352
Views
1
CrossRef citations to date
0
Altmetric
Ecology

Old-growth Acer macrophyllum trees host a unique suite of arbuscular mycorrhizal fungi and other root-associated fungal taxa in their canopy soil environment

ORCID Icon, , , ORCID Icon, ORCID Icon, ORCID Icon & show all
Pages 470-483 | Received 21 Jul 2022, Accepted 14 Apr 2023, Published online: 01 Jun 2023

LITERATURE CITED

  • Aubrey DA, Nadkarni NM, Broderick CP. 2013. Patterns of moisture and temperature in canopy and terrestrial soils in a temperate rainforest, Washington. Botany. 91(11):739–44. doi:10.1139/cjb-2013-0153.
  • Bakker MG. 2018. A fungal mock community control for amplicon sequencing experiments. Mol Ecol Resour. 18(3):541–56. doi:10.1111/1755-0998.12760.
  • Begum N, Qin C, Ahanger MA, Raza S, Khan MI, Ashraf M, Ahmed N, Zhang L. 2019. Role of arbuscular mycorrhizal fungi in plant growth regulation: implications in abiotic stress tolerance. Front Plant Sci. 10:1068. doi:10.3389/fpls.2019.01068.
  • Bender SF, Conen F, Van der Heijden MG. 2015. Mycorrhizal effects on nutrient cycling, nutrient leaching and N2O production in experimental grassland. Soil Biol Biochem. 80:283–92. doi:10.1016/j.soilbio.2014.10.016.
  • Bennett AE, Classen AT. 2020. Climate change influences mycorrhizal fungal–plant interactions, but conclusions are limited by geographical study bias. Ecology. 101(4):e02978. doi:10.1002/ecy.2978.
  • Brandt P, Abson DJ, DellaSala DA, Feller R, von Wehrden H. 2014. Multifunctionality and biodiversity: ecosystem services in temperate rainforests of the Pacific Northwest, USA. Biol Conserv. 169:362–71. doi:10.1016/j.biocon.2013.12.003.
  • Brundrett MC. 2006. Understanding the roles of multifunctional mycorrhizal and endophytic fungi. In: Schulz BJE, Boyle CJC, Sieber TN, editors. Microbial root endophytes. Berlin (Heidelberg): Springer. p. 281–98.
  • Brundrett MC, Tedersoo L. 2020. Resolving the mycorrhizal status of important northern hemisphere trees. Plant Soil. 454(1):3–34. doi:10.1007/s11104-020-04627-9.
  • Bunn RA, Simpson DT, Bullington LS, Lekberg Y, Janos DP. 2019. Revisiting the ‘direct mineral cycling’ hypothesis: arbuscular mycorrhizal fungi colonize leaf litter, but why? ISME J. 13(8):1891–98. doi:10.1038/s41396-019-0403-2.
  • Coxson DS, Nadkarni NM. 1995. Ecological roles of epiphytes in nutrient cycles of forest ecosystems. In: Lowman M, Nadkarni NM, editors. Forest canopies. San Diego (CA): Academic Press. p. 495–543.
  • De Cáceres M 2013. How to use the indicspecies package (ver. 1.7. 1). R Proj.
  • De Coster W, D’hert S, Schultz DT, Cruts M, Van Broeckhoven C. 2018. NanoPack: visualizing and processing long-read sequencing data. Bioinformatics. 34(15):2666–69. doi:10.1093/bioinformatics/bty149.
  • Deveautour C, Donn S, Power SA, Bennett AE, Powell JR. 2018. Experimentally altered rainfall regimes and host root traits affect grassland arbuscular mycorrhizal fungal communities. Mol Ecol. 27(8):2152–63. doi:10.1111/mec.14536.
  • Dufrêne M, Legendre P. 1997. Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecol Monogr. 67(3):345–66.
  • Edgar RC. 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 26(19):2460–61. doi:10.1093/bioinformatics/btq461.
  • Edgar RC, Flyvbjerg H. 2015. Error filtering, pair assembly and error correction for next-generation sequencing reads. Bioinformatics. 31(21):3476–82. doi:10.1093/bioinformatics/btv401.
