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Different soil moisture conditions change the outcome of the ectomycorrhizal symbiosis between Rhizopogon species and Pinus muricata

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Abstract

The outcome of species interactions often depends on the environmental conditions under which they occur. In this study, we tested how different soil moisture conditions affected the outcome of the ectomycorrhizal symbiosis between three Rhizopogon species and Pinus muricata in a factorial growth chamber experiment. We found that when grown in 7% soil moisture conditions, ectomycorrhizal plants had similar biomass, photosynthesis, conductance, and total leaf nitrogen as non-mycorrhizal plants. However, when grown at 13% soil moisture, ectomycorrhizal plants had significantly greater shoot biomass, higher photosynthetic and conductance rates, and higher total leaf nitrogen than non-mycorrhizal plants. The differences in plant response by mycorrhizal status in the two soil moisture treatments corresponded with evidence of water limitation experienced by the fungi, which had much lower colonization at 7% compared to 13% soil moisture. Our results suggest that the outcome of the ectomycorrhizal symbiosis can be context-dependent and that fluctuating environmental conditions may strongly affect the way plants and fungi interact.

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References

  • 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

    Article  Google Scholar 

  • Bell TL, Adams MA (2004) Ecophysiology of ectomycorrhizal fungi associated with Pinus spp. In low rainfall areas of Western Australia. Plant Ecol 171:35–52

    Article  Google Scholar 

  • Bronstein JL (1994) Conditional outcomes of mutualistic interactions. Trends Eco Evol 9:214-217

    Article  Google Scholar 

  • 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 71:433–443

    Article  Google Scholar 

  • Coleman MD, Bledsoe CS, Lopushinsky W (1989) Pure culture response of ectomycorrhizal fungi to imposed water stress. Can J Bot 67:29–39

    Google Scholar 

  • Coleman MD, Bledsoe CS, Smit BA (1990) Root hydraulic conductivity and xylem sap levels of zeatin riboside and abscisic acid in ectomycorrhizal Douglas fir seedlings. New Phytol 115:275–284

    Article  CAS  Google Scholar 

  • Cushman JH, Whitham TG (1989) Conditional mutualism in a membracid-ant association: temporal, age-specific, and density-dependent effects. Ecology 70:1040–1047

    Article  Google Scholar 

  • Davies FT, Svenson SE, Cole JC, Phavaphutanon L, Duray SA, OlaldePortugal V, Meier CE, Bo SH (1996) Non-nutritional stress acclimation of mycorrhizal woody plants exposed to drought. Tree Physiol 16:985–993

    Google Scholar 

  • Dawson TE, Mambelli S, Plamboeck AH, Templer PH, Tu KP (2002) Stable isotopes in plant ecology. Ann Rev Ecol Evol S33:507–559

    Article  Google Scholar 

  • Dixon RK, Wright GM, Behrns GT, Teskey KO, Hinckley TM (1980) Water deficits and root growth of ectomycorrhizal white oak seedlings. Can J For Res 10:545–548

    Google Scholar 

  • 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 117:327–334

    Article  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 

  • Dunham AE (1980) An experimental study of interspecific competition between the iguanid lizards Sceloporus merriami ad Urosaurus ornatus. Eco Mono 50:309–330

    Article  Google Scholar 

  • Dunne JA, Parker VT (1999) Species-mediated soil moisture availability and patchy establishment of Pseudotsuga menziesii in chaparral. Oecologia 119:36–45

    Article  Google Scholar 

  • Dupponois R, Ba AM (1999) Growth stimulation of Acacia mangium Willd. By Pisolithus sp. in some Senegalese soils. For Eco Manage 119:209–215

    Article  Google Scholar 

  • Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Ann Rev Plant Biol 40:503–537

    Article  CAS  Google Scholar 

  • Gehring CA, Whitham TG (2002) Mycorrhizae–herbivore interactions: population and community consequences. In: van der Heijden MGA, Sanders IR (eds) Mycorrhizal ecology. Springer, New York, pp 295–320

  • Gehring CA, Mueller RC, Whitham TG (2006) Environmental and genetic effects on the formation of ectomycorrhizal and arbuscular mycorrhizal associations in cottonwoods. Oecologia 149:158–164

    Article  PubMed  Google Scholar 

  • Grubisha LC, Trappe JM, Molina R, Spatafora JW (2002) Biology of the ectomycorrhizal genus Rhizopogon VI Re-examination of infrageneric relationships inferred from phylogenetic analyses from phylogenetic analyses of ITS sequences. Mycologia 94:607–619

    Article  Google Scholar 

  • Hasselquist N, Germino MJ, McGonigle T, Smith WK (2005) Variability of Cenococcum colonization and its ecophysiological significant for young conifers at alpine-treeline. New Phytol 165:867–873

