Abstract
Little is known about water transfer via mycorrhizal hyphae to plants, despite its potential importance in seedling establishment and plant community development, especially in arid environments. Therefore, this process was investigated in the study reported in this paper in laboratory-based tripartite mesocosms containing the shrub Arctostaphylos viscida (manzanita) and young seedlings of sugar pine (Pinus lambertiana) and Douglas-fir (Pseudotsuga menziesii). The objectives were to determine whether water could be transported through mycorrhizal symbionts shared by establishing conifers and A. viscida and to compare the results obtained using two tracers: the stable isotope deuterium and the dye lucifer yellow carbohydrazide. Water containing the tracers was added to the central compartment containing single manzanita shrubs. The fungal hyphae were then collected as well as plant roots from coniferous seedlings in the other two compartments to determine whether water was transferred via fungal hyphae. In addition, the length of the hyphae and degree of mycorrhizal colonisation were determined. Internal transcribed spacer–restriction fragment length polymorphism (ITS-RFLP) analysis was used to identify the fungal species involved in dye (water) transfer. Results of the stable isotope analysis showed that water is transferred via mycorrhizal hyphae, but isotopically labelled water was only detected in Douglas-fir roots, not in sugar pine roots. In contrast, the fluorescent dye was transported via mycorrhizal hyphae to both Douglas-fir and sugar pine seedlings. Only 1 of 15 fungal morphotypes (identified as Atheliaceae) growing in the mesocosms transferred the dye. Differences were detected in the water transfer patterns indicated by the deuterium and fluorescent dye tracers, suggesting that the two labels are transported by different mechanisms in the same hyphae and/or that different fungal taxa transfer them via different routes to host plants. We conclude that both tracers can provide information on resource transfer between fungi and plants, but we cannot be sure that the dye transfer data provide accurate indications of water transfer rates and patterns. The isotopic tracer provides more direct indications of water movement and is therefore more suitable than the dye for studying water relations of plants and their associated mycorrhizal fungi.
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References
Acsai J, Largent D (1983) Mycorrhizae of Arbutus menziesii Pursh., and Arctostaphylos manzanita parry in northern California. Mycotaxon 16:519–536
Agerer R (1986–1998) Colour atlas of ectomycorrhizae. Munich, Germany, Einhorn-Verlag
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 11:107–114
Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST—a new generation of protein database search programs. Nucleic Acids Res 25(17):3389–3402
Anderson PD, Helms JA (1994) Tissue water relations of Pinus ponderosa and Arctostaphylos patula exposed to various levels of soil moisture depletion. Can J For Res 24:1495–1505
Ashford AE, Allaway WG, Cairney JW (1989) Nutrient transfer and the fungus-root interface. Aust J Plant Physiol 16:85–87
Barker SJ, Tagu D, Delp G (1998) Regulation of root and fungal morphogenesis in mycorrhizal symbioses. Plant Physiol 116:1201–1207
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 forming inter-plant connections and providing pathways for assimilate and water transport. Plant Soil 71:43–443
Dawson TE, Mambelli S, Plamboeck AH, Templer PH, Tu KP (2002) Stable isotopes in plant ecology. Ann Rev Ecolog Syst 33:507–559
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
Dunne JA, Parker VT (1999) Species-mediated soil moisture availability and patchy establishment of Pseudotsuga Menziesii in chaparral. Oecologia 119:35–45
Ehleringer JR, Roden J, Dawson TE (2000) Assessing ecosystem-level water relations through stable isotope ratio analyses. In: Sala OE, Jackson RB, Mooney HA, Howarth RW (eds) Methods in ecosystem science. Springer, New York, pp 181–198
Ek H, Andersson S, Arnebrant K, Söderström B (1994) Growth and assimilation of \( {\text{NH}}^{ + }_{4} \) and \( {\text{NO}}^{ - }_{3} \) by Paxillus involutus in association with Betula pendula and Picea abies as affected by substrate pH. New Phytol 128:629–637
Finlay RD, Read DJ (1986a) The structure and function of the vegetative mycelium of ectomycorrhizal plants. I. Translocation of 14C-löabeled carbon between plants interconnected by a common mycelium. New Phytol 103:143–156
Finlay RD, Read DJ (1986b) The structure and function of the vegetative mycelium of ectomycorrhizal plants. II. The uptake and distribution of phosphorus by mycelium interconnecting host plants. New Phytol 103:157–165
Finlay RD, Ek H, Odham G, Söderström B (1989) Uptake, translocation and assimilation of nitrogen from 15N-labelled ammonium and nitrate sources by intact ectomycorrhizal systems of Fagus sylvatica infected with Paxillus involutus. New Phytol 113:47–55
