A continental view of pine-associated ectomycorrhizal fungal spore banks: A quiescent functional guild with a strong biogeographic pattern

New Phytologist

Volumn 205, Issue 4, 2015, Pages 1619-1631

  Glassman, Sydney I ^a   Peay, Kabir G ^b   Talbot, Jennifer M ^b   Smith, Dylan P ^b   Chung, Judy A ^c   Taylor, John W ^c   Vilgalys, Rytas ^d   Bruns, Thomas D ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b STANFORD UNIVERSITY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d DUKE UNIVERSITY   (United States)

Author keywords

Biogeography; Ectomycorrhizae; Ectomycorrhizal (ECM) fungi; Microbial seed bank; Pine forests; Resistant propagule community; Symbiosis

Indexed keywords

BIOASSAY; BIOGEOGRAPHY; CONIFEROUS TREE; ECTOMYCORRHIZA; HOST PLANT; SOIL MICROORGANISM; SYMBIOSIS;

NORTH AMERICA;

CENOCOCCUM; FUNGI; LACCARIA; RHIZOPOGON; SUILLUS; THELEPHORA; WILCOXINA;

SOIL;

BIOASSAY; BIODIVERSITY; ECOSYSTEM; FOREST; FUNGUS SPORE; GEOGRAPHY; MICROBIOLOGY; MYCORRHIZA; NORTH AMERICA; PHYSIOLOGY; PINE; REGRESSION ANALYSIS; SOIL;

BIODIVERSITY; BIOLOGICAL ASSAY; ECOSYSTEM; FORESTS; GEOGRAPHY; MYCORRHIZAE; NORTH AMERICA; PINUS; REGRESSION ANALYSIS; SOIL; SPORES, FUNGAL;

EID: 84922826611     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.13240     Document Type: Article

References (67)

