Advertisement

Mycorrhiza

, Volume 21, Issue 2, pp 71–90 | Cite as

Ectomycorrhizas and water relations of trees: a review

  • Tarja Lehto
  • Janusz J. Zwiazek
Review

Abstract

There is plenty of evidence for improved nutrient acquisition by ectomycorrhizas in trees; however, their role in water uptake is much less clear. In addition to experiments showing improved performance during drought by mycorrhizal plants, there are several studies showing reduced root hydraulic conductivity and reduced water uptake in mycorrhizal roots. The clearest direct mechanism for increased water uptake is the increased extension growth and absorbing surface area, particularly in fungal species with external mycelium of the long-distance exploration type. Some studies have found increased aquaporin function and, consequently, increased root hydraulic conductivity in ectomycorrhizal plants while other studies showed no effect of ectomycorrhizal associations on root water flow properties. The aquaporin function of the fungal hyphae is also likely to be important for the uptake of water by the ectomycorrhizal plant, but more work needs to be done in this area. The best-known indirect mechanism for mycorrhizal effects on water relations is improved nutrient status of the host. Others include altered carbohydrate assimilation via stomatal function, possibly mediated by changes in growth regulator balance; increased sink strength in mycorrhizal roots; antioxidant metabolism; and changes in osmotic adjustment. None of these possibilities has been sufficiently explored. The mycorrhizal structure may also reduce water movement because of different fine root architecture (thickness), cell wall hydrophobicity or the larger number of membranes that water has to cross on the way from the soil to the xylem. In future studies, pot experiments comparing mycorrhizal and nonmycorrhizal plants will still be useful in studying well-defined physiological details. However, the quantitative importance of ectomycorrhizas for tree water uptake and water relations can only be assessed by field studies using innovative approaches. Hydraulic redistribution can support nutrient uptake during prolonged dry periods. In large trees with deep root systems, it may turn out that the most important function of mycorrhizas during drought is to facilitate nutrient acquisition.

Keywords

Ectomycorrhiza Mycelium Mineral nutrient Root conductance Water stress Water uptake 

Notes

Acknowledgements

We thank Pedro J. Aphalo for the constructive comments on the manuscript. The Academy of Finland (decision no.: 123637) provided funding for this study.

References

  1. Adler PR, Wilcox GE, Markhart AH III (1996) Ammonium decreases muskmelon root system hydraulic conductivity. J Plant Nutr 19:1395–1403Google Scholar
  2. Agerer R (2001) Exploration types of ectomycorrhizae—a proposal to classify ectomycorrhizal mycelial systems according to their patterns of differentiation and putative ecological importance. Mycorrhiza 11:107–114Google Scholar
  3. Allen MF (2007) Mycorrhizal fungi: highways for water and nutrients in arid soils. Vadose Zone J 6:291–297Google Scholar
  4. Allen MF (2009) Bidirectional water flows through the soil–fungal–plant mycorrhizal continuum. Commentary. New Phytol 182:290–293PubMedGoogle Scholar
  5. Allen EB, Allen MF, Helm FJ, Trappe JM, Molina R, Rincon E (1995) Patterns and regulation of mycorrhizal plant and fungal diversity. Plant Soil 170:47–62Google Scholar
  6. Alvarez M, Huygens D, Fernandez C, Gacitua Y, Olivares E, Saavedra I, Alberdi M, Valenzuela E (2009a) Effect of ectomycorrhizal colonization and drought on reactive oxygen species metabolism of Nothofagus dombeyi roots. Tree Physiol 29:1047–1057PubMedGoogle Scholar
  7. Alvarez M, Huygens D, Olivares E, Saavedra I, Alberdi M, Valenzuela E (2009b) Ectomycorrhizal fungi enhance nitrogen and phosphorus nutrition of Nothofagus dombeyi under drought conditions by regulating assimilative enzyme activities. Physiol Plant 136:426–436PubMedGoogle Scholar
  8. Amir R, Steudle E, Levanon D, Hadar Y, Chet I (1995) Turgor changes in Morchella esculenta during translocation and sclerotial formation. Exp Mycol 19:129–136Google Scholar
  9. Andersen CP, Sucoff EI, Dixon RK, Markhart AH III (1989) Effects of phosphorus deficiency on root hydraulic conductivity in Fraxinus pennsylvanica. Can J Bot 67:472–476Google Scholar
  10. Aphalo PJ, Lahti M, Lehto T, Repo T, Rummukainen A, Mannerkoski H, Finér L (2006) Responses of silver birch saplings to low soil temperature. Silva Fenn 40:429–442Google Scholar
