DOI QR코드

DOI QR Code

Tuber borchii Shapes the Ectomycorrhizosphere Microbial Communities of Corylus avellana

  • Li, Xiaolin (Soil and Fertilizer Institute, Sichuan Academy of Agricultural Sciences) ;
  • Zhang, Xiaoping (Soil and Fertilizer Institute, Sichuan Academy of Agricultural Sciences) ;
  • Yang, Mei (Panzhihua Academy of Agricultural and Forestry Sciences) ;
  • Yan, Lijuan (Aquatic Geomicrobiology, Institute of Biodiversity, Friedrich Schiller University Jena) ;
  • Kang, Zongjing (Soil and Fertilizer Institute, Sichuan Academy of Agricultural Sciences) ;
  • Xiao, Yujun (Panzhihua Academy of Agricultural and Forestry Sciences) ;
  • Tang, Ping (Panzhihua Academy of Agricultural and Forestry Sciences) ;
  • Ye, Lei (Soil and Fertilizer Institute, Sichuan Academy of Agricultural Sciences) ;
  • Zhang, Bo (Soil and Fertilizer Institute, Sichuan Academy of Agricultural Sciences) ;
  • Zou, Jie (Soil and Fertilizer Institute, Sichuan Academy of Agricultural Sciences) ;
  • Liu, Chengyi (Panzhihua Academy of Agricultural and Forestry Sciences)
  • Received : 2018.12.25
  • Accepted : 2019.04.28
  • Published : 2019.06.01

Abstract

In this study, eight-month-old ectomycorrhizae of Tuber borchii with Corylus avellana were synthesized to explore the influence of T. borchii colonization on the soil properties and the microbial communities associated with C. avellana during the early symbiotic stage. The results showed that the bacterial richness and diversity in the ectomycorrhizae were significantly higher than those in the control roots, whereas the fungal diversity was not changed in response to T. borchii colonization. Tuber was the dominant taxon (82.97%) in ectomycorrhizae. Some pathogenic fungi, including Ilyonectria and Podospora, and other competitive mycorrhizal fungi, such as Hymenochaete, had significantly lower abundance in the T. borchii inoculation treatment. It was found that the ectomycorrhizae of C. avellana contained some more abundant bacterial genera (e.g., Rhizobium, Pedomicrobium, Ilumatobacter, Streptomyces, and Geobacillus) and fungal genera (e.g., Trechispora and Humicola) than the control roots. The properties of rhizosphere soils were also changed by T. borchii colonization, like available nitrogen, available phosphorus and exchangeable magnesium, which indicated a feedback effect of mycorrhizal synthesis on soil properties. Overall, this work highlighted the interactions between the symbionts and the microbes present in the host, which shed light on our understanding of the ecological functions of T. borchii and facilitate its commercial cultivation.

