Plant and Soil

, Volume 406, Issue 1–2, pp 15–27 | Cite as

Species-specific roles of ectomycorrhizal fungi in facilitating interplant transfer of hydraulically redistributed water between Pinus halepensis saplings and seedlings

  • Iván Prieto
  • Antonio Roldán
  • Dries Huygens
  • María del Mar Alguacil
  • José A. Navarro-Cano
  • José I. Querejeta
Regular Article


Background and aims

Interplant transfer of hydraulically redistributed water (HRW) can take place via mycorrhizal hyphal networks linking the roots of neighboring plants. We conducted a mesocosm experiment to evaluate the influence of reduced extraradical hyphal lengths on interplant HRW transfer.


Ectomycorrhizal Pinus halepensis saplings and seedlings were grown together in two-compartment mesocosms (fungicide-treated or control), and deuterium-labeled water was supplied to the taproot compartment (accessible to sapling taproots) during a 9-day soil drying cycle.


Upper soil water contents and seedling water potentials at the end of the drying cycle were lower in fungicide-treated than in control mesocosms. The stem water δD values of seedlings increased (marginally) with increasing soil hyphal length in both treatments separately, suggesting that interplant HRW transfer was at least partly mediated by fungal hyphae. In fungicide-treated mesocosms, the difference in δD values between the stem water of seedlings and upper soil water decreased sharply with increasing soil hyphal length, supporting a key role of ectomycorrhizal fungi (EMF) in interplant HRW transfer at low soil hyphal densities. However, two dominant EMF morphotypes differing in their water repellence properties and hyphal exploration types (Thelephora terrestris and Suillus granulatus) had contrasting impacts on hydraulic redistribution patterns, as only the EMF producing hydrophilic hyphae (T. terrestris) enhanced HRW transfer between pine saplings and seedlings.


Changes in the abundance and/or composition of EMF communities in response to anthropogenic disturbance or climate change could affect facilitative plant interactions through alterations of interplant HRW transfer.


Aleppo pine Hydraulic redistribution Interplant water transfer Ectomycorrhizal pathways Specific root length 



This work was supported by the Ministerio de Ciencia e Innovación (Reference Grant number CGL2010-21064). Iván Prieto acknowledges support from the “Juan de la Cierva” program of the Spanish Ministerio de Economía y Competitividad (Grant number FPDI-2013-16221). We would like to thank the editor and two anonymous reviewers for their insightful and helpful comments. The experiments reported here comply with the current laws of the country in which the experiments were conducted (Spain).

Supplementary material

11104_2016_2860_MOESM1_ESM.docx (931 kb)
ESM 1 (DOCX 931 kb)


