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

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.

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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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Augé RM (2004) Arbuscular mycorrhizae and soil/plant water relations. Can J Soil Sci 84:373–381

    Article  Google Scholar 

  • Augé RM, Stodola AJW, Tims JE, Saxton AM (2001) Moisture retention properties of a mycorrhizal soil. Plant Soil 230:87–97

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Bingham MA, Simard S (2012) Ectomycorrhizal networks of Pseudotsuga menziesii var. glauca trees facilitate establishment of conspecific seedlings under drought. Ecosystems 15:188–199

    CAS  Article  Google Scholar 

  • 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

    CAS  Article  Google Scholar 

  • Booth MG, Hoeksema JD (2010) Mycorrhizal networks counteract competitive effects of canopy trees on seedling survival. Ecology 91:2294–2302

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    CAS  Article  Google Scholar 

  • Caldwell MM, Richards JH (1989) Hydraulic lift: water efflux from upper roots improves effectiveness of water uptake by deep roots. Oecologia 79:1–5

    Article  Google Scholar 

  • Caldwell MM, Dawson TE, Richards JH (1998) Hydraulic lift: consequences of water efflux from the roots of plants. Oecologia 113:151–161

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    CAS  Article  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    CAS  Article  PubMed  Google Scholar 

  • Grand LF, Harvey AE (1982) Quantitative measurements of ectomycorrhizae on plant roots. methods and principles of mycorrhizal research. Am Phytopathol Soc, St Paul

    Google Scholar 

  • Hoagland DR, Arnon DI (1950) The water-culture method of growing plants without soil. Calif Aes Bull 347:31

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Kummerow J, Krause D, Jow W (1978) Seasonal changes of fine root density in the Southern Californian chaparral. Oecologia 37:201–212

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Maestre FT, Cortina J (2004) Are Pinus halepensis plantations useful as a restoration tool in semiarid Mediterranean areas? For Ecol Manag 198:303–317

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Prieto I, Ryel RJ (2014) Internal hydraulic redistribution prevents the loss of root conductivity during drought. Tree Physiol 34:39–48

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    CAS  Article  Google Scholar 

  • Richter H (1997) Water relations of plants in the field: some comments on the measurement of selected parameters. J Exp Bot 48:1–7

    CAS  Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Sylvia DM (1992) Quantification of external hyphae of vesicular-arbuscular mycorrhizal fungi. Method Microbiol 24:53–65

    Article  Google Scholar 

  • Tennant D (1975) A test of the modified root intersect method of estimating root length. J Ecol 63:995–1001

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Torres P, Honrubia M (1994) Ectomycorrhizal associations proven for Pinus halepensis. Israel J Plant Sci 42:51–58

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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

    CAS  Article  PubMed  Google Scholar 

  • 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

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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).

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Correspondence to José I. Querejeta.

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Responsible Editor: Thom W. Kuyper.

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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

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Keywords

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