  11. Aroca R, Bago A, Sutka M, Paz JA, Cano C, Amodeo G, Ruiz-Lozano JM (2009) Expression analysis of the first arbuscular mycorrhizal fungi expression between salt-stressed and nonstressed mycelium. MPMI 22:1169–1178PubMedGoogle Scholar
  12. Augé R (2001) Water relations, drought and vesicular–arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42Google Scholar
  13. Augé R (2004) Arbuscular mycorrhizae and soil/plant water relations. Can J Soil Sci 84:373–381Google Scholar
  14. Bakker MR, Augusto L, Achat DL (2006) Fine root distribution of trees and understory in mature stands of maritime pine (Pinus pinaster) on dry and humid sites. Plant Soil 286:37–51Google Scholar
  15. Beniwal RS, Langenfeld-Heyser R, Polle A (2010) Ectomycorrhiza and hydrogel protect hybrid poplar from water deficit and unravel plastic responses of xylem anatomy. Environ Exp Bot 69:189–197Google Scholar
  16. Bergh J, Linder S, Lundmark T, Elfving B (1999) The effect of water and nutrient availability on the productivity of Norway spruce in northern and southern Sweden. Forest Ecol Manage 119:51–62Google Scholar
  17. Biela A, Grote K, Otto B, Hoth S, Hedrich R, Kaldenhoff R (1999) The Nicotiana tabacum plasma membrane aquaporin NtAQP1 is mercury-insensitive and permeable for glycerol. Plant J 18:565–570PubMedGoogle Scholar
  18. Bogeat-Triboulot M-B, Bartoli F, Garbaye J, Marmeisse R, Tagu D (2004) Fungal ectomycorrhizal community affect root hydraulic properties and soil adherence to roots of Pinus pinaster seedlings. Plant Soil 267:213–223Google Scholar
  19. Boyd R (1987) The role of ectomycorrhiza in the water relations of plants. Ph.D. thesis, University of Sheffield, UK, p 136Google Scholar
  20. Boyd R, Furbank RT, Read DJ (1986) Ectomycorrhiza and the water relations of trees. In: Gianinazzi-Pearson V, Gianinazzi S (eds) Physiological and genetic aspects of mycorrhizae. INRA, Paris, pp 689–694Google Scholar
  21. Boyle CD, Hellenbrand KE (1991) Assessment of the effect of mycorrhizal fungi on drought tolerance of conifer seedlings. Can J Bot 69:1764–1771Google Scholar
  22. Brownlee C, Duddridge JA, Malibari A, Read DJ (1983) The structure and function of mycelia systems of ectomycorrhizal roots with special reference to their role in forming inter-plant connections and providing pathways for assimilate and water transport. Plant Soil 71:433–443Google Scholar
  23. Cairney JWG (1992) Translocation of solutes in ectomycorrhizal and saprotrophic rhizomorphs. Mycol Res 96:135–141Google Scholar
  24. Cairney JWG (2005) Basidiomycete mycelia in forest soils: dimensions, dynamics and roles in nutrient distribution. Mycol Res 109:7–20PubMedGoogle Scholar
  25. Cajander AK (1949) Forest site types and their significance. Acta For Fenn 56:1–71Google Scholar
  26. Calvo-Polanco M, Zwiazek JJ, Voicu MC (2008) Responses of ectomycorrhizal American elm (Ulmus americana) seedlings to salinity and soil compaction. Plant Soil 308:189–200Google Scholar
  27. Calvo-Polanco M, Jones MD, Zwiazek JJ (2009) Effects of pH on NaCl resistance of American elm (Ulmus americana) seedlings inoculated with Hebeloma crustuliniforme and Laccaria bicolor. Acta Physiol Plant 31:515–522Google Scholar
  28. Carvajal M, Cooke DT, Clarkson DT (1996) Responses of wheat plants to nutrient deprivation may involve regulation of water-channel function. Planta 199:372–381Google Scholar
  29. Coleman MD, Bledsoe CS, Smit-Spinks B (1987) Ectomycorrhizae decrease Douglas-fir root hydraulic conductivity. In: Sylvia DM, Hung LL, Graham JH (eds) Mycorrhizae in the next decade. Practical applications and research priorities. Institute of Food and Agricultural Sciences, University of Florida, Gainesville, p 243Google Scholar
  30. Coleman MD, Bledsoe CS, Lopushinsky W (1989) Pure culture response of ectomycorrhizal fungi to imposed water stress. Can J Bot 67:29–39Google Scholar
  31. Coleman MD, Bledsoe CS, Smit B (1990) Root hydraulic conductivity and xylem sap levels of zeatin riboside and abscisic acid in ectomycorrhizal Douglas fir seedlings. New Phytol 115:275–284Google Scholar
  32. Crowe JH (2007) Trehalose as a “chemical chaperone”: facts and fantasy. Adv Exp Med Biol 594:143–158PubMedGoogle Scholar
  33. Cudlín P, Kieliszewska-Rokicka B, Rudawska M, Grebenc T, Alberton O, Lehto T, Bakker M, Børja I, Konopka B, Leski T, Kraigher H, Kuyper T (2007) Fine roots and ectomycorrhizas as indicators of environmental change. Plant Biosystems 141:406–425Google Scholar
  34. Davies FT, Svenson SE, Cole JC, Phavaphutanon L, Duray SA, Olalde-Portugal V, Meier CE, Bo SH (1996) Non-nutritional stress acclimation of mycorrhizal woody plants exposed to drought. Tree Physiol 16:985–993Google Scholar