  • Edmonds RL, Lebo DS. 1998. Diversity, production, and nutrient dynamics of fungal sporocarps on logs in an old-growth temperate rain forest, Olympic National Park, Washington. Can J For Res. 28(5):665–73. doi:10.1139/x98-029.
  • Enloe HA, Graham RC, Sillett SC. 2006. Arboreal histosols in old–growth redwood forest canopies, northern California. Soil Sci Soc Am J. 70(2):408–18. doi:10.2136/sssaj2004.0229.
  • Erwin TL. 1983. Tropical forest canopies: the last biotic frontier. Bull ESA. 29(1):14–20.
  • Fadaei S, Vaziriyeganeh M, Young M, Sherr I, Zwiazek JJ. 2020. Ericoid mycorrhizal fungi enhance salt tolerance in ericaceous plants. Mycorrhiza. 30(4):419–29. doi:10.1007/s00572-020-00958-8.
  • Fernandez CW, Kennedy PG. 2015. Moving beyond the black-box: fungal traits, community structure, and carbon sequestration in forest soils. New Phytol. 205(4):1378–80. doi:10.1111/nph.13289.
  • Ficken CD, Warren JM. 2019. The carbon economy of drought: comparing respiration responses of roots, mycorrhizal fungi and free–living microbes to an extreme dry–rewet cycle. Plant Soil. 435(1):407–22. doi:10.1007/s11104-018-03900-2.
  • Frank D, Finckh M, Wirth C. 2009. Impacts of land–use on habitat functions of old–growth forests and their biodiversity. In: Wirth C, Gleixner G, Heimann M, editors. Old–growth forests: function, fate and value. Berlin (Heidelberg): Springer. p. 429–50.
  • Franklin JF. 1988. Structural and functional diversity in temperate forests. In: Wilson EO, editor. Biodiversity. Washington (DC): National Academy Press. p. 166–75.
  • Gardes M, Bruns TD. 1993. ITS primers with enhanced specificity for basidiomycetes: application to the identification of mycorrhizae and rusts. Mol Ecol. 2(2):113–18. doi:10.1111/j.1365-294X.1993.tb00005.x.
  • Giovannetti M, Mosse B. 1980. An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol. 84(3):489–500. doi:10.1111/j.1469-8137.1980.tb04556.x.
  • Glassman SI, Wang IJ, Bruns TD. 2017. Environmental filtering by pH and soil nutrients drives community assembly in fungi at fine spatial scales. Mol Ecol. 26(24):6960–73. doi:10.1111/mec.14414.
  • Gotsch SG, Nadkarni N, Amici A. 2016. The functional roles of epiphytes and arboreal soils in tropical montane cloud forests. J Trop Ecol. 32(5):455–68. doi:10.1017/S026646741600033X.
  • Grelet GA, Ba R, Goeke DF, Houliston GJ, Taylor AF, Durall DM. 2017. A plant growth–promoting symbiosis between Mycena galopus and Vaccinium corymbosum seedlings. Mycorrhiza. 27(8):831–39. doi:10.1007/s00572-017-0797-5.
  • Grelet GA, Johnson D, Paterson E, Anderson IC, Alexander IJ. 2009. Reciprocal carbon and nitrogen transfer between an ericaceous dwarf shrub and fungi isolated from Piceirhiza bicolorata ectomycorrhizas. New Phytol. 182(2):359–66. doi:10.1111/j.1469-8137.2009.02813.x.
  • Hertel D, Köhler L, Rillig MC. 2011. Mycorrhizal, endophytic and ecomorphological status of tree roots in the canopy of a montane rain forest. Biotropica. 43(4):401–04. doi:10.1111/j.1744-7429.2011.00792.x.
  • Hodge A, Campbell CD, Fitter AH. 2001. An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material. Nature. 413(6853):297–99. doi:10.1038/35095041.
  • Hoysted GA, Kowal J, Jacob A, Rimington WR, Duckett JG, Pressel S, Orchard S, Ryan MH, Field KJ, Bidartondo MI. 2018. A mycorrhizal revolution. Curr Opin Plant Biol. 44:1–6. doi:10.1016/j.pbi.2017.12.004.