Keywords

References

  1. Kues U, Martin F. On the road to understanding truffles in the underground. Fungal Genet Biol. 2011;48:555-560. https://doi.org/10.1016/j.fgb.2011.02.002
  2. Iotti M, Lancellotti E, Hall I, et al. The ectomycorrhizal community in natural Tuber borchii grounds. FEMS Microbiol Ecol. 2010;72:250-260. https://doi.org/10.1111/j.1574-6941.2010.00844.x
  3. D'Auria M, Rana GL, Racioppi R, et al. Studies on volatile organic compounds of Tuber borchii and T. asa-foetida. J Chromatogr Sci. 2012;50:775-778. https://doi.org/10.1093/chromsci/bms060
  4. Zambonelli A, Iotti M, Rossi I, et al. Interactions between Tuber borchii and other ectomycorrhizal fungi in a field plantation. Mycol Res. 2000;104:698-702. https://doi.org/10.1017/S0953756299001811
  5. Zambonelli A, Lotti M, Giomaro G, et al. T. borchii cultivation: an interesting perspective. Proceedings of 2nd international workshop on edible ectomycorrhizal mushrooms; 2001 July; New Zealand Institute for Crop and Food Research Limited, CD room. p. 3-6.
  6. Benucci GM, Bonito G, Baciarelli Falini L, et al. Mycorrhization of pecan trees (Carya illinoinensis) with commercial truffle species: Tuber aestivum vittad. and Tuber borchii Vittad. Mycorrhiza. 2012;22:383-392. https://doi.org/10.1007/s00572-011-0413-z
  7. Zhang H, Hu H, Yang L, et al. Preliminary Study on the mycorrhizal synthesis of Tuber borchii Vittadini on Quercus franchetii Skan seedlings. Edible Fungi of China. 2013;32:30-31.
  8. Bertini L, Rossi I, Zambonelli A, et al. Molecular identification of Tuber magnatum ectomycorrhizae in the field. Microbiol Res. 2006;161:59-64. https://doi.org/10.1016/j.micres.2005.06.003
  9. Mello A, Murat C, Bonfante P. Truffles: much more than a prized and local fungal delicacy. FEMS Microbiol Lett. 2006;260:1-8. https://doi.org/10.1111/j.1574-6968.2006.00252.x
  10. Murat C, Vizzini A, Bonfante P, et al. Morphological and molecular typing of the belowground fungal community in a natural Tuber magnatum truffle-ground. FEMS Microbiol Lett. 2005;245:307-313. https://doi.org/10.1016/j.femsle.2005.03.019
  11. Brenna A, Montanini B, Muggiano E, et al. Integrative gene transfer in the truffle Tuber borchii by Agrobacterium tumefaciens-mediated transformation. AMB Express. 2014;4:43. eCollection 2014. https://doi.org/10.1186/s13568-014-0043-x
  12. Bradshaw BP. Physiological aspects of corylus avellana associated with the French black truffle fungus Tuber melanosporum and the consequence for commercial production of black truffles in Western Australia [dissertation]. Perth: Murdoch University; 2005.
  13. Santelices R, Palfner G. Controlled rhizogenesis and mycorrhization of hazelnut (Corylus avellana L.) cuttings with black truffle (Tuber melanosporum vitt.). Chil J Agric Res. 2010;70:204-212.
  14. Wang B, Qiu Y. Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza. 2006;16:299-363. https://doi.org/10.1007/s00572-005-0033-6
  15. Guo L, Tian C. Progress of the function of mycorrhizal fungi in the cycle of carbon and nitrogen. Microbiology China. 2013;40:158-171.
  16. Duponnois R, Garbaye J. Some mechanisms involved in growth stimulation of ectomycorrhizal fungi by bacteria. Can J Bot. 1990;68:2148-2152. https://doi.org/10.1139/b90-280
  17. Vivas A, Azcon R, Biro B, et al. Influence of bacterial strains isolated from lead-polluted soil and their interactions with arbuscular mycorrhizae on the growth of Trifolium pratense L. under lead toxicity. Can J Microbiol. 2003;49:577-588. https://doi.org/10.1139/w03-073
  18. Barbieri E, Bertini L, Rossi I, et al. New evidence for bacterial diversity in the ascoma of the ectomycorrhizal fungus Tuber borchii vittad. FEMS Microbiol Lett. 2005;247:23-35. https://doi.org/10.1016/j.femsle.2005.04.027
  19. Mello A, Miozzi L, Vizzini A, et al. Bacterial and fungal communities associated with Tuber magnatum-productive niches. G. Bot. Ital. 2010;144:323-332.
  20. Splivallo R, Deveau A, Valdez N, et al. Bacteria associated with truffle-fruiting bodies contribute to truffle aroma. Environ Microbiol. 2015;17:2647-2660. https://doi.org/10.1111/1462-2920.12521
  21. Deveau A, Antony-Babu S, Tacon FL, et al. Temporal changes of bacterial communities in the Tuber melanosporum, ectomycorrhizosphere during ascocarp development. Mycorrhiza. 2016;26:389-399. https://doi.org/10.1007/s00572-015-0679-7