  1. Agerer R (ed) (1987–2006) Colour Atlas of Ectomycorrhizae. Einhorn-Verlag, Schwäbisch GmündGoogle Scholar
  2. Agerer R (2001) Exploration types of ectomycorrhizae. Mycorrhiza 11:107–114CrossRefGoogle Scholar
  3. Allison GB, Barnes CJ, Hughes MW (1983) The distribution of deuterium and 18O in dry soils 2. Experimental. J Hydrol 64:377–397Google Scholar
  4. Amaranthus MP, Perry D (1989) Rapid root tip and mycorrhiza formation and increased survival of Douglas-fir seedlings after soil transfer. New Forest 3:259–264CrossRefGoogle Scholar
  5. Armas C, Kim JH, Bleby TM, Jackson RB (2012) The effect of hydraulic lift on organic matter decomposition, soil nitrogen cycling, and nitrogen acquisition by a grass species. Oecologia 168:11–22CrossRefPubMedGoogle Scholar
  6. Augé RM (2004) Arbuscular mycorrhizae and soil/plant water relations. Can J Soil Sci 84:373–381CrossRefGoogle Scholar
  7. Augé RM, Stodola AJW, Tims JE, Saxton AM (2001) Moisture retention properties of a mycorrhizal soil. Plant Soil 230:87–97CrossRefGoogle Scholar
  8. Bardgett RD (1991) The use of the membrane filter technique for comparative measurements of hyphal lengths in different grassland sites. Agr Ecosyst Environ 34:115–119CrossRefGoogle Scholar
  9. Bauerle TL, Richards JH, Smart DR, Eissenstat DM (2008) Importance of internal hydraulic redistribution for prolonging the lifespan of roots in dry soil. Plant Cell Environ 31:177–186PubMedGoogle Scholar
  10. Bingham MA, Simard S (2012) Ectomycorrhizal networks of Pseudotsuga menziesii var. glauca trees facilitate establishment of conspecific seedlings under drought. Ecosystems 15:188–199CrossRefGoogle Scholar
  11. Bogeat-Triboulot MB, 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 267:213–223CrossRefGoogle Scholar
  12. Booth MG, Hoeksema JD (2010) Mycorrhizal networks counteract competitive effects of canopy trees on seedling survival. Ecology 91:2294–2302CrossRefPubMedGoogle Scholar
  13. Brooks JR, Meinzer FC, Coulombe R, Gregg J (2002) Hydraulic redistribution of soil water during summer drought in two contrasting Pacific Northwest coniferous forests. Tree Physiol 22:1107–1117CrossRefPubMedGoogle Scholar
  14. Brownlee C, Duddridge JA, Malibari A, Read DJ (1983) The structure and function of mycelial systems of ectomycorrhizal roots with a special reference to their role in forming inter-plant connections and providing pathways for assimilate and water transport. Plant Soil 71:433–443CrossRefGoogle Scholar
  15. Brundrett MC (2009) Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil 320:37–77CrossRefGoogle Scholar
  16. Caldwell MM, Richards JH (1989) Hydraulic lift: water efflux from upper roots improves effectiveness of water uptake by deep roots. Oecologia 79:1–5CrossRefGoogle Scholar
  17. Caldwell MM, Dawson TE, Richards JH (1998) Hydraulic lift: consequences of water efflux from the roots of plants. Oecologia 113:151–161CrossRefGoogle Scholar
  18. Cardon ZG, Stark JM, Herron PM, Rasmussen JA (2013) Sagebrush carrying out hydraulic lift enhances surface soil nitrogen cycling and nitrogen uptake into inflorescences. Proc Natl Acad Sci USA 110:18988–18993Google Scholar
  19. Dawson TE (1993) Hydraulic lift and water use by plants: implications for water balance, performance, and plant–plant interactions. Oecologia 95:565–574CrossRefGoogle Scholar
  20. Dawson TE (1996) Determining water use by trees and forests from isotopic, energy balance, and transpiration analyses: the roles of tree size and hydraulic lift. Tree Physiol 16:263–272CrossRefPubMedGoogle Scholar
  21. Domec JC, King JS, Noormets A, Treasure E, Gavazzi MJ, Sun G, McNulty SG (2010) Hydraulic redistribution of soil water by roots affects whole-stand evapotranspiration and net ecosystem carbon exchange. New Phytol 187:171–183CrossRefPubMedGoogle Scholar
