Abstract
Arbuscular mycorrhizal fungi (AMF) form probably the most widespread symbiosis on earth and are found across all ecosystems including the Arctic regions. In the Arctic, the prevalent harsh cold conditions experienced by both host plants and fungi may have selected for AMF species with long-surviving spores, the principal means for dispersal and survival. However, basic knowledge about their viability is lacking. AMF spore assembly from two Arctic sites was examined in soil samples collected across an 11-year period and stored at −20 °C for up to 10 years. AMF spore viability and ability to colonize plants were investigated in the greenhouse using Plantago lanceolata. It was predicted that Arctic AMF spores would survive in cold conditions for several years, with an expected decrease in viability over time as suggested by other experiments with temperate material. Results show that even though the two study sites differed in AMF spore density, the relative abundance of spore morphotypes was rather similar across sites and years. Furthermore, spore viability over time was site-dependent as it decreased only in one site. Although spores were viable, only a very small proportion of hosts and roots became colonized in the greenhouse even 21 months after inoculation. Taken together, these results suggest a certain site-dependent variability in AMF spore communities and the ability of Arctic AMF spores to remain viable after a long-term storage in cold conditions. The lack of host colonization in the greenhouse may be related to the inability to overcome spore dormancy under these conditions.
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References
Adams BJ, Wall DH, Virginia RA, Broos E, Knox MA (2014) Ecological biogeography of the terrestrial nematodes of Victoria Land, Antarctica. Zoo Keys 419:29–71
An Z-Q, Hendrix JW (1988) Determining viability of endogonaceous spores with a vital stain. Mycologia 80:259–261
An Z-Q, Guo BZ, Hendrix JW (1998) Viability of soilborne spores of glomalean mycorrhizal fungi. Soil Biol Biochem 30:1133–1136
Belay Z, Vestberg M, Assefa F (2013) Diversity and abundance of arbuscular mycorrhizal fungi associated with acacia tress from different land use systems in Ethiopia. Afr J Microbiol Res 7:5503–5515
Bever JD, Morton JB, Antonovics J, Schultz PA (1996) Host-dependent sporulation and species diversity of arbuscular mycorrhizal fungi in a mown grassland. J Ecol 84:71–82
Bliss LC (1981) The evolution and characteristics of tundra. In: Bliss LC, Heal OW, Moore JJ (eds) Evolution of tundra ecosystems. Cambridge University Press, Cambridge, pp 5–7
Chapin FS III, Körner C (1995) Patterns, causes, changes and consequences of biodiversity in arctic and alpine ecosystems. In: Chapin FS III, Körner C (eds) Arctic and alpine biodiversity: patterns, causes and ecosystem consequences. Springer, Berlin, pp 313–320
Coulson SJ, Hodkinson ID, Strathdee AT, Block W, Webb NR, Bale JS, Worland MR (1995) Thermal environments of Arctic soil organisms during winter. Arct Alp Res 27:364–370
Dalpé Y, Aiken SG (1998) Arbuscular mycorrhizal fungi associated with Festuca species in the Canadian high Arctic. Can J Bot 76:1930–1938
Daniels BA, Trappe JM (1980) Factors affecting spore germination of the vesicular–arbuscular mycorrhizal fungus, Glomus epigaeus. Mycologia 72:457–471
Douds DD, Schenck NC (1990) Cryopreservation of spores of vesicular–arbuscular mycorrhizal fungi. New Phytol 115:667–674
Fitter AH, Garbaye J (1994) Interactions between mycorrhizal fungi and other soil organisms. Plant Soil 159:123–132
Francini G, Männistö M, Alaoja V, Kytöviita M-M (2014) Arbuscular mycorrhizal fungal community divergence within a common host plant in two different soils in a subarctic Aeolian sand area. Mycorrhiza 24:539–550
Gemma JN, Koske RE (1988) Seasonal variation in spore abundance and dormancy of Gigaspora gigantea and in mycorrhizal inoculum potential of a dune soil. Mycologia 80:211–216