  35. Diebolt K, Mudge KW (1987) Do ectomycorrhizae influence host plant response to drought. In: Sylvia DM, Hung LL, Graham JH (eds) Mycorrhizae in the next decade. Practical applications and research priorities. Institute of Food and Agricultural Sciences, University of Florida, Gainesville, p 246Google Scholar
  36. di Pietro M, Churin J-L, Garbaye J (2007) Differential ability of ectomycorrhizas to survive drying. Mycorrhiza 17:547–550PubMedGoogle Scholar
  37. Dixon RK, Wright GM, Behrns GT, Tesky RO, Hinckley TM (1980) Water deficits and root growth of ectomycorrhizal white oak seedlings. Can J For Res 10:545–548Google Scholar
  38. Dixon RK, Pallardy SK, Garrett HE, Cox GS, Sander IL (1983) Comparative water relations of container-grown and bare-root ectomycorrhizal and nonmyocorrhizal Quercus velutina seedlings. Can J Bot 61:1559–1565Google Scholar
  39. Dordas C, Brown PH (2001) Evidence of channel mediated transport of boric acid in squash (Cucurbita pepo). Plant Soil 235:95–103Google Scholar
  40. Dosskey MG, Ballard TM (1980) Resistance to water uptake by Douglas-fir seedlings in soils of different texture. Can J For Res 10:530–534Google Scholar
  41. Dosskey MG, Boersma L, Linderman RG (1991) Role for the photosynthate demand of ectomycorrhizas in the response of Douglas fir seedlings to drying soil. New Phytol 117:327–334Google Scholar
  42. Douhan GW, Rizzo DM (2005) Phylogenetic divergence in a local population of the ectomycorrhizal fungus Cenococcum geophilum. New Phytol 166:263–271PubMedGoogle Scholar
  43. Dowd C, Wilson LW, McFadden H (2004) Gene expression profile changes in cotton root and hypocotyls tissues in response to infection with Fusarium oxysporum f. sp vasinfectum. Mol Plant-Microb Interact 17:654–667Google Scholar
  44. Duddridge JA, Malibari A, Read DJ (1980) Structure and function of mycorrhizal rhizomorphs with special reference to their role in water transport. Nature 287:834–836Google Scholar
  45. Dunabeitia MK, Hormilla S, Garcia-Plazaola JI, Txarterina K, Arteche U, Becerril JM (2004) Differential response of three fungal species to environmental factors and their role in the mycorrhization of Pinus radiata D. Don Mycorrhiza 14:11–18Google Scholar
  46. Egerton-Warburton LM, Graham RC, Hubbert KR (2003) Spatial variability in mycorrhizal hypae and nutrient and water availability in a soil–weathered bedrock profile. Plant Soil 249:331–342Google Scholar
  47. Egerton-Warburton LM, Querejeta JI, Allen MF (2007) Common mycorrhizal networks provide a potential pathway for the transfer of hydraulically lifted water between plants. J Exp Bot 58:1473–1483PubMedGoogle Scholar
  48. Fitter AH, Heinemeyer A, Staddon PL (2000) The impact of elevated CO2 and global climate change on arbuscular mycorrhizas: a mycocentric approach. New Phytol 147:179–187Google Scholar
  49. Fransson PMA, Taylor AFS, Finlay RD (2000) Effects of continuous optimal fertilization on belowground ectomycorrhizal community structure in a Norway spruce forest. Tree Physiol 20:599–606PubMedGoogle Scholar
  50. Gao YX, Li Y, Yang XX, Li HL, Shen QR, Guo SW (2010) Ammonium nutrition increases water absorption in rice seedlings (Oryza sativa L.) under water stress. Plant Soil 331:183–201Google Scholar
  51. Gaul D, Hertel D, Borken W, Matzner E, Leuschner C (2008) Effects of experimental drought on the fine root system of mature Norway spruce. Forest Ecol Manage 256:1151–1159Google Scholar
  52. Garbaye J (2000) The role of ectomycorrhizal symbiosis in the resistance of forests to water stress. Outlook Agric 29:63–69Google Scholar
  53. Garbaye J, Churin JL (1997) Growth stimulation of young oak plantations inoculated with the ectomycorrhizal fungus Paxillus involutus with special reference to summer drought. Forest Ecol Manage 98:221–228Google Scholar
  54. Gehring CA, Mueller RC, Whitham TG (2006) Environmental and genetic effects on the formation of ectomycorrhizal and arbuscular mycorrhizal associations in cottonwoods. Oecologia 149:158–164PubMedGoogle Scholar
  55. Gerbeau P, Amodeo G, Henzler T, Santoni V, Ripoche P, Maurel C (2002) The water permeability of Arabidopsis plasma membrane is regulated by divalent cations and pH. Plant J 30:71–81PubMedGoogle Scholar
  56. Giesler R, Högberg M, Högberg P (1998) Soil chemistry and plants in Fennoscandian boreal forest as exemplified by a local gradient. Ecology 79:119–137Google Scholar
  57. Glosser V, Zwieniecki MA, Orians CM, Holbrook NM (2007) Dynamic changes in root hydraulic properties in response to nitrate availability. J Exp Bot 58:2409–2415Google Scholar
