Root-colonizing and soil-borne communities of arbuscular mycorrhizal fungi in a temperate forest understorey1

Botany

Volumn 92, Issue 4, 2014, Pages 277-285

  Saks, Ülle ^a   Davison, John ^a   Öpik, Maarja ^a   Vasar, Martti ^a   Moora, Mari ^a   Zobel, Martin ^a  

^a UNIVERSITY OF TARTU   (Estonia)

Author keywords

Arbuscular mycorrhizal fungi; Microbial communities; Microbial ecology; Soil microbes; Symbionts

Indexed keywords

ARBUSCULAR MYCORRHIZA; COMMUNITY COMPOSITION; FOREST ECOSYSTEM; FUNGUS; MICROBIAL COMMUNITY; MICROBIAL ECOLOGY; PHYLOGENETICS; ROOT COLONIZATION; SOIL MICROORGANISM; SYMBIONT; TAXONOMY; TEMPERATE FOREST; UNDERSTORY;

ESTONIA; JARVSELJA;

EID: 84898759652     PISSN: 19162804     EISSN: None     Source Type: Journal    
DOI: 10.1139/cjb-2013-0058     Document Type: Article

References (70)

1. Alguacil, M., Torrecillas, E., Caravaca, F., Fernández, D., Azcón, R., and Roldán, A. 2011. The application of an organic amendment modifies the arbuscular mycorrhizal fungal communities colonizing native seedlings grown in a heavy-metal-polluted soil. Soil Biol. Biochem. 43(7): 1498-1508. doi:10.1016/j. soilbio.2011.03.026.
2. Bainard, L.D., Koch, A.M., Gordon, A.M., Newmaster, S.G., Thevathasan, N.V., and Klironomos, J.N. 2011. Influence of trees on the spatial structure of ar-buscular mycorrhizal communities in a temperate tree-based intercropping system. Agric. Ecosyst. Environ. 144(1): 13-20. doi:10.1016/j.agee.2011.07.014.
3. Baldrian, P., Kolařík, M., Štursová, M., Kopecký, J., Valášková, V., Vétrovský, T., Žifčáková, L., Šnajdr, J., Rídl, J., Vlček, C., and Voříšková, J. 2012. Active and total microbial communities in forest soil are largely different and highly stratified during decomposition. ISMEJ.6(2): 248-258. doi:10.1038/ismej.2011. 95. PMID:21776033.
4. Balestrini, R., Magurno, F., Walker, C., Lumini, E., and Bianciotto, V. 2010. Cohorts of arbuscular mycorrhizal fungi (AMF) in Vitis vinifera, a typical Mediterranean fruit crop. Environ. Microbiol. Rep. 2(4): 594-604. doi:10.1111/ j.1758-2229.2010.00160.x. PMID:23766230.
5. Bidartondo, M.I., Redecker, D., Hijri, I., Wiemken, A., Bruns, T.D., Domínguez, L., Sersic, A., Leake, J.R., and Read, D.J. 2002. Epiparasitic plants specialized on arbuscular mycorrhizal fungi. Nature, 419(6905): 389-392. doi:10.1038/ nature01054. PMID:12353033.
6. Busby, R.R., Stromberger, M.E., Rodriguez, G., Gebhart, D.L., and Paschke, M.W. 2013. Arbuscular mycorrhizal fungal community differs between a coexisting native shrub and introduced annual grass. Mycorrhiza, 23(2): 129-141. doi:10.1007/s00572-012-0455-x. PMID:22864708.
7. Chagnon, P.L., Bradley, R.L., and Klironomos, J.N. 2012. Using ecological network theory to evaluate the causes and consequences of arbuscular mycorrhizal communitystructure. NewPhytol.194(2):307-312.doi:10.1111/j.1469-8137.2011. 04044.x. PMID:22269121.
8. Corkidi, L., Rowland, D.L., Johnson, N.C., and Allen, E.B. 2002. Nitrogen fertilization alters the functioning of arbuscular mycorrhizas at two semiarid grasslands. Plant Soil, 240(2): 299-310. doi:10.1023/A:1015792204633.