Gerdemann JW (1965) Vesicular-arbuscular mycorrhizae formed on maize and tulip tree by Endogone fasciculata. Mycologia 57:562–575
Gerdemann JW, Nicolson TH (1963) Spores of mycorrhizal Endogone species extracted from soil by wet sieving and decanting. T Brit Mycol Soc 46:235–244
Giovannetti M (2000) Spore germination and pre-symbiotic mycelial growth. In: Kapulnik Y, Douds DD Jr (eds) Arbuscular mycorrhizas: physiology and function. Springer, Berlin, pp 47–68
Greipsson S, El-Mayas H, Vestberg M, Walker C (2002) Arbuscular mycorrhizal fungi in sandy soils in Iceland. Arct Antarct Alp Res 34:419–427
Hazard C, Gosling P, van der Gast CJ, Mitchell DT, Doohan FM, Bending GD (2013) The role of local environment and geographical distance in determining community composition of arbuscular mycorrhizal fungi at the landscape scale. ISME J 7:498–508
Hillebrand H (2004) On the generality of the latitudinal diversity gradient. Am Nat 163:192–211
Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biomed J 50:346–363
Jonasson S, Michelsen A, Schmidt IK, Nielsen EV (1999) Responses in microbes and plants to changed temperature, nutrient, and light regimes in the arctic. Ecology 80:1828–1843
Juge C, Samson J, Bastien C, Vierheilig H, Coughlan A, Piché Y (2002) Breaking dormancy in spores of the arbuscular mycorrhizal fungus Glomus intraradices: a critical cold-storage period. Mycorrhiza 12:37–42
Klironomos JN (2000) Host-specificity and functional diversity among arbuscular mycorrhizal fungi. In: Bell CR, Brylinsky M, Johnson-Green P (eds) Microbial biosystems: new frontiers. Atlantic Canada Society for Microbial Ecology, Halifax, pp 845–851
Koske RE (1981) Multiple germination by spores of Gigaspora gigantea. Trans Br Mycol Soc 76:328–330
Kuszala C, Gianinazzi S, Gianinazzi-Pearson V (2001) Storage conditions for the long-term survival of AM fungal propagules in wet sieved soil fractions. Symbiosis 30:287–299
Kytöviita M-M, Pietikäinen A, Fritze H (2011) Soil microbial and plant responses to absence of plant cover and monoculturing in low arctic meadows. Appl Soil Ecol 48:142–151
Kytöviita M-M, Ruotsalainen A (2007) Mycorrhizal benefit in two low arctic herbs increases with increasing temperature. Am J Bot 94:1309–1315
Kytöviita M-M, Vestberg M,Tuomi J (2003) A test of mutual aid in common mycorrhizal network: established vegetation negates mycorrhizal benefit in seedlings. Ecology 84:898–906
Lalaymia I, Cranenbrouck S, Declerck S (2014) Maintenance and preservation of ectomycorrhizal and arbuscular mycorrhizal fungi. Mycorrhiza 24:323–337
Liu A, Wang B, Hamel C (2004) Arbuscular mycorrhiza colonization and development at suboptimal root zone temperature. Mycorrhiza 14:93–101
Morton JB, Bentivenga SP, Bever JD (2005) Discovery, measurement, and interpretation of diversity in arbuscular endomycorrhizal fungi (Glomales, Zygomycetes). Can J Bot 73:25–32
Murray DF (1995) Causes of arctic plant diversity: origin and evolution. In: Chapin FS III, Körner C (eds) Arctic and alpine biodiversity: patterns, causes and ecosystem consequences. Springer, Berlin, pp 21–32
Nedwell NB (1999) Effect of low temperature on microbial growth: lowered activity for substrates limits growth at low temperature. FEMS Microbiol Ecol 30:101–111
Nuortila C, Kytöviita M-M, Tuomi J (2004) Mycorrhizal symbiosis has contrasting effects on fitness components in Campanula rotundifolia. New Phytol 164:545–553
Oehl F, Sieverding E, Ineichen K, Mäder P, Boller T, Wiemken A (2003) Impact of land use intensity of the species diversity of arbuscular mycorrhizal fungi in agroecosystems of Central Europe. Appl Environ Microbiol 69:2816–2824
Oehl F, Sieverding E, Ineichen K, Ris E-A, Boller T, Wiemken A (2005) Community structure of arbuscular mycorrhizal fungi at different soil depths in extensively and intensively managed agroecosystems. New Phytol 165:273–283
