Abstract
With large forested urban areas, the city of Edmonton, Alberta, Canada, faces high annual costs of replacing trees injured by deicing salts that are commonly used for winter road maintenance. Ectomycorrhizal fungi form symbiotic associations with tree roots that allow trees to tolerate the detrimental effects of polluted soils. Here, we examined mycorrhizal colonization of Pinus contorta by germinating seeds in soils collected from different locations: (1) two urban areas within the city of Edmonton, and (2) an intact pine forest just outside Edmonton. We then tested the responses of seedlings to 0-, 60-, and 90-mM NaCl. Our results showed lower abundance and diversity of ectomycorrhizal fungi in seedlings colonized with the urban soils compared to those from the pine forest soil. However, when subsequently exposed to NaCl treatments, only seedlings inoculated with one of the urban soils containing fungi from the genera Tuber, Suillus, and Wilcoxina, showed reduced shoot Na accumulation and higher growth rates. Our results indicate that local ectomycorrhizal fungi that are adapted to challenging urban sites may offer a potential suitable source for inoculum for conifer trees designated for plating in polluted urban environments.
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References
Bainard LD, Klironomos JN, Gordon AM (2011) The mycorrhizal status and colonization of 26 tree species growing in urban and rural environments. Mycorrhiza 21:91–96. https://doi.org/10.1007/s00572-010-0314-6
Belfiori B, Riccioni C, Tempesta S, Pasqualetti M, Paolocci F, Rubini A (2012) Comparison of ectomycorrhizal communities in natural and cultivated Tuber melanosporum truffle grounds. FEMS Microbiol Ecol 81:547–561. https://doi.org/10.1111/j.1574-6941.2012.01379.x
Bills RJ, Stutz JC (2009) AMF associated with indigenous and non-indigenous plants at urban and desert sites in Arizona. In: Azcón-Aguilar C, Barea J, Gianinazzi-Pearson V (eds) Mycorrhizas-functional processes and ecological impact. Springer, Berlin, Heidelberg, pp 207–220
Bois G, BigrasFJ BA, Piché Y, Fung MY, Khasa DP (2006a) Ectomycorrhizal fungi affect the physiological responses of Picea glauca and Pinus banksiana seedlings exposed to an NaCl gradient. Tree Physiol 26:1185–1196. https://doi.org/10.1093/treephys/26.9.1185
Bois G, Bertrand A, Piché Y, Fung M, Khasa DP (2006b) Growth, compatible solute and salt accumulation of five mycorrhizal fungal species grown over a range of NaCl concentrations. Mycorrhiza 16:99–109. https://doi.org/10.1007/s00572-005-0020-y
Branco S, Gladieux P, Ellison CE, Kuo A, LaButti K, Lipzen A, Grigoriev IV, Liao H-L, Vilgalys R, Peay G, Taylor JW, Bruns TD (2015) Genetic isolation between two recently diverged populations of a symbiotic fungus. Mol Ecol 24:2747–2758. https://doi.org/10.1111/mec.13132
Branco S, Bi K, Liao H-L, Gladieux P, Badouin H, Ellison CE, Nguyen NH, Vilgalys R, Peay KG, Taylor JW, Bruns TD (2017) Continental-level population differentiation and environmental adaptation in the mushroom Suillus brevipes. Mol Ecol 26:2063–2076. https://doi.org/10.1111/mec.13892
Brundrett M, Bougher N, Dell B, Grove T (1996) Working with mycorrhizas in forestry and agriculture. Australian Centre for International Agricultura Research, Canberra. https://doi.org/10.13140/2.1.4880.5444
Bücking H, Liepold E, Ambilwade P (2012) The role of the mycorrhizal symbiosis in nutrient uptake of plants and the regulatory mechanisms underlying these transport processes. In: Plant Science. InTechOpen. https://doi.org/10.5772/52570
Calfapietra C, Peñuelas J, Niinemets Ü (2015) Urban plant physiology: adaptation-mitigation strategies under permanent stress. Trends Plant Sci 20:72–75. https://doi.org/10.1016/j.tplants.2014.11.001
Calvo-Polanco M, Zwiazek JJ, Jones MD, MacKinnon MD (2008) Responses of mycorrhizal jack pine (Pinus banksiana) seedlings to NaCl and boron. Trees 22:825–834. https://doi.org/10.1007/s00468-008-0243-6
