Abstract
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.
Methods
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.
Results
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.
Conclusions
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.
Similar content being viewed by others
References
Agerer R (ed) (1987–2006) Colour Atlas of Ectomycorrhizae. Einhorn-Verlag, Schwäbisch Gmünd
Agerer R (2001) Exploration types of ectomycorrhizae. Mycorrhiza 11:107–114
Allison GB, Barnes CJ, Hughes MW (1983) The distribution of deuterium and 18O in dry soils 2. Experimental. J Hydrol 64:377–397
Amaranthus MP, Perry D (1989) Rapid root tip and mycorrhiza formation and increased survival of Douglas-fir seedlings after soil transfer. New Forest 3:259–264
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 168:11–22
Augé RM (2004) Arbuscular mycorrhizae and soil/plant water relations. Can J Soil Sci 84:373–381
Augé RM, Stodola AJW, Tims JE, Saxton AM (2001) Moisture retention properties of a mycorrhizal soil. Plant Soil 230:87–97
Bardgett RD (1991) The use of the membrane filter technique for comparative measurements of hyphal lengths in different grassland sites. Agr Ecosyst Environ 34:115–119
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 31:177–186
Bingham MA, Simard S (2012) Ectomycorrhizal networks of Pseudotsuga menziesii var. glauca trees facilitate establishment of conspecific seedlings under drought. Ecosystems 15:188–199
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 267:213–223
Booth MG, Hoeksema JD (2010) Mycorrhizal networks counteract competitive effects of canopy trees on seedling survival. Ecology 91:2294–2302
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 22:1107–1117
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 71:433–443
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 320:37–77
Caldwell MM, Richards JH (1989) Hydraulic lift: water efflux from upper roots improves effectiveness of water uptake by deep roots. Oecologia 79:1–5
Caldwell MM, Dawson TE, Richards JH (1998) Hydraulic lift: consequences of water efflux from the roots of plants. Oecologia 113:151–161
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 110:18988–18993
Dawson TE (1993) Hydraulic lift and water use by plants: implications for water balance, performance, and plant–plant interactions. Oecologia 95:565–574
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 16:263–272
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 187:171–183
Duddridge JA, Malibari A, Read DJ (1980) Structure and function of mycorrhizal rhizomorphs with special reference to their role in water transport. Nature 287:834–836
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 58:1473–1483
Egerton-Warburton LM, Querejeta JI, Allen MF (2008) Efflux of hydraulically lifted water from mycorrhizal fungal hyphae during imposed drought. Plant Signal Behav 3:68–71
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 281–300
Eissenstat DM (1991) On the relationship between specific root length and the rate of root proliferation: a field study using citrus rootstocks. New Phytol 118:63–68
Filella I, Peñuelas J (2003) Indications of hydraulic lift by Pinus halepensis and its effects on the water relations of neighbour shrubs. Biol Plantarum 47:209–214
Flanagan LB, Ehleringer JR (1991) Stable isotope composition of stem and leaf water: applications to the study of plant water use. Funct Ecol 5:270–277
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 36:1213–1221
Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes—application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118
Grand LF, Harvey AE (1982) Quantitative measurements of ectomycorrhizae on plant roots. methods and principles of mycorrhizal research. Am Phytopathol Soc, St Paul
Hoagland DR, Arnon DI (1950) The water-culture method of growing plants without soil. Calif Aes Bull 347:31
Huang B, Eissenstat DM (2000) Linking hydraulic conductivity to anatomy in plants that vary in specific root length. J Am Soc Hortic Sci 125:260–264
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 173:313–321
Kummerow J, Krause D, Jow W (1978) Seasonal changes of fine root density in the Southern Californian chaparral. Oecologia 37:201–212
Lehto T, Zwiazek J (2011) Ectomycorrhizas and water relations of trees: a review. Mycorrhiza 21:71–90
Maestre FT, Cortina J (2004) Are Pinus halepensis plantations useful as a restoration tool in semiarid Mediterranean areas? For Ecol Manag 198:303–317
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 222:258–268
Muhsin TM, Zwiazek JJ (2002) Ectomycorrhizas increase apoplastic water transport and hydraulic conductivity in Ulmus americana seedlings. New Phytol 153:153–158
Plamboeck AH, Dawson TE, Egerton-Warburton LE, North M, Bruns TD, Querejeta JI (2007) Water transfer via ectomycorrhizal fungal hyphae to conifer seedlings. Mycorrhiza 17:439–447
Prieto I, Ryel RJ (2014) Internal hydraulic redistribution prevents the loss of root conductivity during drought. Tree Physiol 34:39–48
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 13:181–187
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 193:830–841
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 149:115–128
Querejeta JI, Egerton-Warburton LM, Allen MF (2003) Direct nocturnal transfer from oaks to their mycorrhizal symbionts during severe soil drying. Oecologia 134:55–64
Querejeta JI, Egerton-Warburton LM, Allen MF (2009) Topographic position modulates the mycorrhizal response of oak trees to interannual rainfall variability. Ecology 90:649–662
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 355:63–73
Richter H (1997) Water relations of plants in the field: some comments on the measurement of selected parameters. J Exp Bot 48:1–7
Roberts J (1976) A study of root distribution and growth in a Pinus sylvestris L. (Scots Pine) plantation in East Anglia. Plant Soil 44:607–621
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 154:455–466
Sylvia DM (1992) Quantification of external hyphae of vesicular-arbuscular mycorrhizal fungi. Method Microbiol 24:53–65
Tennant D (1975) A test of the modified root intersect method of estimating root length. J Ecol 63:995–1001
Teste F, Simard S (2008) Mycorrhizal networks and distance from mature trees alter patterns of competition and facilitation in dry Douglas-fir forests. Oecologia 158:193–203
Teste F, Karst J, Jones MD, Simard S, Durall DM (2006) Methods to control ectomycorrhizal colonization: effectiveness of chemical and physical barriers. Mycorrhiza 17:51–65
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 41:437–443
Torres P, Honrubia M (1994) Ectomycorrhizal associations proven for Pinus halepensis. Israel J Plant Sci 42:51–58
Unestam T (1991) Water repellency, mat formation and leaf-stimulated growth of some ectomycorrhizal fungi. Mycorrhiza 1:13–20
Unestam T, Sun YP (1995) Extramatrical structures of hydrophobic and hydrophilic ectomycorrhizal fungi. Mycorrhiza 5:301–311
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 178:382–394
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. 315–322
Acknowledgments
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).
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Thom W. Kuyper.
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(DOCX 931 kb)
Rights and permissions
About this article
Cite this article
Prieto, I., Roldán, A., Huygens, D. et al. Species-specific roles of ectomycorrhizal fungi in facilitating interplant transfer of hydraulically redistributed water between Pinus halepensis saplings and seedlings. Plant Soil 406, 15–27 (2016). https://doi.org/10.1007/s11104-016-2860-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-016-2860-y