  • Jiang F, Zhang L, Zhou J, George TS, Feng G. 2021. Arbuscular mycorrhizal fungi enhance mineralisation of organic phosphorus by carrying bacteria along their extraradical hyphae. New Phytol. 230(1):304–15. doi:10.1111/nph.17081.
  • Jumpponen A. 2001. Dark septate endophytes–are they mycorrhizal? Mycorrhiza. 11(4):207–11. doi:10.1007/s005720100112.
  • Kennedy PG, Schouboe JL, Rogers RH, Weber MG, Nadkarni NM. 2010. Frankia and Alnus rubra canopy roots: an assessment of genetic diversity, propagule availability and effects on soil nitrogen. Microb Ecol. 59(2):214–20. doi:10.1007/s00248-009-9587-8.
  • Kivlin SN, Emery SM, Rudgers JA. 2013. Fungal symbionts alter plant responses to global change. Am J Bot. 100(7):1445–57. doi:10.3732/ajb.1200558.
  • Kubisch P, Hertel D, Leuschner C. 2015. Do ectomycorrhizal and arbuscular mycorrhizal temperate tree species systematically differ in root order-related fine root morphology and biomass? Front Plant Sci. 6:64. doi:10.3389/fpls.2015.00064.
  • Leigh J, Hodge A, Fitter AH. 2009. Arbuscular mycorrhizal fungi can transfer substantial amounts of nitrogen to their host plant from organic material. New Phytol. 181(1):199–207. doi:10.1111/j.1469-8137.2008.02630.x.
  • Lindo Z, Gonzalez A. 2010. The bryosphere: an integral and influential component of the Earth’s biosphere. Ecosystems. 13(4):612–27. doi:10.1007/s10021-010-9336-3.
  • Looby CI, Hollenbeck EC, Treseder KK. 2020. Fungi in the canopy: how soil fungi and extracellular enzymes differ between canopy and ground soils. Ecosystems. 23(4):768–82. doi:10.1007/s10021-019-00439-w.
  • Mafune KK 2021. Root-associated fungal diversity, nutrient mineralization and micro-climatic interconnections: fundamental processes in canopy soils of old-growth Acer macrophyllum in Washington State’s temperate rainforests [dissertation]. University of Washington, Seattle (WA, USA).
  • Mafune KK, Godfrey BJ, Vogt DJ, Vogt KA. 2020. A rapid approach to profiling diverse fungal communities using the MinION™ nanopore sequencer. BioTechniques. 68(2):72–78. doi:10.2144/btn-2019-0072.
  • Matson AL, Corre MD, Veldkamp E. 2014. Nitrogen cycling in canopy soils of tropical montane forests responds rapidly to indirect N and P fertilization. Glob Change Biol. 20(12):3802–13. doi:10.1111/gcb.12668.
  • McMurdie PJ, Holmes S. 2013. Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PloS One. 8(4):e61217. doi:10.1371/journal.pone.0061217.
  • Molina-Montenegro MA, Acuña-Rodríguez IS, Torres-Díaz C, Gundel PE, Dreyer I. 2020. Antarctic root endophytes improve physiological performance and yield in crops under salt stress by enhanced energy production and Na+ sequestration. Sci Rep. 10(1):1–10. doi:10.1038/s41598-020-62544-4.
  • Nadkarni NM. 1981. Canopy roots: convergent evolution in rainforest nutrient cycles. Science. 214(4524):1023–24. doi:10.1126/science.214.4524.1023.
  • Nadkarni NM. 1986. The nutritional effects of epiphytes on host trees with special reference to alteration of precipitation chemistry. Selbyana. (9): 44–51.
  • Nadkarni NM, Schaefer D, Matelson TJ, Solano R. 2002. Comparison of arboreal and terrestrial soil characteristics in a lower montane forest, Monteverde, Costa Rica. Pedobiologia. 46(1):24–33. doi:10.1078/0031-4056-00110.
  • Nilsen AR, Teasdale SE, Guy PL, Summerfield TC, Orlovich DA. 2020. Fungal diversity in canopy soil of silver beech, Nothofagus menziesii (Nothofagaceae). PloS One. 15(1):e0227860. doi:10.1371/journal.pone.0227860.