9. Davison, J., Öpik, M., Daniell, T.J., Moora, M., and Zobel, M. 2011. Arbuscular mycorrhizal fungal communities in plant roots are not random assemblages. FEMS Microbiol. Ecol. 78(1): 103-115. doi:10.1111/j.1574-6941.2011.01103.x. PMID:21457278.
10. Davison, J., Öpik, M., Zobel, M., Vasar, M., Metsis, M., and Moora, M. 2012. Communities of arbuscular mycorrhizal fungi detected in forest soil are spatially heterogeneous but do not vary throughout the growing season. [Online.] PLoS ONE, 7(8): e41938. doi:10.1371/journal.pone.0041938.
11. Dumbrell, A.J., Ashton, P.D., Aziz, N., Feng, G., Nelson, M., Dytham, C., Fitter, A.H., and Helgason, T. 2011. Distinct seasonal assemblages of arbuscu-lar mycorrhizal fungi revealed by massively parallel pyrosequencing. New Phytol. 190(3): 794-804. doi:10.1111/j.1469-8137.2010.03636.x. PMID:21294738.
12. Edgar, R.C., Haas, B.J., Clemente, J.C., Quince, C., and Knight, R. 2011. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics, 27(16): 2194-2200. doi:10.1093/bioinformatics/btr381. PMID:21700674.
13. Fitter, A.H. 2005. Darkness visible: reflections on underground ecology. J. Ecol. 93(2): 231-243. doi:10.1111/j.0022-0477.2005.00990.x.
14. Gamper, H.A., Young, J.P.W., Jones, D.L., and Hodge, A. 2008. Real-time PCR and microscopy: Are the two methods measuring the same unit of arbuscular mycorrhizal fungal abundance? Fungal Genet. Biol. 45(5): 581-596. doi:10. 1016/j.fgb.2007.09.007.
15. Götzenberger, L., de Bello, F., Bråthen, K.A., Davison, J., Dubuis, A., Guisan, A., Lepš, J., Lindborg, R., Moora, M., Pärtel, M., Pellissier, L., Pottier, J., Vittoz, P., Zobel, K., and Zobel, M. 2012. Ecological assembly rules in plant communities-approaches, patterns and prospects. Biol. Rev. Cambridge Philos. Soc. 87(1): 111-127. doi:10.1111/j.1469-185X.2011.00187.x. PMID:21692965.
16. Hannula, S., de Boer, W., and van Veen, J. 2010. In situ dynamics of soil fungal communities under different genotypes of potato, including a genetically modified cultivar. Soil Biol. Biochem. 42(12): 2211-2223. doi:10.1016/j.soilbio. 2010.08.020.
17. Hart, M.M., and Reader, R.J. 2002. Taxonomic basis for variation in the colonization strategy of arbuscular mycorrhizal fungi. New Phytol. 153(2): 335-344. doi:10.1046/j.0028-646X.2001.00312.x.
18. Hart, M.M., Reader, R.J., and Klironomos, J.N. 2001. Life-history strategies of arbuscular mycorrhizal fungi in relation to their successional dynamics. Mycologia, 93(6): 1186-1194. doi:10.2307/3761678.
19. Hassan, S.E.D., Boon, E., St-Arnaud, M., and Hijri, M. 2011. Molecular biodiversity of arbuscular mycorrhizal fungi in trace metal-polluted soils. Mol. Ecol. 20(16): 3469-3483. doi:10.1111/j.1365-294X.2011.05142.x. PMID:21668808.
20. Helgason, T., Fitter, A.H., and Young, J.P.W. 1999. Molecular diversity of arbus-cular mycorrhizal fungi colonising Hyacinthoides non-scripta (bluebell) in a seminatural woodland. Mol. Ecol. 8(4): 659-666. doi:10.1046/j.1365-294x.1999. 00604.x.
