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Greenhouse Seedlings of Alnus Showed Low Host Intrageneric Specificity and a Strong Preference for Some Tomentella Ectomycorrhizal Associates

  • Fungal Microbiology
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Abstract

Ectomycorrhizal (ECM) fungal associates of Alnus are relatively few in comparison with those associated with other tree hosts. The composition of ECM assemblages associated with Alnus seems to change very little across the Northern Hemisphere. However, Alnus-associated ECM assemblages from the Western United States, Mexico, and Argentina tend to differ from those in eastern North America and Europe, presumably due to their different biogeographic histories. Alnus glutinosa is a northern European species subjected to diverse environmental conditions. To address intrageneric host preference within two distantly related Alnus species (Alnus acuminata and A. glutinosa), we tested the ECM colonization on seedlings of both species inoculated with natural soil from A. acuminata forests. Two tomentelloid ECM fungi from A. acuminata natural soils were determined from the anatomotyping and molecular analysis. Both species colonized A. glutinosa seedlings and presented similar relative abundances. Additional soil sequence data from A. acuminata sites suggest that a variety of tomentelloid taxa occur, including several unidentified Tomentella lineages. Maximum-likelihood and Bayesian inference analyses based on internal transcribed spacer (ITS) sequences from various locations do not reflect associations of taxa based on their biogeographic origin, and clades are in general constituted by sequences from diverse regions, including South America, Mexico, USA, and Europe. Results illustrate the probable role of specific tomentelloid fungi in the early colonization of seedlings in A. acuminata forests as well as their importance in the structure of the ECM propagule community at the sites.

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References

  1. Carú M, Becerra A, Sepúlveda D, Cabello A (2000) Isolation of infective and effective Frankia strains from root nodules of Alnus acuminata (Betulaceae). World J Microbiol Biotechnol 16:647–651

    Article  Google Scholar 

  2. Becerra A, Daniele G, Dominguez L, Nouhra E, Horton T (2002) Ectomycorrhizae between Alnus acuminata H.B.K. and Naucoria escharoides (Fr.:Fr.) Kummer from Argentina. Mycorrhiza 12:61–66. doi:10.1007/s00572-001-0148-3

    Article  PubMed  Google Scholar 

  3. Becerra A, Pritsch K, Arrigo N, Palma M, Bartoloni N (2005) Ectomycorrhizal colonization of Alnus acuminata in northwestern Argentina in relation to season and soil parameters. Ann For Sci 62:325–332. doi:10.1051/forest:2005027

    Article  Google Scholar 

  4. Becerra A, Zak MR, Horton TR, Micolini J (2005) Ectomycorrhizal and arbuscular mycorrhizal colonization of Alnus acuminata from Calilegua National Park (Argentina). Mycorrhiza 15:525–531. doi:10.1007/s00572-005-0360-7

    Article  PubMed  Google Scholar 

  5. Nouhra E, Domínguez L, Becerra A, Mangeaud A (2003) Colonización micorricica y actinorricica en plantines de Alnus acuminata (Betulaceae), cultivados en suelos nativos de Alnus rubra. Bol Soc Argent Bot 38:199–206

    Google Scholar 

  6. Benson DR, Clawson ML (2000) Evolution of the actinorhizal plant symbioses. In: Triplett EW (ed) Prokaryotic nitrogen fixation: a model system for analysis of biological process. Horizon Scientific, Wymondham, pp 207–224

    Google Scholar 

  7. Yamanaka T, Li CY, Bormann BT, Okabe H (2003) Tripartite associations in an alder: effects of Frankia and Alpova diplophloeus on the growth, nitrogen fixation and mineral acquisition of Alnus tenuifolia. Plant Soil 254:179–186. doi:10.1023/A:1024938712822

    Article  CAS  Google Scholar 

  8. Walker J, Cohen H, Higgins L, Kennedy PG. Testing the link between community structure and function for ectomycorrhizal fungi involved in a global tri-partite symbiosis. New Phytol (in press)

  9. Roy S, Khasa DP, Greer CW (2007) Combining alders, frankiae, and mycorrhizae for the revegetation and remediation of contaminated ecosystems. Can J Bot 85:237–251. doi:10.1139/B07-017