1. Adams RI, Miletto M, Taylor JW, Bruns TD. 2013. Dispersal in microbes: fungi in indoor air are dominated by outdoor air and show dispersal limitation at short distances. Isme Journal 7: 1262-1273.
2. Amend AS, Seifert KA, Samson R, Bruns TD. 2010. Indoor fungal composition is geographically patterned and more diverse in temperate zones than in the tropics. Proceedings of the National Academy of Sciences, USA 107: 13748-13753.
3. Anderson MJ. 2001. A new method for non-parametric multivariate analysis of variance. Austral Ecology 26: 32-46.
4. Baar J, Horton TR, Kretzer AM, Bruns TD. 1999. Mycorrhizal colonization of Pinus muricata from resistant propagules after a stand-replacing wildfire. New Phytologist 143: 409-418.
5. Bohn K, Pavlick R, Reu B, Kleidon A. 2014. The strengths of r- and K-selection shape diversity-disturbance relationships. PLoS One 9: 10.
6. Bonito G, Smith ME, Brenneman T, Vilgalys R. 2012. Assessing ectomycorrhizal fungal spore banks of truffle producing soils with pecan seedling trap-plants. Plant and Soil 356: 357-366.
7. Brundrett MC, Ashwath N, Jasper DA. 1996. Mycorrhizas in the Kakadu region of tropical Australia. 2. Propagules of mycorrhizal fungi in disturbed habitats. Plant and Soil 184: 173-184.
8. Bruns TD, Bidartondo MI, Taylor DL. 2002. Host specificity in ectomycorrhizal communities: what do the exceptions tell us? Integrative and Comparative Biology 42: 352-359.
9. Bruns TD, Fogel R, White TJ, Palmer JD. 1989. Accelerated evolution of a false-truffle from a mushroom ancestor. Nature 339: 140-142.
10. Bruns TD, Peay KG, Boynton PJ, Grubisha LC, Hynson NA, Nguyen NH, Rosenstock NP. 2009. Inoculum potential of Rhizopogon spores increases with time over the first 4 yr of a 99-yr spore burial experiment. New Phytologist 181: 463-470.
11. Buscardo E, Rodriguez-Echeverria S, Martin MP, De Angelis P, Pereira JS, Freitas H. 2010. Impact of wildfire return interval on the ectomycorrhizal resistant propagules communities of a Mediterranean open forest. Fungal Biology 114: 628-636.
12. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI et al. 2010. QIIME allows analysis of high-throughput community sequencing data. Nature Methods 7: 335-336.
13. Caporaso JG, Paszkiewicz K, Field D, Knight R, Gilbert JA. 2012. The Western English Channel contains a persistent microbial seed bank. Isme Journal 6: 1089-1093.
14. Cowden CC, Peterson CJ. 2013. Annual and seasonal dynamics of ectomycorrhizal fungi colonizing white pine (Pinus strobus) seedlings following catastrophic windthrow in northern Georgia, USA. Canadian Journal of Forest Research 43: 215-223.
15. Danielson RM. 1984. Ectomycorrhizal assoications in jack pine stands in northeastern Alberta. Canadian Journal of Botany 62: 932-939.
16. Dickie IA. 2007. Host preference, niches and fungal diversity. New Phytologist 174: 230-233.
17. Dickie IA, Martinez-Garcia LB, Koele N, Grelet GA, Tylianakis JM, Peltzer DA, Richardson SJ. 2013. Mycorrhizas and mycorrhizal fungal communities throughout ecosystem development. Plant and Soil 367: 11-39.
18. Dickie IA, Richardson SJ, Wiser SK. 2009. Ectomycorrhizal fungal communities and soil chemistry in harvested and unharvested temperate Nothofagus rainforests. Canadian Journal of Forest Research 39: 1069-1079.
19. Edgar RC. 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26: 2460-2461.
20. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. 2011. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27: 2194-2200.
21. Ehrlen J, van Groenendael JM. 1998. The trade-off between dispersability and longevity - an important aspect of plant species diversity. Applied Vegetation Science 1: 29-36.
22. Fleming LV. 1983. Succession of mycorrhizal fungi on birch - infection of seedlings planted around mature trees. Plant and Soil 71: 263-267.
23. Fleming LV. 1984. Effects of soil trenching and coring on the formation of ectomycorrhizas on birch seedlings grown around mature trees. New Phytologist 98: 143-153.
24. Frank JL, Anglin S, Carrington EM, Taylor DS, Viratos B, Southworth D. 2009. Rodent dispersal of fungal spores promotes seedling establishment away from mycorrhizal networks on Quercus garryana. Botany-Botanique 87: 821-829.
25. Gardes M, Bruns TD. 1993. ITS primers with enhanced specificity for Basidiomycetes - application to the identification of mycorrhizae and rusts. Molecular Ecology 2: 113-118.
26. Goslee SC, Urban DL. 2007. The ecodist package for dissimilarity-based analysis of ecological data. Journal of Statistical Software 22: 1-19.
27. Grime JP. 1977. Evidence for existence of 3 primary strategies in plants and its relevance to ecological and evolutionary theory. American Naturalist 111: 1169-1194.
28. Hagerman SM, Jones MD, Bradfield GE, Gillespie M, Durall DM. 1999. Effects of clear-cut logging on the diversity and persistence of ectomycorrhizae at a subalpine forest. Canadian Journal of Forest Research 29: 124-134.
29. Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A. 2005. Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology 25: 1965-1978.
30. Hoeksema JD, Vargas Hernandez J, Rogers DL, Luna Mendoza L, Thompson JN. 2012. Geographic divergence in a species-rich symbiosis: interactions between Monterey pines and ectomycorrhizal fungi. Ecology 93: 2274-2285.
31. Hopfensperger KN. 2007. A review of similarity between seed bank and standing vegetation across ecosystems. Oikos 116: 1438-1448.
32. Ishida TA, Nara K, Hogetsu T. 2007. Host effects on ectomycorrhizal fungal communities: insight from eight host species in mixed conifer-broadleaf forests. New Phytologist 174: 430-440.
33. Izzo A, Nguyen DT, Bruns TD. 2006. Spatial structure and richness of ectomycorrhizal fungi colonizing bioassay seedlings from resistant propagules in a Sierra Nevada forest: comparisons using two hosts that exhibit different seedling establishment patterns. Mycologia 98: 374-383.