  58. Guehl JM, Garbaye J (1990) The effects of ectomycorrhizal status on carbon-dioxide assimilation capacity, water-use efficiency and response to transplanting in seedlings of Pseudotsuga menziesii (Mirb.) Franco. Ann Sci For 47:551–563Google Scholar
  59. Guehl JM, Mousain D, Falconnet G, Gruez J (1990) Growth, carbon dioxide assimilation capacity and water-use efficiency of Pinus pinea L. seedlings inoculated with different ectomycorrhizal fungi. Ann Sci For 47:91–100Google Scholar
  60. Haberer K, Herbinger K, Alexou M, Rennenberg H, Tausz M (2008) Effects of drought and canopy ozone exposure on antioxidants in fine roots of mature European beech (Fagus sylvatica). Tree Physiol 28:713–719PubMedGoogle Scholar
  61. Helmisaari H-S, Ostonen I, Lõhmus K, Derome J, Lindroos A-J, Merilä P, Nöjd P (2009) Ectomycorrhizal root tips in relation to site and stand characteristics in Norway spruce and Scots pine stands in boreal forests. Tree Physiol 29:445–456PubMedGoogle Scholar
  62. Holm LM, Jahn TP, Moller AL, Schjoerring JK, Ferri D et al (2005) NH3 and NH4+permeability in aquaporin-expressing Xenopus oocytes. Pflügers Arch 450:415–428PubMedGoogle Scholar
  63. Huesken D, Steudle E, Zimmermann U (1978) Pressure probe technique for measuring water relations of cells in higher plants. Plant Physiol 61:158–163Google Scholar
  64. Hunt GA, Fogel R (1983) Fungal hyphal dynamics in a Western Oregon Douglas-fir stand. Soil Biol Biochem 15:641–649Google Scholar
  65. Jany JL, Martin F, Garbaye J (2003) Respiration activity of ectomycorrhizas from Cenococcum geophilum and Lactarius sp. in relation to soil water potential in five beech forests. Plant Soil 255:487–494Google Scholar
  66. Jentschke G, Godbold DL (2000) Metal toxicity and ectomycorrhizas. Physiol Plant 109:107–116Google Scholar
  67. Johansson I, Karlsson M, Shukla VK, Chrispeels MJ, Larsson C, Kjellbom P (1998) Water transport activity of the plasma membrane aquaporin PM28A is regulated by phosphorylation. Plant Cell 10:451–460PubMedGoogle Scholar
  68. Jones H (2004) What is water use efficiency? In: Bacon MA (ed) Water use efficiency in plant biology. Blackwell, Oxford, pp 27–41. ISBN 1-4051-1434-7Google Scholar
  69. Jones MD, Durall DM, Tinker PB (1998) Comparison of arbuscular and ectomycorrhizal Eucalyptus coccifera: growth response, phosphorus uptake efficiency and external hyphal production. New Phytol 140:125–134Google Scholar
  70. Jonsson L, Dahlberg A, Brandrud T-E (2000) Spatiotemporal distribution of an ectomycorrhizal community in an oligotrophic Swedish Picea abies forest subjected to experimental nitrogen addition: above- and below-ground views. Forest Ecol Manage 132:143–156Google Scholar
  71. Karlsson M, Fotiadis D, Sjövall S, Johansson I, Hedfalk K, Engel E, Kjellbomm P (2003) Reconstitution of water channel function of an aquaporin overexpressed and purified from Pichia pastoris. FEBS Lett 537:69–72Google Scholar
  72. Kojima S, Bohner A, von Wirén N (2006) Molecular mechanisms of urea transport in plants. J Membr Biol 212:83–91PubMedGoogle Scholar
  73. Kotze DJ, Johnson CA, O’Hara RB, Vepsäläinen K, Fowler MS (2004) Editorial. JNR 1:1–15Google Scholar
  74. Kramer PJ (1988) Changing concepts regarding plant water relations. Plant, Cell Environ 11:565–568Google Scholar
  75. Kramer PJ, Bullock HC (1966) Seasonal variations in the proportions of suberized and unsuberized roots of trees in relation to the absorption of water. Amer J Bot 53:200–204Google Scholar
  76. Lahti M, Aphalo PJ, Finér L, Lehto T, Leinonen I, Mannerkoski H, Ryyppö A (2002) Soil temperature, gas exchange and nitrogen status of 5-year-old Norway spruce seedlings. Tree Physiol 22:1311–1316PubMedGoogle Scholar
  77. Lambers H, Chapin FSIII, Pons TL (2008) Plant physiological ecology, 2nd edn. Springer, New YorkGoogle Scholar
  78. Lamhamedi MS, Bernier PY, Fortin JA (1992a) Growth, nutrition and response to water stress of Pinus pinaster inoculated with ten dikaryotic strains of Pisolithus sp. Tree Physiol 10:153–167PubMedGoogle Scholar
  79. Lamhamedi MS, Bernier PY, Fortin JA (1992b) Hydraulic conductance and soil water potential at the soil–root interface of Pinus pinaster seedlings inoculated with different dikaryons of Pisolithus sp. Tree Physiol 10:231–244PubMedGoogle Scholar
  80. Landhäusser SM, Muhsin TM, Zwiazek JJ (2002) The effect of ectomycorrhizae on water relations in aspen (Populus tremuloides) and white spruce (Picea glauca) at low soil temperatures. Can J Bot 80:684–689Google Scholar