21. Helgason, T., Merryweather, J.W., Denison, J., Wilson, P., Young, J.P.W., and Fitter, A.H. 2002. Selectivity and functional diversity in arbuscular mycorrhi-zas of co-occurring fungi and plants from a temperate deciduous woodland. J. Ecol. 90(2): 371-384. doi:10.1046/j.1365-2745.2001.00674.x.
22. Helgason, T., Merryweather, J.W., Young, J., and Fitter, A.H. 2007. Specificity and resilience in the arbuscular mycorrhizal fungi of a natural woodland community. J. Ecol. 95(4): 623-630. doi:10.1111/j.1365-2745.2007.01239.x.
23. Hempel, S., Renker, C., and Buscot, F. 2007. Differences in the species composition of arbuscular mycorrhizal fungi in spore, root and soil communities in a grassland ecosystem. Environ. Microbiol. 9(8): 1930-1938. doi:10.1111/j.1462-2920.2007.01309.x. PMID:17635540.
24. Johnson, N.C., Zak, D.R., Tilman, D., and Pfleger, F.L. 1991. Dynamicsofvesicular-arbuscular mycorrhizae during old field succession. Oecologia, 86(3): 349-358. doi:10.1007/BF00317600.
25. Johnson, N.C., Rowland, D.L., Corkidi, L., and Allen, E.B. 2008. Plant winners and losers during grassland N-eutrophication differ in biomass allocation and mycorrhizas. Ecology, 89(10): 2868-2878. doi:10.1890/07-1394.1. PMID:18959324.
26. Jumpponen, A. 2011. Analysis of ribosomal RNA indicates seasonal fungal community dynamics in Andropogon gerardii roots. Mycorrhiza, 21(6): 453-464. doi:10.1007/s00572-010-0358-7. PMID:21207073.
27. Kembel, S.W., Cowan, P.D., Helmus, M.R., Cornwell, W.K., Morlon, H., Ackerly, D.D., Blomberg, S.P., and Webb, C.O. 2010. Picante: R tools for integrating phylogenies and ecology. Bioinformatics, 26(11): 1463-1464. doi:10. 1093/bioinformatics/btq166. PMID:20395285.
28. Kivlin, S.N., Hawkes, C.V., and Treseder, K.K. 2011. Global diversity and distribution of arbuscular mycorrhizal fungi. Soil Biol. Biochem. 43(11): 2294-2303. doi:10.1016/j.soilbio.2011.07.012.
29. Klironomos, J.N. 2003. Variation in plant response to native and exotic arbuscu-lar mycorrhizal fungi. Ecology, 84(9): 2292-2301. doi:10.1890/02-0413.
30. Lee, J., Lee, S., and Young, J.P.W. 2008. Improved PCR primers for the detection and identification of arbuscular mycorrhizal fungi. FEMS Microbiol. Ecol. 65(2): 339-349. doi:10.1111/j.1574-6941.2008.00531.x. PMID:18631176.
31. Lumini, E., Orgiazzi, A., Borriello, R., Bonfante, P., and Bianciotto, V. 2010. Disclosing arbuscular mycorrhizal fungal biodiversity in soil through a land-use gradient using a pyrosequencing approach. Environ. Microbiol. 12(8): 2165-2179. doi:10.1111/j.1462-2920.2009.02099.x. PMID:21966911.
32. Maherali, H., and Klironomos, J.N. 2012. Phylogenetic and trait-based assembly of arbuscular mycorrhizal fungal communities. [Online.] PloS ONE, 7(5): e36695. doi:10.1371/journal.pone.0036695.
33. Marleau, J., Dalpé, Y., St-Arnaud, M., and Hijri, M. 2011. Spore development and nuclear inheritance in arbuscular mycorrhizal fungi. BMC Evol. Biol. 11: 51. doi:10.1186/1471-2148-11-51. PMID:21349193.
34. Martinez, T.N., and Johnson, N.C. 2010. Agricultural management influences propagule densities and functioning of arbuscular mycorrhizas in low- and high-input agroecosystems in arid environments. Appl. Soil Ecol. 46(2): 300-306. doi:10.1016/j.apsoil.2010.07.001.