34. Jones MD, Durall DM, Cairney JWG. 2003. Ectomycorrhizal fungal communities in young forest stands regenerating after clearcut logging. New Phytologist 157: 399-422.
35. Kipfer T, Moser B, Egli S, Wohlgemuth T, Ghazoul J. 2011. Ectomycorrhiza succession patterns in Pinus sylvestris forests after stand-replacing fire in the Central Alps. Oecologia 167: 219-228.
36. Kjøller R, Bruns TD. 2003. Rhizopogon spore bank communities within and among California pine forests. Mycologia 95: 603-613.
37. Koljalg U, Larsson KH, Abarenkov K, Nilsson RH, Alexander IJ, Eberhardt U, Erland S, Hoiland K, Kjoller R, Larsson E et al. 2005. UNITE: a database providing web-based methods for the molecular identification of ectomycorrhizal fungi. New Phytologist 166: 1063-1068.
38. Kreft H, Jetz W. 2010. A framework for delineating biogeographical regions based on species distributions. Journal of Biogeography 37: 2029-2053.
39. Last FT, Dighton J, Mason PA. 1987. Successions of sheathing mycorrhizal fungi. Trends in Ecology & Evolution 2: 157-161.
40. Legendre P, Fortin MJ. 1989. Spatial pattern and ecological analysis. Vegetatio 80: 107-138.
41. Lennon JT, Jones SE. 2011. Microbial seed banks: the ecological and evolutionary implications of dormancy. Nature Reviews Microbiology 9: 119-130.
42. Lichstein JW. 2007. Multiple regression on distance matrices: a multivariate spatial analysis tool. Plant Ecology 188: 117-131.
43. Massicotte HB, Molina R, Luoma DL, Smith JE. 1994. Biology of ectomycorrhizal genus, Rhizopogon 2. Patterns of host-fungus specificity following spore inoculation of diverse hosts grown in monoculture and dual culture. New Phytologist 126: 677-690.
44. Martiny JBH, Eisen JA, Penn K, Allison SD, Horner-Devine MC. 2011. Drivers of bacterial beta-diversity depend on spatial scale. Proceedings of the National Academy of Sciences, USA 108: 7850-7854.
45. Meiser A, Balint M, Schmitt I. 2014. Meta-analysis of deep-sequenced fungal communities indicates limited taxon sharing between studies and the presence of biogeographic patterns. New Phytologist 201: 623-635.
46. Miller SL, Torres P, McClean TM. 1994. Persistence of basidiospores and sclerotia of ectomycorrhizal fungi and morchella in soil. Mycologia 86: 89-95.
47. Nilsson RH, Veldre V, Hartmann M, Unterseher M, Amend A, Bergsten J, Kristiansson E, Ryberg M, Jumpponen A, Abarenkov K. 2010. An open source software package for automated extraction of ITS1 and ITS2 from fungal ITS sequences for use in high-throughput community assays and molecular ecology. Fungal Ecology 3: 284-287.
48. Oksanen J, Blanchet F, Kindt R, Legendre P, Minchin P, O'Hara R, Simpson GL, Solymos P, Stevens M, Wagner H. 2012. Vegan: community ecology package, R Package Version 2.0-10.
49. Peay KG, Schubert MG, Nguyen NH, Bruns TD. 2012. Measuring ectomycorrhizal fungal dispersal: macroecological patterns driven by microscopic propagules. Molecular Ecology 21: 4122-4136.
50. R Core Team. 2013. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
51. Reeder J, Knight R. 2009. The 'rare biosphere': a reality check. Nature Methods 6: 636-637.
52. Reeder J, Knight R. 2010. Rapidly denoising pyrosequencing amplicon reads by exploiting rank-abundance distributions. Nature Methods 7: 668-669.
53. Rusca TA, Kennedy PG, Bruns TD. 2006. The effect of different pine hosts on the sampling of Rhizopogon spore banks in five Eastern Sierra Nevada forests. New Phytologist 170: 551-560.
54. Sato H, Tsujino R, Kurita K, Yokoyama K, Agata K. 2012. Modelling the global distribution of fungal species: new insights into microbial cosmopolitanism. Molecular Ecology 21: 5599-5612.
55. Talbot JM, Bruns TD, Smith DP, Branco S, Glassman SI, Erlandson S, Vilgalys R, Peay KG. 2013. Independent roles of ectomycorrhizal and saprotrophic communities in soil organic matter decomposition. Soil Biology & Biochemistry 57: 282-291.
56. Talbot JM, Bruns TD, Taylor JW, Smith DP, Branco S, Glassman SI, Erlandson S, Vilgalys R, Liao H-L, Smith ME et al. 2014. Endemism and functional convergence across the North American soil mycobiome. Proceedings of the National Academy of Sciences, USA 111: 6341-6346.
57. 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. Molecular Ecology 8: 1837-1850.
58. Taylor JW, Turner E, Townsend JP, Dettman JR, Jacobson D. 2006. Eukaryotic microbes, species recognition and the geographic limits of species: examples from the kingdom Fungi. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences 361: 1947-1963.
59. Tedersoo L, May TW, Smith ME. 2010a. Ectomycorrhizal lifestyle in fungi: global diversity, distribution, and evolution of phylogenetic lineages. Mycorrhiza 20: 217-263.
60. Tedersoo L, Nilsson RH, Abarenkov K, Jairus T, Sadam A, Saar I, Bahram M, Bechem E, Chuyong G, Koljalg U. 2010b. 454 pyrosequencing and Sanger sequencing of tropical mycorrhizal fungi provide similar results but reveal substantial methodological biases. New Phytologist 188: 291-301.
61. Tedersoo L, Sadam A, Zambrano M, Valencia R, Bahram M. 2010c. Low diversity and high host preference of ectomycorrhizal fungi in Western Amazonia, a neotropical biodiversity hotspot. Isme Journal 4: 465-471.
62. Thompson K. 1987. Seeds and seed banks. New Phytologist 106: 23-34.
63. Thompson K, Band SR, Hodgson JG. 1993. Seed size and shape predict persistence in soil. Functional Ecology 7: 236-241.
64. Tilman D. 1994. Competition and biodiversity in spatially structured habitats. Ecology 75: 2-16.
65. Venables WN, Ripley BD. 2002. Modern applied statistics with S. New York, NY, USA: Springer.
66. Visser S. 1995. Ectomycorrhizal fungal succession in jack pine stands following wildfire. New Phytologist 129: 389-401.
67. White TJ, Bruns T, Lee S, Taylor J. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ, eds. PCR protocols: a guide to methods and applications. San Diego, CA, USA & London, UK: Academic Press, 315-322.