  22. Duddridge JA, Malibari A, Read DJ (1980) Structure and function of mycorrhizal rhizomorphs with special reference to their role in water transport. Nature 287:834–836CrossRefGoogle Scholar
  23. 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 58:1473–1483CrossRefPubMedGoogle Scholar
  24. Egerton-Warburton LM, Querejeta JI, Allen MF (2008) Efflux of hydraulically lifted water from mycorrhizal fungal hyphae during imposed drought. Plant Signal Behav 3:68–71CrossRefPubMedPubMedCentralGoogle Scholar
  25. Ehleringer JR, Osmond CB (1989) Stable isotopes. In: Pearcy RW, Ehleringer JR, Mooney HA, Rundel PW (eds) Plant physiological ecology. Kluwer Academic Publishers, London, pp 281–300CrossRefGoogle Scholar
  26. Eissenstat DM (1991) On the relationship between specific root length and the rate of root proliferation: a field study using citrus rootstocks. New Phytol 118:63–68CrossRefGoogle Scholar
  27. Filella I, Peñuelas J (2003) Indications of hydraulic lift by Pinus halepensis and its effects on the water relations of neighbour shrubs. Biol Plantarum 47:209–214CrossRefGoogle Scholar
  28. Flanagan LB, Ehleringer JR (1991) Stable isotope composition of stem and leaf water: applications to the study of plant water use. Funct Ecol 5:270–277CrossRefGoogle Scholar
  29. Fuentes D, Valdecantos A, Llovet J, Cortina J, Vallejo VR (2010) Fine-tuning of sewage sludge application to promote the establishment of Pinus halepensis seedlings. Ecol Eng 36:1213–1221CrossRefGoogle Scholar
  30. Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes—application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118CrossRefPubMedGoogle Scholar
  31. Grand LF, Harvey AE (1982) Quantitative measurements of ectomycorrhizae on plant roots. methods and principles of mycorrhizal research. Am Phytopathol Soc, St PaulGoogle Scholar
  32. Hoagland DR, Arnon DI (1950) The water-culture method of growing plants without soil. Calif Aes Bull 347:31Google Scholar
  33. Huang B, Eissenstat DM (2000) Linking hydraulic conductivity to anatomy in plants that vary in specific root length. J Am Soc Hortic Sci 125:260–264Google Scholar
  34. Hummel I, Vile D, Violle C, Devaux J, Ricci B, Blanchard A, Garnier E, Roumet C (2007) Relating root structure and anatomy to whole-plant functioning in 14 herbaceous Mediterranean species. New Phytol 173:313–321CrossRefPubMedGoogle Scholar
  35. Kummerow J, Krause D, Jow W (1978) Seasonal changes of fine root density in the Southern Californian chaparral. Oecologia 37:201–212CrossRefGoogle Scholar
  36. Lehto T, Zwiazek J (2011) Ectomycorrhizas and water relations of trees: a review. Mycorrhiza 21:71–90CrossRefPubMedGoogle Scholar
  37. Maestre FT, Cortina J (2004) Are Pinus halepensis plantations useful as a restoration tool in semiarid Mediterranean areas? For Ecol Manag 198:303–317CrossRefGoogle Scholar
  38. Marjanović Ž, Uehlein N, Kaldenhoff R, Zwiazek JJ, Weiß M, Hampp R, Nehls U (2005) Aquaporins in poplar: what a difference a symbiont makes! Planta 222:258–268CrossRefPubMedGoogle Scholar
  39. Muhsin TM, Zwiazek JJ (2002) Ectomycorrhizas increase apoplastic water transport and hydraulic conductivity in Ulmus americana seedlings. New Phytol 153:153–158CrossRefGoogle Scholar
  40. Plamboeck AH, Dawson TE, Egerton-Warburton LE, North M, Bruns TD, Querejeta JI (2007) Water transfer via ectomycorrhizal fungal hyphae to conifer seedlings. Mycorrhiza 17:439–447CrossRefPubMedGoogle Scholar
  41. Prieto I, Ryel RJ (2014) Internal hydraulic redistribution prevents the loss of root conductivity during drought. Tree Physiol 34:39–48CrossRefPubMedGoogle Scholar
  42. Prieto I, Padilla FM, Armas C, Pugnaire FI (2011) The role of hydraulic lift on seedling establishment under a nurse plant species in a semi-arid environment. Perspect Plant Ecol Evol Syst 13:181–187CrossRefGoogle Scholar