35. Martínez-García, L.B., Armas, C., de Dios Miranda, J., Padilla, F.M., and Pugnaire, F.I. 2011. Shrubs influence arbuscular mycorrhizal fungi communities in a semi-arid environment. Soil Biol. Biochem. 43(3): 682-689. doi:10. 1016/j.soilbio.2010.12.006.
36. Mayfield, M.M., and Levine, J.M. 2010. Opposing effects of competitive exclusion on the phylogenetic structure of communities. Ecol. Lett. 13(9): 1085-1093. doi:10.1111/j.1461-0248.2010.01509.x. PMID:20576030.
37. Mirás-Avalos, J.M., Antunes, P.M., Koch, A., Khosla, K., Klironomos, J.N., and Dunfield, K.E. 2011. The influence of tillage on the structure of rhizosphere and root-associated arbuscular mycorrhizal fungal communities. Pedobiolo-gia, 54(4): 235-241. doi:10.1016/j.pedobi.2011.03.005.
38. Moora, M., Öpik, M., Sen, R., and Zobel, M. 2004. Native arbuscular mycorrhizal fungal communities differentially influence the seedling performance of rare and common Pulsatilla species. Funct. Ecol. 18(4): 554-562. doi:10.1111/j. 0269-8463.2004.00876.x.
39. Moora, M., Berger, S., Davison, J., Öpik, M., Bommarco, R., Bruelheide, H., Kühn, I., Kunin, W.E., Metsis, M., Rortais, A., Vanatoa, A., Vanatoa, E., Stout, J.C., Truusa, M., Westphal, C., Zobel, M., and Walther, G.R. 2011. Alien plants associate with widespread generalist arbuscular mycorrhizal fungal taxa: evidence from a continental-scale study using massively parallel 454 sequencing. J. Biogeogr. 38(7): 1305-1317. doi:10.1111/j.1365-2699.2011.02478.x.
40. Oksanen, J., Blanchet, F.G., Kindt, R., Legendre, P., Minchin, P.R., O'Hara, R.B., Simpson, G.L., Solymos, P., Stevens, H.M.H., and Wagner, H. 2012. Vegan: community ecology package, ver.2.0-3. Available from http://CRAN.R-project.org/package=vegan [accessed 6 March 2013].
41. Olsson, P.A., Rahm, J., and Aliasgharzad, N. 2010. Carbon dynamics in mycorrhi-zal symbioses is linked to carbon costs and phosphorus benefits. FEMS Microbiol. Ecol. 72: 125-131. doi:10.1111/j.1574-6941.2009.00833.x.
42. Öpik, M., and Moora, M. 2012. Missing nodes and links in mycorrhizal networks. New Phytol. 194(2): 304-306. doi:10.1111/j.1469-8137.2012.04121.x. PMID:22428699.
43. Öpik, M., Moora, M., Liira, J., and Zobel, M. 2006. Composition of root-colonizing arbuscular mycorrhizal fungal communities in different ecosystems around the globe. J. Ecol. 94(4): 778-790. doi:10.1111/j.1365-2745.2006.01136.x.
44. Öpik, M., Moora, M., Zobel, M., Saks, U., Wheatley, R., Wright, F., and Daniell, T. 2008. High diversity of arbuscular mycorrhizal fungi in a boreal herb-rich coniferous forest. New Phytol. 179(3): 867-876. doi:10.1111/j.1469-8137.2008. 02515.x. PMID:18537886.
45. Öpik, M., Metsis, M., Daniell, T.J., Zobel, M., and Moora, M. 2009. Large-scale parallel 454 sequencing reveals host ecological group specificity of arbuscu-lar mycorrhizal fungi in a boreonemoral forest. New Phytol. 184(2): 424-437. doi:10.1111/j.1469-8137.2009.02920.x. PMID:19558424.
46. Öpik, M., Vanatoa, A., Vanatoa, E., Moora, M., Davison, J., Kalwij, J.M., Reier, U., and Zobel, M. 2010. The online database MaarjAM reveals global and ecosys-temic distribution patterns in arbuscular mycorrhizal fungi (Glomeromy-cota). New Phytol. 188(1): 223-241. doi:10.1111/j.1469-8137.2010.03334.x. PMID: 20561207.