  • Nilsson RH, Larsson KH, Taylor AFS, Bengtsson-Palme J, Jeppesen TS, Schigel D, Kennedy P, Picard K, Glöckner FO, Tedersoo L, et al. 2019. The UNITE database for molecular identification of fungi: handling dark taxa and parallel taxonomic classifications. Nucleic Acids Res. 47(D1):D259–D264. doi:10.1093/nar/gky1022.
  • O’Dell TE, Ammirati JF, Schreiner EG. 2000. Species richness and abundance of ectomycorrhizal basidiomycete sporocarps on a moisture gradient in the Tsuga heterophylla zone. Can J Bot. 77(12):1699–711. doi:10.1139/b99-144.
  • O’Keefe TC, Naiman RJ. 2006. The influence of forest structure on riparian litterfall in a Pacific Coastal rain forest. Can J For Res. 36(11):2852–63. doi:10.1139/x06-180.
  • Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H. 2013. Package ‘vegan. Community Ecol Package. version 2:1–295.
  • Orlovich DA, Draffin SJ, Daly RA. 2013. Piracy in the high trees: ectomycorrhizal fungi from an aerial ‘canopy soil’ microhabitat. Mycologia. 105(1):52–60. doi:10.3852/11-307.
  • Pérez CA, Guevara R, Carmona MR, Armesto JJ. 2005. Nitrogen mineralization in epiphytic soils of an old-growth Fitzroya cupressoides forest, southern Chile. Écoscience. (12):210–215. doi: 10.2980/i1195-6860-12-2-210.1
  • Perry DR. 1978. A method of access into the crowns of emergent and canopy trees. Biotropica. 10(2):155–57. doi:10.2307/2388019.
  • Phillips JM, Hayman DS. 1970. Improved procedures for clearing roots and staining parasitic and vesicular–arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycologia Soc. 55(1):158–61. doi:10.1016/S0007-1536(70)80110-3.
  • Rath M, Grolig F, Haueisen J, Imhof, S. 2014. Combining microtomy and confocal laser scanning microscopy for structural analyses of plant–fungus associations. Mycorrhiza (24): 293–300. https://doi.org/10.1007/s00572-013-0530-y
  • R Core Team. 2018. R: a language and environment for statistical computing. Vienna (Austria): R Foundation for Statistical Computing.
  • Rice AV, Currah RS. 2005. Oidiodendron: a survey of the named species and related anamorphs of Myxotrichum. Stud Mycol. 53(1):83–120. doi:10.3114/sim.53.1.83.
  • Röhrig E, Ulrich B. 1991. Temperate deciduous forests. Amsterdam (Netherlands): Elsevier.
  • Rozmoš M, Bukovská P, Hršelová H, Kotianova M, Dudáš M, Gančarčíková K, Jansa J. 2022. Organic nitrogen utilisation by an arbuscular mycorrhizal fungus is mediated by specific soil bacteria and a protist. ISME J. 16(3):676–85. doi:10.1038/s41396-021-01112-8.
  • Schimel J. 2013. Microbes and global carbon. Nat Clim Chang. 3(10):867–68. doi:10.1038/nclimate2015.
  • Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, et al. 2009. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol. 75(23):7537–41. doi:10.1128/AEM.01541-09.
  • Selosse MA, Le Tacon F. 1998. The land flora: a phototroph-fungus partnership? Trends Ecol Evol. 13(1):15–20. doi:10.1016/S0169-5347(97)01230-5.
  • Smith DP, Peay KG. 2014. Sequence depth, not PCR replication, improves ecological inference from next generation DNA sequencing. PLoS One. 9(2):e90234. doi:10.1371/journal.pone.0090234.
  • Smith SE, Read DJ. 2008. Mycorrhizal symbiosis. Cambridge (UK): Academic Press.
  • Tejo CF, Fontúrbel FE. 2019. A vertical forest within the forest: millenary trees from the Valdivian rainforest as biodiversity hubs. Ecology. 100(4):e02584. doi:10.1002/ecy.2584.