    Article  CAS  Google Scholar 

  10. Teklehaimanot Z, Mmolotsi RM (2007) Contribution of red alder to soil nitrogen input in a silvopastoral system. Biol Fertil Soils 43:843–848. doi:10.1007/s00374-006-0163-9

    Article  Google Scholar 

  11. Molina R, Massicotte H, Trappe JM (1992) Specificity phenomena in mycorrhizal symbioses: community-ecological consequences and practical implications. In: Allen MF (ed) Mycorrhizal functioning: an integrative plant-fungal process. Chapman and Hall, New York, pp 357–423

    Google Scholar 

  12. Ding Q, Liang Y, Legendre P, He X, Pei K, Du X, Ma K (2011) Diversity and composition of ectomycorrhizal community on seedling roots: the role of host preference and soil origin. Mycorrhiza 21:669–680. doi:10.1007/s00572-011-0374-2

    Article  PubMed  Google Scholar 

  13. Baar J, Bastiaans T, van de Coevering MA, Roelots JGM (2002) Ectomycorrhizal root development in wet alder carr forests in response to desiccation and eutrophication. Mycorrhiza 12:147–151. doi:10.1007/s00572-002-0158-9

    Article  CAS  PubMed  Google Scholar 

  14. Pritsch K, Boyle H, Munch J, Buscot F (1997) Characterization and identification of black alder ectomycorrhizas by PCR/RFLP analyses of the rDNA internal transcribed spacer (ITS). New Phytol 137:357–369. doi:10.1046/j.1469-8137.1997.00806.x

    Article  CAS  Google Scholar 

  15. Tedersoo L, Suvi T, Jairus T, Ostonen I, Polme S (2009) Revisiting ectomycorrhizal fungi of the genus Alnus: differential host specificity, diversity and determinants of the fungal community. New Phytol 182:727–735. doi:10.1111/j.1469-8137.2009.02792.x

    Article  PubMed  Google Scholar 

  16. Põlme S, Bahram M, Yamanaka T, Nara K, Dai YC, Grebenc T, Kraigher H, Toivonen M, Wang PH, Matsuda Y, Naadel T, Kennedy PG, Koljalg U, Tedersoo L (2013) Biogeography of ectomycorrhizal fungi associated with alders (Alnus spp.) in relation to biotic and abiotic variables at the global scale. New Phytol. doi:10.1111/nph.12170

    PubMed  Google Scholar 

  17. Bormann B, Cromack K, Russell W (1994) Influences of red alder on soils and long-term ecosystem productivity. In: Hibbs D, DeBell D, Tarrant R (eds) The biology and management of red alder. Oregon State University Press, Corvallis, pp 47–56

    Google Scholar 

  18. Lilleskov E, Hobbie E, Fahey T (2002) Ectomycorrhizal fungal taxa differing in response to nitrogen deposition also differ in pure culture organic nitrogen use and natural abundance of nitrogen isotopes. New Phytol 154:219–231. doi:10.1046/j.1469-8137.2002.00367.x

    Article  CAS  Google Scholar 

  19. Toljander J, Eberhardt U, Toljander Y, Paul L, Taylor A (2006) Species composition of an ectomycorrhizal fungal community along a local nutrient gradient in a boreal forest. New Phytol 170:873–884. doi:10.1111/j.1469-8137.2006.01718.x

    Article  CAS  PubMed  Google Scholar 

  20. Van Miegroet H, Cole DW (1985) Acidification sources in Red Alder and Douglas-fir soils—importance of nitrification soil. Soil Sci Soc Am J 49:1274–1279

    Article  Google Scholar 

  21. Kennedy P, Garibay-Orijel R, Higgins L, Angeles-Arguiz R (2011) Ectomycorrhizal fungi in Mexican Alnus forests support the host co-migration hypothesis and continental-scale patterns in phylogeography. Mycorrhiza 21(6):559–568. doi:10.1007/s00572-011-0366-2

    Article  PubMed  Google Scholar 

  22. Molina R (1981) Ectomycorrhizal specificity in the genus Alnus. Can J Bot 59:325–334. doi:10.1139/b81-045

    Article  Google Scholar 

  23. Crane P (1989) Early fossil history and evolution of the Betulaceae. In: Crane P, Blackmore S (eds) Evolution, systematics, and fossil history of the Hamamelidae: “higher” Hamamelidae, vol 2. Clarendon, Oxford, pp 87–116