Calvo-Polanco M, Zwiazek JJ, Jones MD, MacKinnon MD (2009) Effects of NaCl on responses of ectomycorrhizal black spruce (Picea mariana), white spruce (Picea glauca) and jack pine (Pinus banksiana) to fluoride. Physiol Plant 135:51–61. https://doi.org/10.1111/j.1399-3054.2008.01170.x
Calvo-Polanco M, Señorans J, Zwiazek JJ (2012) Role of adventitious roots in water relations of tamarack (Larix laricina) seedlings exposed to flooding. BMC Plant Biol 12:99. https://doi.org/10.1186/1471-2229-12-99
Calvo-Polanco M, Sanchez-Romera B, Aroca R (2014) Mild salt stress conditions induce different responses in root hydraulic conductivity of Phaseolus vulgaris over-time. PLoS One 9(3):e90631. https://doi.org/10.1371/journal.pone.0090631
Cousins JR, Hope D, Gries C, Stutz JC (2003) Preliminary assessment of arbuscular mycorrhizal fungal diversity and community structure in an urban ecosystem. Mycorrhiza 13:319–326. https://doi.org/10.1007/s00572-003-0239-4
Critchfield WB, Little EL (1966) Geographic distribution of the pines of the world. No 991, US Department of Agriculture, Forest Service
Cullingham C, Cooke JEK, Coltman DW (2013) Effects of introgression on the genetic population structure of two ecologically and economically important conifer species: logepole pine (Pinus contorta var. latifolia) and jack pine (Pinus banksiana). Genome 56:577–585. https://doi.org/10.1139/gen-2013-0071
Deinlein U, Stephan AB, Horie T, Luo W, Xu G, Schroeder JI (2014) Plant salt-tolerance mechanisms. Trends Plant Sci 19:371–379. https://doi.org/10.1016/j.tplants.2014.02.001
Di B, Luoranen J, Lehto T, Himanen K, Silvennoinen M, Silvennoinen R, Repo T (2019) Biophysical changes in the roots of Scots pine seedlings during cold acclimation and after frost damage. Forest Ecol Man 431:63–72. https://doi.org/10.1016/j.foreco.2018.04.008
Dixon RK, Rao MV, Garg VK (1993) Salt stress affects in vitro growth and in situ symbioses of ectomycorrhizal fungi. Mycorrhiza 3:63–68. https://doi.org/10.1007/BF00210694
Epstein E, Bloom A (2005) Inorganic components of plants. In: Epstein E, Bloom AJ (eds) Mineral nutrition of plants: principles and perspectives, 2nd edn. Sinauer Associates, Sunderland, Massachusetts, pp 44–45
Equiza MA, Calvo-Polanco M, Cirelli D, Señorans J, Wartenbe M, Saunders C, Zwiazek JJ (2017) Long-term impact of road salt (NaCl) on soil and urban trees in Edmonton, Canada. Urban For Urban Green 21:16–28. https://doi.org/10.1016/j.ufug.2016.11.003
Fay L, Shi X (2012) Environmental impacts of chemicals for snow and ice control: state of the knowledge. Water Air Soil Pollut 223:2751–2770. https://doi.org/10.1007/s11270-011-1064-6
Flowers TJ, Munns R, Colmer TD (2015) Sodium chloride toxicity and the cellular basis of salt tolerance in halophytes. Ann Bot 115:419–431. https://doi.org/10.1093/aob/mcu217
Franklin JA, Zwiazek JJ (2004) Ion uptake in Pinus banksiana treated with sodium chloride and sodium sulphate. Physiol Plant 120:482–490. https://doi.org/10.1111/j.0031-9317.2004.00246.x
Gaster J, Karst J, Landhäusser SM (2015) The role of seedling nutrient status on development of ectomycorrhizal fungal communities in two soil types following surface mining disturbance. Pedobiologia 58:129–135. https://doi.org/10.1016/j.pedobi.2015.07.001
Goodman D, Durall D, Trofymow T, Berch S (1996) A manual of concise descriptions of North American ectomycorrhizae including microscopic and molecular characterization. Natural Resources Canada, Canadian Forestry Service, Victoria, BC
Hrynkiewicz K, Szymańska S, Piernik A, Thiem D (2015) Ectomycorrhizal community structure of Salix and Betula spp. at a saline site in Central Poland in relation to the seasons and soil parameters. Water Air Soil Pollut 226:99. https://doi.org/10.1007/s11270-015-2308-7