  81. Lee J-E, Oliveira RS, Dawson TE, Fung I (2005) Root functioning modifies seasonal climate. Proc Natl Acad Sci USA 102:17576–17581PubMedGoogle Scholar
  82. Lee SH, Zwiazek JJ, Chung GC (2008) Light-induced transpiration alters cell water relations in figleaf gourd (Cucurbita ficifolia) seedlings exposed to low root temperatures. Physiol Plant 133:354–362PubMedGoogle Scholar
  83. Lee SH, Calvo Polanco M, Chung GC, Zwiazek JJ (2010) Cell water flow properties in root cortex of ectomycorrhizal (Pinus banksiana) seedlings. Plant Cell Environ 33:769–780PubMedGoogle Scholar
  84. Lehto J (1956) Studies on the natural reproduction of Scots pine on the upland soils of Southern Finland. Acta For Fenn 66:1–106Google Scholar
  85. Lehto T (1992a) Mycorrhizas and drought resistance of Picea sitchensis. I. In nutrient deficient conditions. New Phytol 122:661–668Google Scholar
  86. Lehto T (1992b) Mycorrhizas and drought resistance of Picea sitchensis. II. In conditions of adequate nutrition. New Phytol 122:669–673Google Scholar
  87. Lehto T (1992c) Effect of drought on Picea sitchensis seedlings inoculated with mycorrhizal fungi. Scand J For Res 7:177–182Google Scholar
  88. Lehto T, Brosinsky A, Heinonen-Tanski H, Repo T (2008) Freezing tolerance of ectomycorrhizal fungi in pure culture. Mycorrhiza 18:385–392PubMedGoogle Scholar
  89. Lilleskov EA, Bruns TD, Dawson TE, Camacho FJ (2009) Water sources and controls of water-loss rates of epigeous ectomycorrhizal fungal sporocarps during summer drought. New Phytol 182:483–494PubMedGoogle Scholar
  90. Linder MB, Szilvay GR, Nakari-Setälä T, Penttilä ME (2005) Hydrophobins: the protein-amphiphiles of filamentous fungi. FEMS Microbiol Rev 29:877–896PubMedGoogle Scholar
  91. Loqué D, Ludewig U, Yuan L, vonWirén N (2005) Tonoplast intrinsic proteins AtTIP2;1 and AtTIP2;3 facilitate NH3 transport into the vacuole. Plant Physiol 137:671–680PubMedGoogle Scholar
  92. Lovisolo C, Secchi F, Nardini A, Salleo S, Buffa R, Schubert A (2007) Expression of PIP1 and PIP2 aquaporins is enhanced in olive dwarf genotypes and is related to root and leaf hydraulic conductance. Physiol Plant 130:543–552Google Scholar
  93. Lucash MS, Eissenstat DM, Joslin JD, McFarlane KJ, Yanai RD (2007) Estimating nutrient uptake by mature tree roots under field conditions: challenges and opportunities. Trees 21:593–603Google Scholar
  94. Ma JF, Tamai K, Yamaji N, Mitani N, Konishi S et al (2006) A silicon transporter in rice. Nature 440:688–691PubMedGoogle Scholar
  95. Majdi H (2001) Changes in fine root production and longevity in relation to water and nutrient availability in a Norway spruce stand in northern Sweden. Tree Physiol 21:1057–1061PubMedGoogle Scholar
  96. Marjanović Ž (2004) Impact of mycorrhiza formation and drought stress on the expression and function of aquaporins in Norway spruce (Picea abies (L.) Karst.) and hybrid aspen (Populus tremula L. × Populus tremuloides Mich.) Ph.D. thesis, Karl-Eberhard Universität Tübingen, GermanyGoogle Scholar
  97. Marjanović Ž, Uehlein N, Kaldenhoff R, Zwiazek JJ, Weiß M, Hampp R, Nehls U (2005a) Aquaporins in poplar: what a difference a symbiont makes! Planta 222:258–268PubMedGoogle Scholar
  98. Marjanović Z, Nehls U, Hampp R (2005b) Mycorrhiza formation enhances adaptive response of hybrid poplar to drought. Ann NY Acad Sci 1048:496–499PubMedGoogle Scholar
  99. Martin F, Díez J, Dell B, Delaruelle C (2002) Phylogeography of the ectomycorrhizal Pisolithus species as inferred from nuclear ribosomal DNA ITS sequences. New Phytol 153:345–357Google Scholar
  100. Marulanda A, Azcon R, Chaumont F, Ruiz-Lozano JM, Aroca R (2010) Regulation of plasma membrane aquaporins by inoculation with a Bacillus megaterium strain in maize (Zea mays L.) plants under unstressed and salt-stressed conditions. Planta 232:533–543PubMedGoogle Scholar
  101. Marx DH, Cordell CE, Kenney DS, Mexal JG, Artman JD, Riffle JW, Molina RJ (1984) Commercial vegetative inoculums of Pisolithus tinctorius and inoculation techniques for development of ectomycorrhizae on bare-root tree seedlings. Forest Sci Monograph 25 (Suppl to vol 30)Google Scholar
  102. Maurel C, Verdoucq L, Luu D-T, Santoni V (2008) Plant aquaporins: membrane channels with multiple integrated functions. Annu Rev Plant Biol 59:595–624PubMedGoogle Scholar
  103. Maurel C, Santoni V, Luu D-T, Wudick MM, Verdoucq L (2009) The cellular dynamics of plant aquaporin expressions and functions. Curr Opin Plant Biol 12:690–698PubMedGoogle Scholar
  104. Meyer FH (1974) Physiology of mycorrhiza. Ann Rev Plant Physiol 25:567–586Google Scholar