Fitter AH, Graves JD, Watkins NK, Robinson D, Scrimgeour C (1998) Carbon transfer between plants and its control in networks of arbuscular mycorrhizas. Funct Ecol 12:406–412
Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes-application to the identification of mycorrhizae and rust. Mol Ecol 2:113–118
Hanssen JF, Thingstad TF, Goksoyr J (1974) Evaluation of hyphal lengths and fungal biomass in soil by a membrane filter technique. Oikos 25:102–107
Harley JL, Smith SE (1983) Mycorrhizal symbiosis. Academic, London, UK
Horton TR, Bruns TD, Parker VT (1999) Ectomycorrhizal fungi associated with Arctostaphylos contribute to Pseudotsuga menziesii establishment. Can J Bot 77:93–103
Krajinski F, Biela A, Schubert D, Gianinazzi-Pearson V, Kaldenhoff R, Franken P (2000) Arbuscular mycorrhiza development regulates the mRNA abundance of Mtaqp1 encoding a mercury-insensitive aquaporin in Medicago truncatula. Planta 211:85–90
Lamhamedi MS, Bernier PY, Fortin JA (1992) Hydraulic conductance and soil water potential at the soil-root interface of Pinus pinaster seedlings inoculated with different dikaryons of Pisolithus sp. Tree Physiol 10:231–244
Lerat S, Gauci R, Catford JG, Vierheilig H, Piche Y, Lapointe L (2002) C-14 transfer between the spring ephemeral Erythronium americanum and sugar maple saplings via arbuscular mycorrhizal fungi in natural stands. Oecologia 132(2):181–187
Melin E, Nilsson H (1950) Transfer of radioactive phosphorus to pine seedlings by means of mycorrhizal hyphae. Physiol Plant 3:88–92
Molina R, Trappe JM (1982) Lack of mycorrhizal specificity by the ericaceous hosts Arbutus menziesii and Arctostaphylos uva-ursi. New Phytol 90:485–509
Newman EI (1988) Mycorrhizal links between plants: their functioning and ecological significance. Adv Ecol Res 18:243–270
Parker VT, Vasey MC, Keeley JE (2007) Taxonomic revisions in the genus Arctostaphylos (Ericaceae). Madroño (in press)
Peterson CA, Murrmann M, Steudle E (1993) Location of major barriers to water and ion movement in young roots of Zea mays L. Planta 190:127–136
Perry DA, Amaranthus MP, Borchers JG, Borchers SL, Brainerd RE (1989) Bootstrapping in ecosystems. BioScience 39:230–237
Querejeta JI, Egerton-Warburton LM, Allen MF (2003) Direct nocturnal water transfer from oaks to their mycorrhizal symbionts during severe soil drying. Oecologia 134:55–64
Read DJ, Francis R, Finlay RD (1985) Mycorrhizal mycelia and nutrient cycling in plant communities. In: Fitter AH (ed) Ecological interaction in soil. Blackwell, Oxford, UK, pp 193–217
Rousseau JVD, Sylvia DM, Fox AJ (1994) Contribution of ectomycorrhiza to the potential nutrient-absorbing surface of pine. New Phytol 128:639–644
Royce EB, Barbour MG (2001) Mediterranean climate effects. I. Conifer water use across a Sierra Nevada ecotone. Am J Bot 88:911–918
Simard SW, Jones MD, Durall DM, Perry DA, Myrold DD, Molina R (1997a) Reciprocal transfer of carbon isotopes between ectomycorrhizal Betula papyrifera and Pseudotsuga menziesii. New Phytol 137:529–542
Simard SW, Perry DA, Jones MD, Myrold DD, Durall DM, Molina R (1997b) Net transfer of carbon between ectomycorrhizal tree species in the field. Nature 388:579–582
Smith SE, Read DJ (1997) Mycorrhizal symbiosis, 2nd edn. Academic, London, UK
Steudle E (2000a) Water uptake by roots: effects of water deficits. J Exp Bot 51:1531–1542
Steudle E (2000b) Water uptake by roots: an integration of views. Plant Soil 226:45–56
Steudle E, Murrman M, Peterson CA (1993) Transport of water and solutes across maize roots modified by puncturing the endodermis. Further evidence for the composite transport model of the root. Plant Physiol 103:335–349
Tennant D (1975) A test of a modified line intersect method of estimating root length. J Ecol 63:995–1001
Watkins NK, Fitter AH, Graves JD, Robinson D (1996) Carbon transfer between C-3 and C-4 plants linked by a common mycorrhizal network, quantified using stable carbon isotopes. Soil Biol Biochem 28:471–477
White TJ, Bruns TD, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gefland DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to method and applications. Academic, San Diego, CA, USA, pp 315–322
Zak B (1976) Pure culture synthesis of bearberry mycorrhizae. Can J Bot 54:1297–1305
Acknowledgements
Financial support was provided by the Swedish Foundation for International Cooperation in Research and Higher Education, STINT (Dnr 99/666), the University of California, The A.W. Mellon Foundation and the National Science Foundation (DEB 9981548). We thank Drs. Antonio Izzo and Martin Bidartondo for the help and advice they provided through the DNA work, Professor V. Tom Parker for his feedback on many aspects of this investigation and Dr. Andy Taylor for valuable comments on the manuscript.
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Plamboeck, A.H., Dawson, T.E., Egerton-Warburton, L.M. et al. Water transfer via ectomycorrhizal fungal hyphae to conifer seedlings. Mycorrhiza 17, 439–447 (2007). https://doi.org/10.1007/s00572-007-0119-4
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DOI: https://doi.org/10.1007/s00572-007-0119-4