Hui N, Liu X, Kotze DJ, Jumpponen A, Francini G, Setälä H (2017) Ectomycorrhizal fungal communities in urban parks are similar to those in natural forests but shaped by vegetation and park age. Appl Environ Microbiol 83:e01797–e01717. https://doi.org/10.1128/AEM.01797-17
Izzo A, Canright M, Bruns TD (2006) The effects of heat treatments on ectomycorrhizal resistant propagules and their ability to colonize bioassay seedlings. Mycol Res 110:196–202. https://doi.org/10.1016/j.mycres.2005.08.010
Jonsson L, Dahlberg A, Nilsson M-C, Zackrisson O, Ola K (1999) Ectomycorrhizal fungal communities in late-successional Swedish boreal forests, and their composition following wildfire. Mol Ecol 8:205–215. https://doi.org/10.1046/j.1365-294x.1999.00553.x
Karpati AS, Handel SN, Dighton J, Horton TR (2011) Quercus rubra-associated ectomycorrhizal fungal communities of disturbed urban sites and mature forests. Mycorrhiza 21:537–547. https://doi.org/10.1007/s00572-011-0362-6
Kennedy P (2010) Ectomycorrhizal fungi and interspecific competition: species interactions, community structure, coexistence mechanisms, and future research directions. New Phytol 187:895–910. https://doi.org/10.1111/j.1469-8137.2010.03399.x
Korhonen A, Lehto T, Heinonen J, Repo T (2018) Whole-plant frost hardiness of mycorrhizal (Hebeloma sp. or Suillus luteus) and non-mycorrhizal Scots pine seedlings. Tree Physiol tpy105. https://doi.org/10.1093/treephys/tpy105
Langenfeld-Heyser R, Gao J, Ducic T, Tachd P, Lu CF, Fritz E, Gafur A, Polle A (2007) Paxillus involutus mycorrhiza attenuate NaCl-stress responses in the salt-sensitive hybrid poplar Populus x canescens. Mycorrhiza 17:121–131. https://doi.org/10.1007/s00572-006-0084-3
Lee EH, Eom AH (2013) Ectomycorrhizal fungal communities of red pine (Pinus densiflora) seedlings in disturbed sites and undisturbed old forest sites. Mycobiol 41:77–81. https://doi.org/10.5941/MYCO.2013.41.2.77
Lee SH, Calvo-Polanco M, Chung GC, Zwiazek JJ (2010) Role of aquaporins in root water transport of ectomycorrhizal jack pine (Pinus banksiana) seedlings exposed to NaCl and fluoride. Plant Cell Environ 33:769–780. https://doi.org/10.1111/j.1365-3040.2009.02103.x
Lehto T (1992) Mycorrhizas and drought resistance of Picea sitchensis (Bong.) Carr. New Phytol 122:661–668. https://doi.org/10.1111/j.1469-8137.1992.tb00094.x
Ma X, Sun M, Sa G, Zhang Y, Li J, Sun J, Shen X, Polle A, Chen S (2014) Ion fluxes in Paxillus involutus-inoculated roots of Populus canescens under saline stress. Environ Exp Bot 108:99–108. https://doi.org/10.1016/j.envexpbot.2013.11.016
Mah K, Tackaberry L, Egger KN, Massicotte HB (2001) The impacts of broadcast burning after clear-cutting on the diversity of ectomycorrhizal fungi associated with hybrid spruce seedlings in Central British Columbia. Can J For Res 31:224–235. https://doi.org/10.1139/cjfr-31-2-224
Martin KJ, Rygiewicz PT (2005) Fungal-specific PCR primers developed for analysis of the ITS region of environmental DNA extracts. BMC Microbiol 5:28. https://doi.org/10.1186/1471-2180-5-28
Muhsin TM, Zwiazek JJ (2002) Colonization with Hebeloma crustuliniforme increases water conductance and limits shoot sodium uptake in white spruce (Picea glauca) seedlings. Plant Soil 238:217–225. https://doi.org/10.1023/a:1014435407735
Nara K (2006) Ectomycorrhizal networks and seedling establishment during early primary succession. New Phytol 169:169–178. https://doi.org/10.1111/j.1469-8137.2005.01545.x
Nehls U, Göhringer F, Wittulsky S, Dietz S (2010) Fungal carbohydrate support in the ectomycorrhizal symbiosis: a review. Plant Biol 12:292–301. https://doi.org/10.1111/j.1438-8677.2009.00312.x
Newbound M, McCarthy MA, Lebel T (2010) Fungi and the urban environment: a review. Landsc Urban Plan 96:138–145. https://doi.org/10.1016/j.landurbplan.2010.04.005