47. Öpik, M., Zobel, M., Cantero, J., Davison, J., Facelli, J., Hiiesalu, I., Jairus, T., Kalwij, J., Koorem, K., Leal, M., Liira, J., Metsis, M., Neshataeva, V., Paal, J., Phosri, C., Põlme, S., Reier, U., Saks, U., Schimann, H., Thiéry, O., Vasar, M., and Moora, M. 2013. Global sampling of plant roots expands the described molecular diversity of arbuscular mycorrhizal fungi. Mycorrhiza, 23(5): 411-430. doi:10.1007/s00572-013-0482-2.
48. Paradis, E., Claude, J., and Strimmer, K. 2004. APE: analyses of phylogenetics and evolution in R language. Bioinformatics, 20: 289-290. doi:10.1093/bio informatics/btg412. PMID:14734327.
49. Parameswaran, P., Jalili, R., Tao, L., Shokralla, S., Gharizadeh, B., Ronaghi, M., and Fire, A.Z. 2007. A pyrosequencing-tailored nucleotide barcode design unveils opportunities for large-scale sample multiplexing. Nucleic Acids Res. 35(19). doi:10.1093/nar/gkm760.
50. Pivato, B., Mazurier, S., Lemanceau, P., Siblot, S., Berta, G., Mougel, C., and van Tuinen, D. 2007. Medicago species affect the community composition of arbuscular mycorrhizal fungi associated with roots. New Phytol. 176(1): 197-210. doi:10.1111/j.1469-8137.2007.02151.x. PMID:17803650.
51. Pringle, A., and Bever, J.D. 2008. Analogous effects of arbuscular mycorrhizal fungi in the laboratory and a North Carolina field. New Phytol. 180(1): 162-175. doi:10.1111/j.1469-8137.2008.02537.x. PMID:18643939.
52. Roberts, D.W. 2012. Labdsv: ordination and multivariate analysis for ecology, package version 1.5-0. Available from http://CRAN.R-project.org/package=labdsv [accessed 6 March 2013].
53. Robinson-Boyer, L., Grzyb, I., and Jeffries, P. 2009. Shifting the balance from qualitative to quantitative analysis of arbuscular mycorrhizal communities in field soils. Fungal Ecol. 2: 1-9. doi:10.1016/j.funeco.2008.11.001.
54. Simon, L., Lalonde, M., and Bruns, T.D. 1992. Specific amplification of 18S fungal ribosomal genes from vesicular-arbuscular endomycorrhizal fungi colonizing roots. Appl. Environ. Microbiol. 58(1): 291-295. PMID:1339260.
55. Smith, S.E., and Read, D.J. 2008. Mycorrhizal symbiosis. Academic Press. Amsterdam.
56. Su, Y.-Y., Sun, X., and Guo, L.-D. 2011. Seasonality and host preference of arbus-cular mycorrhizal fungi of five plant species in the inner Mongolia steppe, China. Braz. J. Microbiol. 42(1): 57-65. doi:10.1590/S1517-83822011000100008.
57. Torrecillas, E., Alguacil, M.M., and Roldán, A. 2012. Host preferences of arbuscu-lar mycorrhizal fungi colonizing annual herbaceous plant species in semi-arid mediterranean prairies. Appl. Environ. Microbiol.78(17): 6180-6186. doi: 10.1128/AEM.01287-12. PMID:22752164.
58. Turrini, A., and 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(2): 81-97. doi:10.1007/s00572-011-0419-6. PMID:22075570.
59. Uibopuu, A., Moora, M., Saks, U., Daniell, T., Zobel, M., and Öpik, M. 2009. Differential effect of arbuscular mycorrhizal fungal communities from ecosystems along management gradient on the growth of forest understorey plant species. Soil Biol. Biochem. 41(10): 2141-2146. doi:10.1016/j.soilbio.2009. 07.026.
