3):885–96
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
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
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
Richards JH, Caldwell MM (1987) Hydraulic lift: substantial nocturnal water transport between soil layers by Artemisia tridentata roots. Oecologia 73(4):486–489
Robinson CH (2001) Cold adaptation in Arctic and Antarctic fungi. New Phytol 151(2):341–353
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
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
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
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
Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic, London
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
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
Soveral G, Madeira A, Loureiro-Dias MC, Moura TF (2008) Membrane tension regulates water transport in yeast. BBA 1778(11):2573–2579
Soveral G, Prista C, Moura TF, Loureiro-Dias MC (2011) Yeast water channels: an overview of orthodox aquaporins. Biol Cell 103(1):35–54
Steudle E (1989) Water flow in plants and its coupling to other processes: an overview. Methods Enzymol 174:183–225
Steudle E (1994) Water transport across roots. Plant Soil 167:79–90
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
Sussman AS, Halvorson HO (1966) Spores: their dormancy and germination. Harper and Row, New York
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
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
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
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
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
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
Tanghe A, Van Dijck P, Thevelein JM (2006) Why do microorganisms have aquaporins? Trends Microbiol 14(2):78–85
Theodorou C (1978) Soil moisture and the mycorrhizal association of Pinus radiata. Soil Biol Biochem 10:33–37
Theodorou C, Bowen GD (1970) Mycorrhizal responses of radiata pine in experiments with different fungi. Austr Forestr Res 34:182–191
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
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
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
Uhlig SK (1972) Investigations on the drought resistance of mycorrhiza-forming fungi. Zentralblatt für Bakteriologie, Parasitenkunde, Infectionskrankheiten und Hygiene 127(2):124–33
Unestam T (1991) Water repellency, mat formation, and leaf-stimulated growth of some ectomycorrhizal fungi. Mycorrhiza 1(1):13–20
Unestam T, Sun Y-P (1995) Extramatrical structures of hydrophobic and hydrophilic ectomycorrhizal fungi. Mycorrhiza 5(5):301–311
Vesk PA, Ashford AE, Markovina AL, Allaway WG (2000) Apoplasmic barriers and their significance in the exodermis and sheath of Eucalyptus pilularis–Pisolithus tinctorius ectomycorrhizas. New Phytol 145(2):333–346
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
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
Wessels JGH (1997) Hydrophobins: proteins that change the nature of the fungal surface. Adv Microb Physiol 38:1–45
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
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
Wösten HAB, Richter M, Willey JM (1999) Structural proteins involved in emergence of microbial aerial hyphae. Fungal Genet Biol 27(2–3):153–160
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
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
Young N, Ashford AE (1995) Apoplastic permeability of sclerotia of Sclerotium rolfsii, Sclerotium cepivorum and Rhizoctonia solani. New Phytol 131(1):33–40
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
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
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
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
Corresponding author
Rights and permissions
About this article
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
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-014-6049-0