    Google Scholar 

  24. Furlow J (1979) The systematics of the American species of Alnus (Betulaceae). Rhodora 81(1–121):151–248

    Google Scholar 

  25. Chen Z, Li J (2004) Phylogenetics and biogeography of Alnus (Betulaceae) inferred from sequences of nuclear ribosomal DNA ITS region. Int J Plant Sci 165:325–335

    Article  CAS  Google Scholar 

  26. Navarro E, Bousquet J, Moiroud A, Munive A, Piou D, Normand P (2003) Molecular phylogeny of Alnus (Betulaceae) inferred from nuclear ribosomal DNA ITS sequences. Plant Soil 254:207–217. doi:10.1023/A:1024978409187

    Article  CAS  Google Scholar 

  27. Pritsch K, Beccera A, Polme S, Tedersoo L (2010) Description and identification of Alnus acuminata ectomycorrhizae from Argentinean alder stands. Mycologia 102:1263–1273. doi:10.3852/09-311

    Article  PubMed  Google Scholar 

  28. King A, Ferris C (1998) Chloroplast DNA phylogeography of Alnus glutinosa (L.) Gaertn. Mol Ecol 7:1151–1161

    Article  CAS  Google Scholar 

  29. Gehring CA, Whithan TG (1994) Comparisons of ectomycorrhizae in Pinyon Pines (Pinus edulis; Pinaceae) across extremes of soil type and herbivory. Am J Bot 81:1509–1516

    Article  Google Scholar 

  30. Helm DJ, Allen EB, Trappe JM (1999) Plant growth and ectomycorrhiza formation by transplants on deglaciated land near Exit Glacier, Alaska. Mycorrhiza 8:297–304. doi:10.1007/s005720050250

    Article  Google Scholar 

  31. Agerer R (1991) Characterization of ectomycorrhiza. In: Norris IR, Read DJ, Varma AK (eds) Techniques for the study of mycorrhiza. (Methods microbiol), vol 23. Academic, London, pp 25–73

    Chapter  Google Scholar 

  32. Agerer R (1999) Anatomical characteristics of identified ectomycorrhizas: an attempt towards a natural classification. In: Varma AK, Hock B (eds) Mycorrhiza, structure, function, molecular biology and biotechnology, 2nd edn. Springer, Berlin, pp 633–682

    Google Scholar 

  33. Rogers SO, Bendich AJ (1994) Extraction of total cellular DNA from plants, algae and fungi. In: Gelvin SB, Schilperoort RA (eds) Plant molecular biology manual, 3rd edn.

  34. Gardes M, Bruns T (1993) ITS primers with enhanced specificity for basidiomycetes—application to the identification of mycorrhizae and rust. Mol Ecol 2:113–118

    Article  CAS  PubMed  Google Scholar 

  35. Geml J, Pastor N, Fernandez L, Pacheco S, Semenova TA, Becerra AG, Wicaksono CY, Nouhra ER (2014) Large-scale fungal diversity assessment in the Andean Yungas forests reveals strong community turnover among forest types along an altitudinal gradient. Mol Ecol 23:2452–2472

    Article  CAS  PubMed  Google Scholar 

  36. Hughes KW, Petersen RH, Lickey EB (2009) Using heterozygosity to estimate a percentage DNA sequence similarity for environmental species’ delimitation across basidiomycete fungi. New Phytol 182:795–798. doi:10.1111/j.1469-8137.2009.02802.x

    Article  CAS  PubMed  Google Scholar 

  37. Bjorbækmo MFM, Carlsen T, Brysting A et al (2010) High diversity of root associated fungi in both alpine and arctic Dryas octopetala. BMC Plant Biol 10:244. doi:10.1186/1471-2229-10-244

    Article  PubMed Central  PubMed  Google Scholar 

  38. Geml J, Laursen GA, Herriott I, McFarland JM, Booth MG, Lennon N, Nusbaum HC, Taylor DL (2010) Phylogenetic and ecological analyses of soil and sporocarp DNA sequences reveal high diversity and strong habitat partitioning in the boreal ectomycorrhizal genus Russula Pers. (Russulales; Basidiomycota). New Phytol 187:494–507