Oehl F, Sieverding E, Ineichen K, Mäder P, Wiemken A, Boller T (2009) Distinct sporulation dynamics of arbuscular mycorrhizal fungal communities from different agroecosystems in long-term microcosms. Agric Ecosyst Environ 134:257–268
Olsson PA, Eriksen B, Dahlberg A (2004) Colonization by arbuscularmycorrhizal and fine endophytic fungi in herbaceous vegetation in the Canadian High Arctic. Can J Bot 82:1547–1556
Öpik M, Moora M, Liira J, Zobel M (2006) Composition of root-colonizing arbuscular mycorrhizal fungal communities in different ecosystems around the globe. J Ecol 94:778–790
Öpik M, Vanatoa A, Vanatoa E, Moora M, Davison J, Kalwij JM, Reier Ü, Zobel M (2010) The online database MaarjAM reveals global and ecosystemic distribution patterns in arbuscular mycorrhizal fungi (Glomeromycota). New Phytol 188:223–241
Öpik M, Zobel M, Cantero JJ et al (2013) Global sampling of plant roots expands the described molecular diversity of arbuscular mycorrhizal fungi. Mycorrhiza 23:411–430
Picone C (2000) Diversity and abundance of arbuscular-mycorrhizal fungus spores in tropical forest and pasture. Biotropica 32:734–750
Pietikäinen A, Kytöviita M-M, Husband R, Young JPW (2007) Diversity and persistence of arbuscular mycorrhizas in a low-Arctic meadow habitat. New Phytol 176:691–698
R Development Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org
Robinson-Boyer L, Grzyb I, Jeffries P (2009) Shifting the balance from qualitative to quantitative analysis of arbuscular mycorrhizal communities in field soils. Fungal Ecol 2:1–9
Savile DBO (1972) Arctic adaptations in plants. Canada Department of Agriculture Monograph No 6. Information Canada, Ottawa, Canada
Schalamuk S, Velázquez MS, Cabello MN (2013) Dynamics of arbuscular mycorrhizal fungi spore populations and their viability under contrasting tillage systems in wheat at different phenological stages. Biol Agric Hortic 29:38–45
Sjöberg J, Persson P, Mårtensson A, Adholeya A, Alström S (2004) Occurrence of Glomeromycota spores and some arbuscular mycorrhiza fungal species in arable fields in Sweden. Acta Agric Scand Sect B Soil Plant Sci 54:202–212
Tommerup IC (1983) Spore dormancy in vesicular arbuscular mycorrhizal fungi. T Brit Mycol Soc 81:37–38
Tommerup IC (1988) Long-term preservation by L-drying and storage of vesicular arbuscular mycorrhizal fungi. Trans Br Mycol Soc 90:585–590
Turrini A, Giovannetti M (2012) Arbuscular mycorrhizal fungi in national parks, nature reserves and protected areas worldwide: a strategic perspective for their in situ conservation. Mycorrhiza 22:81–97
Väre H, Vestberg M, Ohtonen R (1997) Shifts in mycorrhiza and microbial activity along an oroarctic altitudinal gradient in northern Fennoscandia. Arct Alp Res 29:93–104
Vega-Frutis R, Varga S, Kytöviita M-M (2014) Host plant and arbuscular mycorrhizal fungi show contrasting responses to temperature increase: implications for dioecious plants. Environ Exp Bot 104:54–64
Vestberg M, Kahiluoto H, Wallius E (2011) Arbuscular mycorrhizal fungal diversity and species dominance in a temperate soil with long-term conventional and low-input cropping systems. Mycorrhiza 21:351–361
Wagner SC, Skipper HD, Walley F, Briges WB (2001) Long-term survival of Glomus claroideum propagules from soil pot cultures under simulated conditions. Mycologia 93:815–820
Acknowledgments
The authors thank Gaia Francini, Tiina Savolainen, and Rocío Vega-Frutis for the help in taking care of the plants and two anonymous reviewers for the valuable comments and suggestions. This study was financially supported by the ERASMUS program (CF), the Academy of Finland (SV, MMK), and the Kone Foundation (MMK).
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Varga, S., Finozzi, C., Vestberg, M. et al. Arctic arbuscular mycorrhizal spore community and viability after storage in cold conditions. Mycorrhiza 25, 335–343 (2015). https://doi.org/10.1007/s00572-014-0613-4
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DOI: https://doi.org/10.1007/s00572-014-0613-4