    Article  PubMed  Google Scholar 

  • Hobbie JE, Hobbie EA (2006) 15N in symbiotic fungi and plants estimates nitrogen and carbon flux rates in Artic tundra. Ecology 87:816–822

    PubMed  Google Scholar 

  • Horton TR, Cazaves E, Bruns TD (1998) Ectomycorrhizal, vesicular-arbuscular and dark septate fungal colonization of bishop pine (Pinus muricata) seedlings in the first five months of growth after wildfire. Mycorrhiza 8:11–18

    Article  Google Scholar 

  • Hutchinson GE (1961) The paradox of the plankton. Am Nat 93l:145–159

    Google Scholar 

  • Johnson NC (1997) Functioning of mycorrhizal associations along the mutualism-parasitism continuum. New Phyto 135:575–586

    Article  Google Scholar 

  • Jones MD, Durall DM, Tinker PB (1990) Phosphorus relationships and production of extramatrical hyphae by two types of willow ecto-mycorrhizas at different soil phosphorus levels. New Phytol 115:259–267

    Article  CAS  Google Scholar 

  • Jonsson LM, Marie-Charlotte N, Wardle DA, Zackrisson O (2001) Context dependent effects of ectomycorrhizal species richness on tree seedling productivity. Oikos 93:353–364

    Article  Google Scholar 

  • Kennedy PG, Bruns TD (2005) Priority effects determine the outcome of ectomycorrhizal competition between two Rhizopogon species colonizing Pinus muricata seedlings. New Phytol 166:631–638

    Article  PubMed  Google Scholar 

  • Kennedy PG, Sousa WP (2006) Forest encroachment into a Californian grassland: examining the simultaneous effects of facilitation and competition on tree seedling recruitment. Oecologia 148:464–474

    Article  PubMed  Google Scholar 

  • Lambers H, Chapin FS, Pons TL (1998) Plant physiological ecology. Springer-Verlag, New York

    Google Scholar 

  • Lansac AR, Martin A, Roldan A (1995) Mycorrhizal colonization and drought interactions of Mediterranean shrubs under greenhouse conditions. Arid Soil Res 9:167–175

    Google Scholar 

  • Lehto TH (1989) Effects of mycorrhiza and drought on photosynthesis and water relations of Sitka Spruce. Agr Ecosyst Environ 28:299–303

    Article  Google Scholar 

  • Lehto T (1992) Effect of drought on Picea sitchensis seedlings inoculated with mycorrhizal fungi. Scand J For Res 7:177–182

    Google Scholar 

  • Lilleskov EA, Bruns TD (2003) Root colonization dynamics of two ectomycorrhizal fungi of contrasting life history strategies are mediated by addition of organic nutrient patches. New Phytol 159:141–151

    Article  Google Scholar 

  • McCreadie JW, Beard CE, Adler PH (2005) Context-dependent symbiosis between black flies (Diptera: Simuliidae) and trichomycete fungi (Harpellales: Legeriomycetaceae). Oikos 108:362–370

    Article  Google Scholar 

  • Mexal J, Reid CPP (1973) Growth of selected mycorrhizal fungi in response to induced water stress. Can J Bot 51:1579–1588

    Article  Google Scholar 

  • Morte A, Diaz G, Rodriguez P, Alarcon JJ, Sanchez-Blanco MJ (2001) Growth and water relations in mycorrhizal and non-mycorrhizal Pinus halpensis plants in response to drought. Biol Plantarum 44:263–267

    Article  Google Scholar 

  • Nara K, Hogetsu T (2004) Ectomycorrhizal fungi on established shrubs facilitate subsequent seedling establishment of successional plant species. Ecology 85:1700–1707

    Google Scholar 

  • Nara K (2006) Ectomycorrhizal networks and seedling establishment during early primary succession. New Phytol 169:69–78

    Article  CAS  Google Scholar 

  • Nilsen P, Borja I, Knutsen H, Brean R (1998) Nitrogen and drought effects on ectomycorrhizae of Norway spruce [Picea abies L. (Karst.)]. Plant Soil 198:179–184

    Article  CAS  Google Scholar 

  • Park T (1954) Experimental studies of interspecies competition. II. Temperature, humidity, and competition in two species of Tribolium. Physiol Zool 27:177–238

    Google Scholar 

  • Parke J, Linderman R, Black C (1983) The role of ectomycorrhizas in drought tolerance of Douglas-fir seedlings. New Phytol 95:83–95