    Article  CAS  PubMed  Google Scholar 

  39. Bellemain E, Davey ML, Kauserud H et al (2013) High paleodiversity of fungi revealed using high-throughput metabarcoding of ancient DNA from arctic permafrost. Environ Microbiol 15:1176–1189. doi:10.1111/1462-2920.12020

    Article  CAS  PubMed  Google Scholar 

  40. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200. doi:10.1093/bioinformatics/btr381

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  41. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461. doi:10.1093/bioinformatics/btq461

    Article  CAS  PubMed  Google Scholar 

  42. Kõljalg U, Nilsson RH, Abarenkov K et al (2013) Towards a unified paradigm for sequence-based identification of fungi. Mol Ecol 22:5271–5277. doi:10.1111/mec.12481

    Article  PubMed  Google Scholar 

  43. Tedersoo L, May T, Smith M (2010) Ectomycorrhizal lifestyle in fungi: global diversity, distribution, and evolution of phylogenetic lineages. Mycorrhiza 20:217–263. doi:10.1007/s00572-009-0274-x

    Article  PubMed  Google Scholar 

  44. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  45. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797. doi:10.1093/nar/gkh340

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  46. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59(3):307–321

    Article  CAS  PubMed  Google Scholar 

  47. Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256. doi:10.1093/molbev/msn083

    Article  CAS  PubMed  Google Scholar 

  48. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61(3):539–542

    Article  PubMed Central  PubMed  Google Scholar 

  49. Di Rienzo J, Robledo W, Casanoves F, Balzarini M, González L, Guzmán A, Tablada E (2002) Infostat. Versión Beta. Estadística y Biometría, Facultad de Ciencias Agropecuarias. Universidad Nacional de Córdoba, Córdoba

    Google Scholar 

  50. Zar JH (1999) Biostatistical analysis, 4th edn. Prentice Hall, Upper Saddle River

    Google Scholar 

  51. Lechevalier MP, Lechevalier HA (1990) Systematics, isolation and culture of Frankia. In: Schwintzer CR, Tjepkema JD (eds) The biology of Frankia and actinorhizal plants. Academic, San Diego, pp 35–60

    Chapter  Google Scholar 

  52. Bosco M, Fernandez MP, Simonet P, Materassi R, Normand P (1992) Evidence that some Frankia sp. strains are able to cross boundaries between Alnus and Elaeagnus host specificity groups. Appl Environ Microbiol 58:1569–1576

    PubMed Central  CAS  PubMed  Google Scholar 

  53. Benecke U (1969) Symbionts of alder nodules in New Zealand. Plant Soil 30:145–149

    Article  Google Scholar 

  54. Dawson JO (1979) Nitrogen-fixing trees and shrubs. Ill Res 21:4–9

    Google Scholar 

  55. Bogar LM, Kennedy PG (2013) New wrinkles in an old paradigm: neighborhood effects can modify the structure and specificity of Alnus-associated ectomycorrhizal fungal communities. FEMS Microbiol Ecol 83:767–777

    Article  CAS  PubMed  Google Scholar 

  56. Miller S, Koo CD, Molina R (1992) Early colonization of red alder and Douglas fir by ectomycorrhizal fungi and Frankia in soils from the Oregon coast range. Mycorrhiza 2:53–61. doi:10.1007/BF00203250

    Article  Google Scholar 

  57. Rochet J, Moreau PA, Manzi S, Gardes M (2011) Comparative phylogenies and host specialization in the alder ectomycorrhizal fungi Alnicola, Alpova and Lactarius (Basidiomycota) in Europe. BMC Evol Biol 11:40–50. doi:10.1186/1471-2148-11-40

    Article  PubMed Central  PubMed  Google Scholar 

  58. Geml J, Timling I, Robinson CH, Lennon N, Nusbaum HC, Brochmann C, Noordeloos ME, Taylor DL (2012) An arctic community of symbiotic fungi assembled by long-distance dispersers: phylogenetic diversity of ectomycorrhizal basidiomycetes in Svalbard based on soil and sporocarp DNA. J Biogeogr 39:74–88. doi:10.1111/j.1365-2699.2011.02588.x