  105. McHugh TA, Gehring CA (2006) Below-ground interactions with arbvuscular mycorrhizal shrubs decrease the performance of pinyon pine and the abundance of its ectomycorrhizas. New Phytol 171:171–178PubMedGoogle Scholar
  106. Mexal J, Reid CPP (1973) The growth of selected mycorrhizal fungi in response to induced water stress. Can J Bot 51:1579–1588Google Scholar
  107. Mikola P (1965) Studies on the ectendotrophic mycorrhiza on pine. Acta For Fenn 79(2):1–56Google Scholar
  108. Money NP (1990) Measurement of hyphal turgor. Exp Mycol 14:416–425Google Scholar
  109. Muhsin TM, Zwiazek JJ (2002a) Ectomycorrhizas increase apoplastic water transport and hydraulic conductivity in Ulmus americana seedlings. New Phytol 153:153–158Google Scholar
  110. Muhsin TM, Zwiazek JJ (2002b) Ectomycorrhizae increase water conductance and protect white spruce (Picea glauca) seedlings against salt stress. Plant Soil 238:217–225Google Scholar
  111. Nadezhdina N, Ferreira MI, Silva R, Pacheco CA (2008) Seasonal variation of water uptake of a Quercus suber tree in Central Portugal. Plant Soil 305:105–119Google Scholar
  112. Nardini A, Salleo S, Tyree MT, Vertovec M (2000) Influence of the ectomycorrhizas formed by Tuber melanosporum Vitt. on hydraulic conductance and water relations of Quercus ilex L. seedlings. Ann For Sci 57:305–312Google Scholar
  113. Nilsen P, Børja I, Knutsen H, Brean R (1998) Nitrogen and drought effects on ectomycorrhizae of Norway spruce [Picea abies L. (Karst.)]. Plant Soil 198:179–184Google Scholar
  114. Nylund J-E (1987) The ectomycorrhizal infection zone and its relation to acid polysaccharides of cortical cell walls. New Phytol 106:505–516Google Scholar
  115. Oertli JJ (1991) Transport of water in the rhizosphere and in roots. In: Waisel Y, Eshel A, Kafkafi U (eds) Plant roots: the hidden half. Marcel Dekker, New YorkGoogle Scholar
  116. Ortega U, Duñabeitia A, Menendez S, Gonzalez-Murua C, Majada J (2004) Effectiveness of mycorrhizal inoculation in the nursery on growth and water relations of Pinus radiata in different water regimes. Tree Physiol 24:65–73PubMedGoogle Scholar
  117. Pallardy SG, Parker WC, Dixon RK, Garrett HE (1983) Tissue water relations of roots and shoots of droughted ectomycorrhizal shortleaf pine seedlings. In: Thielges BA (ed) Proceedings of the 7th North American Forest Biology Workshop “Physiology and Genetics of intensive culture”. University of Kentucky, Lexington, KY, pp 386–373Google Scholar
  118. Parke JL, Linderman RG, Black CH (1983) The role of ectomycorrhizas in drought tolerance of Douglas-fir seedlings. New Phytol 95:83–95Google Scholar
  119. Pettersson N, Filipsson C, Becit E, Brive L, Hohmann S (2005) Aquaporins in yeasts and filamentous fungi. Biol Cell 97:487–500PubMedGoogle Scholar
  120. Peuke AD, Rennenberg H (2004) Carbon, nitrogen, phosphorus, and sulphur concentration and partitioning in beech ecotypes (Fagus sylvatica L.): phosphorus most affected by drought. Trees 18:639–648Google Scholar
  121. Pigott CD (1982) Survival of mycorrhiza formed by Cenococcum geophilum Fr. in dry soils. New Phytol 92:513–517Google Scholar
  122. Plamboeck AH, Dawson TE, Egerton-Warburton LE, North M, Bruns TD, Querejeta JI (2007) Water transfer via ectomycorrhizal fungal hyphae to conifer seedlings. Mycorrhiza 17:439–447PubMedGoogle Scholar
  123. Pratt RB, Jacobsen AL, North GB, Sack L, Schenk HJ (2008) Plant hydraulics: new discoveries in the pipeline. New Phytol 179:590–593PubMedGoogle Scholar
  124. Querejeta JI, Egerton-Warburton LM, Allen MF (2003) Direct nocturnal transfer from oaks to their mycorrhizal symbionts during severe soil drying. Oecologia 134:55–64PubMedGoogle Scholar
  125. Querejeta JI, Egerton-Warburton LM, Allen MF (2007) Hydraulic lift may buffer rhizosphere hyphae against the negative effects of severe soil drying in a California Oak savanna. Soil Biol Biochem 39:409–417Google Scholar
  126. Querejeta JI, Egerton-Warburton LM, Allen MF (2009) Topographic position modulates the mycorrhizal response of oak trees to interannual rainfall variability. Ecology 90:649–662PubMedGoogle Scholar
  127. Radin JW, Boyer JS (1982) Control of leaf expansion by nitrogen nutrition in sunflower plants. Role of hydraulic conductivity and turgor. Plant Physiol 69:771–775PubMedGoogle Scholar
  128. Radin JW, Eidenbock MP (1984) Hydraulic conductance as a factor limiting leaf expansion of phosphorus-deficient cotton plants. Plant Physiol 75:372–377PubMedGoogle Scholar
  129. Read DJ (1984) The structure and function of the vegetative mycelium of mycorrhizal roots. In: Jennings DH, Rayner ADM (eds) The ecology and physiology of the fungal mycelium. Cambridge University Press, Cambridge, pp 215–240Google Scholar