  • Tejo Haristoy C, Zabowski D, Nadkarni NM. 2014. Canopy soils of Sitka spruce and bigleaf maple in the Queets River watershed, Washington. Soil Sci Soc Am J. 78(S1):118–24. doi:10.2136/sssaj2013.07.0300nafsc.
  • Tejo CF, Zabowski D, Nadkarni NM. 2015. Total and epiphytic litter under the canopy of Acer macrophyllum in an old–growth temperate rainforest, Washington State, USA. Can J For Res. 45(11):1654–61. doi:10.1139/cjfr-2014-0492.
  • Terhonen E, Blumenstein K, Kovalchuk A, Asiegbu FO. 2019. Forest tree microbiomes and associated fungal endophytes: functional roles and impact on forest health. Forests. 10(1):42. doi:10.3390/f10010042.
  • Thoen E, Harder CB, Kauserud H, Botnen SS, Vik U, Taylor AF, Menkis A, Skrede I. 2020. In vitro evidence of root colonization suggests ecological versatility in the genus Mycena. New Phytol. 227(2):601–12. doi:10.1111/nph.16545.
  • Thom D, Rammer W, Seidl R. 2017. Disturbances catalyze the adaptation of forest ecosystems to changing climate conditions. Glob Chang Biol. 23(1):269–82. doi:10.1111/gcb.13506.
  • Toju H, Tanabe AS, Yamamoto S, Sato H. 2012. High-coverage ITS primers for the DNA-based identification of ascomycetes and basidiomycetes in environmental samples. PloS One. 7: e40863.
  • Treseder KK, Holden SR. 2013. Fungal carbon sequestration. Science. 339(6127):1528–29. doi:10.1126/science.1236338.
  • Trudell SA, Edmonds RL. 2004. Macrofungus communities correlate with moisture and nitrogen abundance in two old–growth conifer forests, Olympic National Park, Washington, USA. Can J Bot. 82(6):781–800. doi:10.1139/b04-057.
  • Unuk T, Martinović T, Finžgar D, Šibanc N, Grebenc T, Kraigher H. 2019. Root–associated fungal communities from two phenologically contrasting Silver Fir (Abies alba Mill.) groups of trees. Front Plant Sci. 10:214. doi:10.3389/fpls.2019.00214.
  • Urrutia-Jalabert R, Malhi Y, Lara A. 2015. The oldest, slowest rainforests in the world? Massive biomass and slow carbon dynamics of Fitzroya cupressoides temperate forests in Southern Chile. PLoS One. 10(9):e0137569. doi:10.1371/journal.pone.0137569.
  • van der Heijden MGA, Martin FM, Selosse MA, Sanders IR. 2015. Mycorrhizal ecology and evolution: the past, the present and the future. New Phytol. 205(4):1406–23. doi:10.1111/nph.13288.
  • Van Pelt R, O’Keefe TC, Latterell JJ, Naiman RJ. 2006. Riparian forest stand development along the Queets River in Olympic National Park, Washington. Ecol Monogr. 76(2):277–98. doi:10.1890/05-0753.
  • Villarreal-Ruiz L, Anderson IC, Alexander IJ. 2004. Interactions between an isolate from the Hymenoscyphus ericae aggregate and roots of Pinus and Vaccinium. New Phytol. 164(1):183–92. doi:10.1111/j.1469-8137.2004.01167.x.
  • Westcott SL, Schloss PD. 2017. OptiClust, an improved method for assigning amplicon-based sequence data to operational taxonomic units. MSphere 2(2):e00073–e17. doi:10.1128/mSphereDirect.00073-17.
  • White TJ, Bruns T, Lee S, Taylor J. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis M, Gelfand D, Sninsky K, White T, editors. PCR protocols: a guide to methods and applications. New York (USA): Academic Press. p. 315–22.
  • Wickham H. 2016. ggplot2: elegant graphics for data analysis. New York (USA): Springer-Verlag.
  • Yang H, Zhao X, Li L, Zhang J. 2020. Detecting the colonization of ericoid mycorrhizal fungi in Vaccinium uliginosum using in situ polymerase chain reaction and green fluorescent protein. Plant Methods. 16(1):1–8. doi:10.1186/s13007-019-0534-5.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.