    Article  Google Scholar 

  59. Kõljalg U, Dahlberg A, Taylor AF, Larsson E, Hallenberg N, Stenlid J, Larsson KH, Fransson PM, Karen O, Jonsson L (2000) Diversity and abundance of resupinate thelephoroid fungi as ectomycorrhizal symbionts in Swedish boreal forests. Mol Ecol 9(12):1985–1996. doi:10.1046/j.1365-294X.2000.01105.x

    Article  PubMed  Google Scholar 

  60. Tedersoo L, Suvi T, Larsson E, Koljalg U (2006) Diversity and community structure of ectomycorrhizal fungi in a wooded meadow. Mycol Res 110:734–748. doi:10.1016/j.mycres.2006.04.007

    Article  PubMed  Google Scholar 

  61. Sirikintaramas S, Sugioka N, Lee SS, Mohamed LA, Lee HS, Szmidt AE, Yamazaki T (2003) Molecular identification of ectomycorrhizal fungi associated with Dipterocarpaceae. Tropics 13:69–77

    Article  Google Scholar 

  62. Tedersoo L, Suvi T, Beaver K, Koljalg U (2007) Ectomycorrhizal fungi of the Seychelles: diversity patterns and host shifts from the native Vateriopsis seychellarum (Dipterocarpaceae) and Intsia bijuga (Caesalpiniaceae) to the introduced Eucalyptus robusta (Myrtaceae), but not Pinus caribea (Pinaceae). New Phytol 175:321–333. doi:10.1111/j.1469-8137.2007.02104.x

    Article  CAS  PubMed  Google Scholar 

  63. Taylor D, Bruns T (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. doi:10.1046/j.1365-294x.1999.00773.x

    Article  CAS  PubMed  Google Scholar 

  64. Baar J, Horton T, Kretzer A, Bruns T (1999) Mycorrhizal colonization of Pinus muricata from resistant propagules after a stand replacing wildfire. New Phytol 143:409–418. doi:10.1046/j.1469-8137.1999.00452.x

    Article  Google Scholar 

  65. 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. doi:10.3852/mycologia.98.3.374

    Article  PubMed  Google Scholar 

  66. Lilleskov E, Bruns T (2005) Spore dispersal of a resupinate ectomycorrhizal fungus, Tomentella sublilacina, via soil food webs. Mycologia 97(4):762–769. doi:10.3852/mycologia.97.4.762

    Article  PubMed  Google Scholar 

  67. Renvall P (1995) Community structure and dynamics of wood rotting basidiomycetes on decomposing conifer trunks in northern Finland. Karstenia 35:1–51

    Google Scholar 

  68. Barrett CF, Freudestein JV, Taylor DL, Koljalg U (2010) Rangewide analysis of fungal associations in the fully mycoheterotrophic Corallorhiza striata complex (Orchidaceae) reveals extreme specificity on ectomycorrhizal Tomentella (Thelephoraceae) across North America. Am J Bot 97(4):628–643. doi:10.3732/ajb.0900230

    Article  PubMed  Google Scholar 

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Acknowledgments

The authors wish to acknowledge the assistance of the Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) and the Universidad Nacional de Córdoba. Financial supports for the fieldwork, soil, and molecular analysis was provided by the Secretaria de Ciencia y Técnica (SECYT) of Universidad Nacional de Córdoba (26/11; 162/12; 124/13), Alberta Mennega Foundation, and Naturalis Research Initiative grant awarded to József Geml. The authors thank the Administración de Parques Nacionales (APN, Argentina) for providing permits for the scientific work and Marcel Eurlings and Elza Duijm (NBC) for conducting the Ion Torrent sequencing. The authors are also grateful to Lisandro Fernandez, Silvana Longo, and Nicolás Marro for their assistance.

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Nouhra, E., Pastor, N., Becerra, A. et al. Greenhouse Seedlings of Alnus Showed Low Host Intrageneric Specificity and a Strong Preference for Some Tomentella Ectomycorrhizal Associates. Microb Ecol 69, 813–825 (2015). https://doi.org/10.1007/s00248-014-0522-2

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