  130. Read DJ (1991) Mycorrhizas in ecosystems. Experientia 47:376–391Google Scholar
  131. Read DJ, Malibari A (1979) Water transport through mycelial strands to ectomycorrhizal roots of pine. In: Riedacker A, Cagnair-Michard J (eds) Root physiology and symbiosis. CNFR, Nancy, France, pp 410–423Google Scholar
  132. Read DJ, Boyd R (1986) Water relations of mycorrhizal fungi and their host plants. In: Ayres PG, Boddy L (eds) Water, fungi and plants. Cambridge University Press, Cambridge, pp 215–240Google Scholar
  133. Reid CPP (1979) Mycorrhizae and water stress. In: Riedacker A, Gagnaire-Michard J (eds) Root physiology and symbiosis. Proceedings of the IUFRO symposium. Nancy, France, pp 392–409Google Scholar
  134. Reid CPP, Bowen GD (1979) Effect of water stress on phosphorus uptake by mycorrhizas of Pinus radiata. New Phytol 83:103–107Google Scholar
  135. Richards JH, Caldwell MM (1987) Hydraulic lift: substantial nocturnal water transport between soil layers by Artemisia tridentata roots. Oecologia 73:486–489Google Scholar
  136. Rosling A, Landeweert R, Lindahl BD (2003) Vertical distribution of ectomycorrhizal fungal taxa in a podzol soil profile. New Phytol 159:775–783Google Scholar
  137. Sade N, Vincour BJ, Diber A, Shatil A, Ronen G, Nissan H, Wallach R, Karchi H, Moshelion M (2009) Improving plant stress tolerance and yield production: is the tonoplast aquaporin SITIP2;2 a key to isohydric to anisohydric conversion? New Phytol 181:651–661PubMedGoogle Scholar
  138. Sade N, Gebretsadik K, Seligmann R, Scwartz A, Wallach R, Moshelion M (2010) The role of tobacco aquaporin 1 in improving water use efficiency, hydraulic conductivity and yield production under salt stress. Plant Physiol 152:245–254PubMedGoogle Scholar
  139. Sands R, Theodorou C (1978) Water uptake by mycorrhizal roots of radiata pine seedlings. Aust J Plant Physiol 5:301–309Google Scholar
  140. Sands R, Fiscus EL, Reid CPP (1982) Hydraulic properties of pine and bean roots with varying degrees of suberization, vascular differentiation and mycorrhizal infection. Aust J Plant Physiol 9:559–569Google Scholar
  141. Schier GA, McQuattle CJ (2000) Effect of water stress on aluminium toxicity in pitch pine seedlings. J Plant Nutr 23:637–647Google Scholar
  142. Schoonmaker AL, Teste FP, Simard SW, Guy RD (2007) Tree proximity, soil pathways and common mycorrhizal networks: their influence on the utilization of redistributed water by understory seedlings. Oecologia 154:455–466PubMedGoogle Scholar
  143. Schwinning S (2010) The ecohydrology of roots in rocks. Ecohydrol 3:238–245Google Scholar
  144. Shi L, Guttenberger M, Kottke I, Hampp R (2002) The effect of drought on mycorrhizas of beech (Fagus sylvatica L): changes in community structure, and the content of carbohydrates and nitrogen storage bodies of the fungi. Mycorrhiza 12:303–311PubMedGoogle Scholar
  145. Siemens AJ, Zwiazek JJ (2008) Root hydraulic properties and growth of balsam poplar (Populus balsamifera) mycorrhizal with Hebeloma crustuliniforme and Wilcoxina mikolae var. mikolae. Mycorrhiza 18:393–401PubMedGoogle Scholar
  146. Simard SW, Perry DA, Jones MD, Myrolds DD, Durall DM, Molina R (1997) Net transfer of carbon between ectomycorrhizal tree species in the field. Nature 388:579–582Google Scholar
  147. Shvaleva AL, Silva FCE, Breia E, Jouve L, Hausman JF, Almeidea MH, Maroco JP, Rodrigues ML, Pereira JS, Chaves MM (2006) Metabolic responses to water deficits in two Eucalyptus globulus clones with contrasting drought sensitivity. Tree Physiol 26:239–248PubMedGoogle Scholar
  148. Smith SE, Read DJ (1997) Mycorrhizal symbiosis, 2nd ed. Academic Press, p 603Google Scholar
  149. Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3 rd ed. Academic Press, p 787Google Scholar
  150. Steudle E (1993) Pressure probe techniques: basic principles and application to studies of water and to studies of water and solute relations at cell, tissue and organ. In: Smith JAC, Griffiths H (eds) Water deficits: plant responses from cell to community. Bios Scientific Publishers Ltd., Oxford, pp 5–36Google Scholar
  151. Steudle E, Peterson CA (1998) How does water get through roots? J Exp Bot 49:775–788Google Scholar
  152. Sun Y-P, Unestam T, Lucas SD, Johanson KJ, Kenne L, Finlay RD (1999) Exudation-reabsorption in a mycorrhizal fungus, the dynamic interface for interaction with soil and soil microorganisms. Mycorrhiza 9:137–144Google Scholar