60. Uibopuu, A., Moora, M., Öpik, M., and Zobel, M. 2012. Temperate forest under-storey species performance is altered by local arbuscular mycorrhizal fungal communities from stands of different successional stages. Plant Soil, 356(1-2): 331-339. doi:10.1007/s11104-011-1116-0.
61. van der Heijden, M.G., and Scheublin, T.R. 2007. Functional traits in mycorrhizal ecology: their use for predicting the impact of arbuscular mycorrhizal fungal communities on plant growth and ecosystem functioning. New Phytol. 174(2): 244-250. doi:10.1111/j.1469-8137.2007.02041.x. PMID:17388887.
62. van der Heijden, M.G.A., Boller, T., Wiemken, A., and Sanders, I.R. 1998. Different arbuscular mycorrhizal fungal species are potential determinants of plant community structure. Ecology, 79(6): 2082-2091. doi:10.1890/0012-9658(1998)079[2082:DAMFSA]2.0.CO;2.
63. Vandenkoornhuyse, P., Husband, R., Daniell, T.J., Watson, I.J., Duck, J.M., Fitter, A.H., and Young, J.P.W. 2002. Arbuscular mycorrhizal community composition associated with two plant species in a grassland ecosystem. Mol. Ecol. 11(8): 1555-1564. doi:10.1046/j.1365-294X.2002.01538.x. PMID:12144674.
64. Vandenkoornhuyse, P., Ridgway, K.P., Watson, I.J., Fitter, A.H., and Young, J.P.W. 2003. Co-existing grass species have distinctive arbuscular mycorrhizal communities. Mol. Ecol. 12(11): 3085-3095. doi:10.1046/j.1365-294X.2003.01967.x. PMID:14629388.
65. Verbruggen, E., Kuramae, E.E., Hillekens, R., de Hollander, M., Kiers, E.T., Röling, W.F.M., et al. 2012a. Testing potential effects of maize expressing the Bacillus thuringiensis Cry1Ab endotoxin (Bt maize) on mycorrhizal fungal communities via DNA- and RNA-based pyrosequencing and molecular fingerprinting. Appl. Environ. Microbiol. 78(20): 7384-7392. doi:10.1128/AEM.01372-12. PMID:22885748.
66. Verbruggen, E., van der Heijden, M.G.A., Weedon, J.T., Kowalchuk, G.A., and Röling, W.F.M. 2012b. Community assembly, species richness and nestedness of arbuscular mycorrhizal fungi in agricultural soils. Mol. Ecol. 21(10): 2341-2353. doi:10.1111/j.1365-294X.2012.05534.x. PMID:22439851.
67. Williams, A., Ridgway, H.J., and Norton, D.A. 2011. Growth and competitiveness of the New Zealand tree species Podocarpus cunninghamii is reduced by ex-agricultural AMF but enhanced by forest AMF. Soil Biol. Biochem. 43(2): 339-345. doi:10.1016/j.soilbio.2010.10.021.
68. Wu, F., Dong, M., Liu, Y., Ma, X., An, L., Young, J., and Feng, H. 2011. Effects of long-term fertilization on AM fungal community structure and glomalin-related soil protein in the Loess Plateau of China. Plant Soil, 342(1-2): 233-247. doi:10.1007/s11104-010-0688-4.
69. Zobel, K., Zobel, M., and Peet, R.K. 1993. Change in pattern diversity during secondary succession in Estonian forests. J. Veg. Sci. 4(4): 489-498. doi:10. 2307/3236076.
70. Zobel, M. 1989. Secondary forest succession in Järvselja, Southeastern Estonia -changes in field layer vegetation. Ann. Bot. Fenn. 26(2): 171-182.