  43. Prieto I, Armas C, Pugnaire FI (2012) Water release through plant roots: new insights into its consequences at the plant and ecosystem level. New Phytol 193:830–841CrossRefPubMedGoogle Scholar
  44. Querejeta JI, Roldan A, Albaladejo J, Castillo V (2001) Soil water availability improved by site preparation in a Pinus halepensis afforestation under semiarid climate. For Ecol Manag 149:115–128CrossRefGoogle Scholar
  45. Querejeta JI, Egerton-Warburton LM, Allen MF (2003) Direct nocturnal transfer from oaks to their mycorrhizal symbionts during severe soil drying. Oecologia 134:55–64CrossRefPubMedGoogle Scholar
  46. Querejeta JI, Egerton-Warburton LM, Allen MF (2009) Topographic position modulates the mycorrhizal response of oak trees to interannual rainfall variability. Ecology 90:649–662CrossRefPubMedGoogle Scholar
  47. Querejeta JI, Egerton-Warburton LM, Prieto I, Vargas R, Allen MF (2012) Changes in soil hyphal abundance and viability can alter the patterns of hydraulic redistribution by plant roots. Plant Soil 355:63–73CrossRefGoogle Scholar
  48. Richter H (1997) Water relations of plants in the field: some comments on the measurement of selected parameters. J Exp Bot 48:1–7CrossRefGoogle Scholar
  49. Roberts J (1976) A study of root distribution and growth in a Pinus sylvestris L. (Scots Pine) plantation in East Anglia. Plant Soil 44:607–621CrossRefGoogle Scholar
  50. Schoonmaker A, Teste F, Simard S, Guy R (2007) Tree proximity, soil pathways and common mycorrhizal networks: their influence on the utilization of redistributed water by understory seedlings. Oecologia 154:455–466CrossRefPubMedGoogle Scholar
  51. Sylvia DM (1992) Quantification of external hyphae of vesicular-arbuscular mycorrhizal fungi. Method Microbiol 24:53–65CrossRefGoogle Scholar
  52. Tennant D (1975) A test of the modified root intersect method of estimating root length. J Ecol 63:995–1001CrossRefGoogle Scholar
  53. Teste F, Simard S (2008) Mycorrhizal networks and distance from mature trees alter patterns of competition and facilitation in dry Douglas-fir forests. Oecologia 158:193–203CrossRefPubMedGoogle Scholar
  54. Teste F, Karst J, Jones MD, Simard S, Durall DM (2006) Methods to control ectomycorrhizal colonization: effectiveness of chemical and physical barriers. Mycorrhiza 17:51–65CrossRefPubMedGoogle Scholar
  55. Torres P, Honrubia M (1991) In vitro synthesis of ectomycorrhizae between Suillus collinitus (Fr.) O Kuntze and Rhizopogon roseolus (Corda) Th M Fr. with Pinus halepensis Miller. Mycotaxon 41:437–443Google Scholar
  56. Torres P, Honrubia M (1994) Ectomycorrhizal associations proven for Pinus halepensis. Israel J Plant Sci 42:51–58CrossRefGoogle Scholar
  57. Unestam T (1991) Water repellency, mat formation and leaf-stimulated growth of some ectomycorrhizal fungi. Mycorrhiza 1:13–20CrossRefGoogle Scholar
  58. Unestam T, Sun YP (1995) Extramatrical structures of hydrophobic and hydrophilic ectomycorrhizal fungi. Mycorrhiza 5:301–311CrossRefGoogle Scholar
  59. 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 178:382–394CrossRefPubMedGoogle Scholar
  60. White TJ, Bruns T, Lee S et al. (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ and White TJ (Eds.). PCR protocols. a guide to methods and applications, San Diego, pp. 315–322Google Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Iván Prieto
    • 1
  • Antonio Roldán
    • 1
  • Dries Huygens
    • 2
  • María del Mar Alguacil
    • 1
  • José A. Navarro-Cano
    • 3
  • José I. Querejeta
    • 1
  1. 1.Centro de Edafología y Biología Aplicada del Segura-Consejo Superior de Investigaciones Científicas (CEBAS-CSIC), Campus Universitario de EspinardoMurciaSpain
  2. 2.Isotope Bioscience Laboratory – ISOFYSGhent UniversityGhentBelgium
  3. 3.Centro de Investigaciones Sobre Desertificación (CSIC-UVEG-GV), Carretera Moncada - NáqueraMoncadaSpain

Personalised recommendations