  153. Syvertsen JP, Graham JH (1985) Hydraulic conductivity of roots, mineral nutrition, and leaf gas exchange of Citrus rootstocks. J Amer Soc Hort Sci 110:865–869Google Scholar
  154. Swaty RL, Gehring CA, van Ert M, Theimer TC, Keim P, Whitham TG (1998) Temporal variation in temperature and rainfall differentially affects ectomycorrhizal colonization at two contrasting sites. New Phytol 139:733–739Google Scholar
  155. Teste FP, Simard SW, Durall DM, Guy RD, Jones MD, Schoonmaker AL (2009) Access to mycorrhizal networks and roots of trees: importance for seedling survival and resource transfer. Ecology 90:2808–2822PubMedGoogle Scholar
  156. Theodorou C (1978) Soil moisture and the mycorrhizal association of Pinus radiata D.Don. Soil Biol Biochem 10:33–37Google Scholar
  157. Tyree MT, Jarvis PG (1982) Tissue water relations. In: Lange O, Nobel PS, Osmond CB, Ziegler H (eds) Physiological plant ecology II. Encyclopedia of plant physiology, new ser vol 12B. Springer, pp 34–78Google Scholar
  158. Tyree MT, Patino S, Bennink J, Alexander J (1995) Dynamic measurements of root hydraulic conductance using a high-pressure flowmeter in the laboratory and field. J Exp Bot 46:83–94Google Scholar
  159. Uehlein N, Fileschi K, Eckert M, Bienert GP, Bertl A, Kaldenhoff R (2007) Arbuscular mycorrhizal symbiosis and plant aquaporin expression. Phytochemistry 68:122–129PubMedGoogle Scholar
  160. Unestam T (1991) Water repellency, mat formation and leaf-stimulated growth of some ectomycorrhizal fungi. Mycorrhiza 1:13–20Google Scholar
  161. Unestam T, Sun YP (1995) Extramatrical structures of hydrophobic and hydrophilic ectomycorrhizal fungi. Mycorrhiza 5:301–311Google Scholar
  162. Van Scholl L, Kuyper TW, Smits MM, Landeweert R, Hoffland E, van Breemen N (2008) Rock-eating mycorrhizas: their role in plant nutrition and biogeochemical cycles. Plant Soil 303:35–47Google Scholar
  163. Vera-Estrella R, Barkla BJ, Bohnert HJ, Pantoja O (2004) Novel regulation of aquaporins during osmotic stress. Plant Physiol 135:2318–2329PubMedGoogle Scholar
  164. Voicu MC, Zwiazek JJ (2004) Cycloxeximide inhibits root water flow and stomatal conductance in aspen (Populus tremuloides) seedlings. Plant Cell Environ 27:199–208Google Scholar
  165. Walker RF, West DC, McLaughlin SB, Amundsen CC (1989) Growth, xylem pressure potential and nutrient absorption of loblolly pine on a reclaimed surface mine as affected by an induced Pisolithus tinctorius infection. Forest Sci 35:569–581Google Scholar
  166. Wan X, Zwiazek JJ (1999) Mercuric chloride effects on root water transport in aspen (Populus tremuloides) seedlings. Plant Physiol 121:939–946PubMedGoogle Scholar
  167. Wan X, Landhäusser SM, Zwiazek JJ, Lieffers VJ (1999) Root water flow and growth of aspen (Populus tremuloides) at low root temperatures. Tree Physiol 19:879–884PubMedGoogle Scholar
  168. Warren JM, Meinzer FC, Brooks JR, Domec J-C, Coulombe R (2007) Hydraulic redistribution of soil water in two old-growth coniferous forests: quantifying patterns and controls. New Phytol 173:753–765PubMedGoogle Scholar
  169. Warren JM, Brooks JR, Meinzer FC, Eberhart JL (2008) Hydraulic redistribution of water from Pinus ponderosa trees to seedlings: evidence for an ectomycorrhizal pathway. New Phytol 178:382–394PubMedGoogle Scholar
  170. Weatherley PE (1982) Water uptake and flow in roots. In: Lange O, Nobel PS, Osmond CB, Ziegler H (eds) Physiological plant ecology II. Encyclopedia of plant physiology, new ser vol 12B. Springer, New York, pp 79–108Google Scholar
  171. Worley JF, Hacskaylo E (1959) The effect of available soil moisture on the mycorrhizal association of Virginia pine. Forest Sci 5:267–268Google Scholar
  172. Wu B, Watanabe I, Hayatsu M, Nioh I (1999) Effect of ectomycorrhizae on the growth and uptake and transport of N-15-labeled compounds by Pinus tabulaeformis seedlings under water-stressed conditions. Biol Fert Soils 28:136–138Google Scholar
  173. Wudick MM, Luu DT, Maurel C (2009) A look inside: localization patterns and functions of intracellular plant aquaporins. New Phytol 184:289–302PubMedGoogle Scholar
  174. Yi H, Calvo-Polanco M, MacKinnon MD, Zwiazek JJ (2008) Responses of ectomycorrhizal Populus tremuloides and Betula papyrifera seedlings to salinity. Environ Exp Bot 62:357–363Google Scholar
  175. Zardoya R (2005) Phylogeny and evolution of the major intrinsic protein family. Biol Cell 97:397–414PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  1. 1.School of Forest SciencesUniversity of Eastern FinlandJoensuuFinland
  2. 2.Department of Renewable ResourcesUniversity of AlbertaEdmontonCanada

Personalised recommendations