    Article  Google Scholar 

  • Parlade J, Cohen M, Doltra J, Luque J, Pera J (2001) Continuous measurement of stem-diameter growth response of Pinus pinea seedlings mycorrhizal with Rhizopogon roseolus and submitted to two water regimes. Mycorrhiza 11:129–136

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Quoreshi AM, Timmer VR (1998) Exponential fertilization increases nutrient uptake and ectomycorrhizal development of black spruce seedlings. Can J For Res 28:674–682

    Article  Google Scholar 

  • 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 9:559–569

    Article  Google Scholar 

  • Scheromm P, Plassard C, Salsac L (1990) Nitrate nutrition of maritime pine (Pinus pinaster Soland in Ait.) ecto-mycorrhizal with Hebeloma cylindrosporum Romagn. New Phytol 114:93–98

    Article  CAS  Google Scholar 

  • Shi LB, 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 12:303–311

    Article  PubMed  CAS  Google Scholar 

  • Simard SW, Jones MD, Durall DM (2002) Carbon and nutrient fluxes within and between mycorrhizal plants. In van der Heijden MGA, Sanders IR (eds) Mycorrhizal ecology. Springer, New York, pp 34–74

  • Smith SE, Read DJ (1997) Mycorrhizal symbiosis. Academic Press, New York

    Google Scholar 

  • 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 139:733–739

    Article  Google Scholar 

  • Swaty RL, Deckert RJ, Whitham TG, Gehring CA (2004) Ectomycorrhizal abundance and community composition shifts with drought: predictions from tree rings. Ecology 85:1072–1084

    Google Scholar 

  • Taylor DL, Bruns TD (1999) Community structure of ectomycorrhizal fungi in a Pinus muricata forest: minimal overlap between the mature forest and resistant propagule communities. Mol Eco 8:1837–1850

    Article  CAS  Google Scholar 

  • Theodorou C (1978) Soil-moisture and mycorrhizal association of Pinus radiata D. Don. Soil Biol Biochem 10:33–37

    Article  CAS  Google Scholar 

  • Treseder KK (2004) A meta-analysis of mycorrhizal responses to nitrogen, phosphorus, and atmospheric CO2 in field studies. New Phytol 164:347–355

    Article  Google Scholar 

  • Weber A, Karst J, Gilbert B, Kimmins JP (2005) Thuja plicata exclusion in ectomycorrhizal-dominated forests: testing the role of inoculum potential of arbuscular mycorrhizal fungi. Oecologia 143:148–156

    Article  PubMed  Google Scholar 

  • Wiens JA (1977) On competition in variable environments. Am Sci 65:590–597

    Google Scholar 

  • Worley JF, Hacskaylo E (1959) The effect of available soil moisture on the mycorrhizal association of Virginian pine. Forest Sci 5:267–268

    Google Scholar 

  • Zerova MY (1955) Mykorrhiza formation in forest trees of the Ukranian SSR. In: Imshenetskii A (ed) Mycotrophy in plants. USDA and NSF, Washington DC, pp 39–59

    Google Scholar 

  • Zhou M, Sharik TL (1997) Ectomycorrhizal associations of northern red oak (Quercus rubra) seedlings along a environmental gradient. Can J For Res 27:1705–1713

    Article  Google Scholar 

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Acknowledgments

We thank the Pt. Reyes National Seashore for use of their land; Tom Bruns, Todd Dawson, and Matteo Garbelotto for their advice and logistical support; C. Benneman for assistance with the growth chamber experiment; S. Mambelli for assistance with the isotopic analyses. M. Bidartondo and members of both the Bruns and Garbelotto labs at UC Berkeley for constructive criticism on earlier drafts of this manuscript. Financial support for this project was provided by a National Science Foundation doctoral dissertation improvement grant to P.G. Kennedy, T.D. Bruns, and W.P. Sousa (DEB 0309152), a National Parks Ecological Research Fellowship to P.G. Kennedy, and a NASA Earth Systems Science Fellowship to K.G. Peay.

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  1. Department of Plant and Microbial Biology, University of California at Berkeley, Berkeley, USA

    Peter G. Kennedy

  2. Department of Environmental Sciences, Policy & Management, University of California at Berkeley, 321 Koshland Hall, Berkeley, CA, 94720, USA

    Kabir G. Peay

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  1. Peter G. Kennedy
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Correspondence to Kabir G. Peay.

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Peter G. Kennedy and Kabir G. Peay contributed equally to this work and order was determined by a coin toss.

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Kennedy, P.G., Peay, K.G. Different soil moisture conditions change the outcome of the ectomycorrhizal symbiosis between Rhizopogon species and Pinus muricata . Plant Soil 291, 155–165 (2007). https://doi.org/10.1007/s11104-006-9183-3

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