Nguyen H, Calvo-Polanco M, Zwiazek JJ (2006) Gas exchange and growth responses of ectomycorrhizal Picea mariana, Picea glauca, and Pinus banksiana seedlings to NaCl and Na2SO4. Plant Biol 8:646–652. https://doi.org/10.1055/s-2006-924106
Obase K, Lee JK, Lee SK, Lee SY, Chun KW (2010) Variation in sodium chloride resistance of Cenococcum geophilum and Suillus granulatus isolates in liquid culture. Mycobiol 38:225–228. https://doi.org/10.4489/MYCO.2010.38.3.225
Onwuchekwa NE, Zwiazek JJ, Quoreshi A, Khasa DP (2014) Growth of mycorrhizal jack pine (Pinus banksiana) and white spruce (Picea glauca) seedlings planted in oil sands reclaimed areas. Mycorrhiza 24:431–441. https://doi.org/10.1007/s00572-014-0555-x
Ordóñez-Barona C, Sabetski V, Millward AA, Steenberg J (2018) De-icing salt contamination reduces urban tree performance in structural soil cells. Environ Pollut 234:562–571. https://doi.org/10.1016/j.envpol.2017.11.101
Parladé J, Álvarez IF, Pera J (1995) Ability of native ectomycorrhizal fungi from northern Spain to colonize Douglas-fir and other introduced conifers. Mycorrhiza 6:51–55. https://doi.org/10.1007/s005720050105
Quoreshi AM, Khasa DP (2008) Effectiveness of mycorrhizal inoculation in the nursery on root colonization, growth, and nutrient uptake of aspen and balsam poplar. Biomass Bioenergy 32:381–391. https://doi.org/10.1016/j.biombioe.2007.10.010
Renault S, Paton E, Nilsson G, Zwiazek JJ, MacKinnon MD (1999) Responses of boreal plants to high salinity oil sands tailings water. J Environ Qual 28:1957–1962. https://doi.org/10.2134/jeq1999.00472425002800060035x
Šesták Z, Catský J, Jarvis PG (1971) Plant photosynthetic production. Manual of methods. Dr W Junk NV, The Hague
Siemens JA, Zwiazek JJ (2008) Root hydraulic properties and growth of balsam poplar (Populus balsamifera) mycorrhizal with Hebeloma crustuliniforme and Wilcoxina mikolae var. mikolae. Mycorrhiza 18:393–401. https://doi.org/10.1007/s00572-008-0193-2
Stabler LB, Martin CA, Stutz JC (2001) Effect of urban expansion on arbuscular mycorrhizal fungal mediation of landscape tree growth. J Arboric 27:193–202
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 Ecol 8: 1837–1850.4. https://doi.org/10.1046/j.1365-294x.1999.00773.x
Tedersoo L, Suvi T, Jairus T, Kõljalg U (2008) Forest microsite effects on community composition of ectomycorrhizal fungi on seedlings of Picea abies and Betula pendula. Environ Microbiol 10:1189–1201. https://doi.org/10.1111/j.1462-2920.2007.01535.x
Timonen S, Kauppinen P (2008) Mycorrhizal colonisation patterns of Tilia trees in street, nursery and forest habitats in southern Finland. Urban For Urban Green 7:265–276. https://doi.org/10.1016/j.ufug.2008.08.001
Yi H, Calvo-Polanco M, MacKinnon MD, Zwiazek JJ (2008) Responses of ectomycorrhizal Populus tremuloides and Betula papyrifera seedlings to salinity. Environ Exp Bot 62:357–363. https://doi.org/10.1016/j.envexpbot.2007.10.008
Acknowledgments
We gratefully acknowledge research funding from the city of Edmonton, Mr. Tim Ford (city of Edmonton Planning) for his help regarding site descriptions, and Dr. J.Y. Jang for her help with root tips DNA extraction. We also acknowledge Dr. Henryk Kolacz from the Department of Mathematical and Statistical Sciences of the University of Alberta, for his help with statistical analyses.
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M.C-P. and J.S. performed the experimental work. The study was designed and written by J.J-Z and M.C-P, with contributions from M.A-E, J.K., M.W., and C.S.
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Zwiazek, J.J., Equiza, M.A., Karst, J. et al. Role of urban ectomycorrhizal fungi in improving the tolerance of lodgepole pine (Pinus contorta) seedlings to salt stress. Mycorrhiza 29, 303–312 (2019). https://doi.org/10.1007/s00572-019-00893-3
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DOI: https://doi.org/10.1007/s00572-019-00893-3