  22. Li Q, Zhao J, Xiong C, et al. Tuber indicum shapes the microbial communities of ectomycorhizosphere soil and ectomycorrhizae of an indigenous tree (Pinus armandii). PLoS One. 2017;12:e0175720. eCollection 2017. https://doi.org/10.1371/journal.pone.0175720
  23. Wan S, Liu P. Diversity of culturable bacteria associated with ascocarps of a chinese white truffle, Tuber panzhihuanense (Ascomycota). Plant Divers Resourc. 2014;36:29-36.
  24. Zambonelli A, Iotti M, Barbier E, et al. The microbial communities and fruiting of edible ectomycorrhizal mushrooms. Acta Botanica Yunnanica. 2009;31:81-85.
  25. Sbrana C, Agnolucci M, Bedini S, et al. Diversity of culturable bacterial populations associated to Tuber borchii ectomycorrhizas and their activity on T. borchii mycelial growth. FEMS Microbiol Lett. 2002;211:195-201. https://doi.org/10.1111/j.1574-6968.2002.tb11224.x
  26. Barbieri E, Guidi C, Bertaux J, et al. Occurrence and diversity of bacterial communities in Tuber magnatum during truffle maturation. Environ Microbiol. 2007;9:2234-2246. https://doi.org/10.1111/j.1462-2920.2007.01338.x
  27. Hardoim PR, van Overbeek LS, Berg G, et al. The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol Mol Biol Rev. 2015;79:293-320. https://doi.org/10.1128/MMBR.00050-14
  28. Ludwig-Muller J. Plants and endophytes: equal partners in secondary metabolite production?. Biotechnol Lett. 2015;37:1325-1334. https://doi.org/10.1007/s10529-015-1814-4
  29. Geng L, Wang X, Yu F, et al. Mycorrhizal synthesis of Tuber indicum with two indigenous hosts, Castanea mollissima and Pinus armandii. Mycorrhiza. 2009;19:461-467. https://doi.org/10.1007/s00572-009-0247-0
  30. Li Q, Li X, Chen C, et al. Analysis of bacterial diversity and communities associated with Tricholoma matsutake fruiting bodies by barcoded pyrosequencing in Sichuan province, southwest China. J Microbiol Biotechnol. 2016;26:89-98. https://doi.org/10.4014/jmb.1505.05008
  31. Swindles GT, Reczuga M, Lamentowicz M, et al. Ecology of testate amoebae in an amazonian peatland and development of a transfer function for palaeohydrological reconstruction. Microb Ecol. 2014;68:284-298. https://doi.org/10.1007/s00248-014-0378-5
  32. Langenheder S, Szekely AJ. Species sorting and neutral processes are both important during the initial assembly of bacterial communities. ISME J. 2011;5:1086-1094. https://doi.org/10.1038/ismej.2010.207
  33. Laurie C, Doheny KF, Mirel DB, et al. Quality control and quality assurance in genotypic data for genome-wide association studies. Genet Epidemiol. 2010;34:591-602. https://doi.org/10.1002/gepi.20516
  34. Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 2010;26:2460-2461. https://doi.org/10.1093/bioinformatics/btq461
  35. Ramette A, Tiedje JM. Multiscale responses of microbial life to spatial distance and environmental heterogeneity in a patchy ecosystem. Proc Natl Acad Sci USA. 2007;104:2761-2766. https://doi.org/10.1073/pnas.0610671104
  36. Asnicar F, Weingart G, Tickle TL, et al. Compact graphical representation of phylogenetic data and metadata with Graphlan. PeerJ. 2015;3:e1029. https://doi.org/10.7717/peerj.1029
  37. Splivallo R, Novero M, Bertea CM, et al. Truffle volatiles inhibit growth and induce an oxidative burst in Arabidopsis thaliana. New Phytol. 2007;175:417-424. https://doi.org/10.1111/j.1469-8137.2007.02141.x
  38. Streiblova E, Gryndlerova H, Gryndler M. Truffle br^ule: an efficient fungal life strategy. FEMS Microbiol Ecol. 2012;80:1-8. https://doi.org/10.1111/j.1574-6941.2011.01283.x
  39. Garciamontero LG, Casermeiro MA, Hernando J, et al. Soil factors that influence the fruiting of Tuber melanosporum (black truffle). Soil Res. 2006;44:731-738. https://doi.org/10.1071/SR06046
  40. Napoli C, Mello A, Borra A, et al. Tuber melanosporum, when dominant, affects fungal dynamics in truffle grounds. New Phytol. 2010;185:237-247. https://doi.org/10.1111/j.1469-8137.2009.03053.x
  41. Vahdatzadeh M, Deveau A, Splivallo R. The role of the microbiome of truffles in aroma formation: a meta-analysis approach. Appl Environ Microbiol. 2015;81:6946-6952. https://doi.org/10.1128/AEM.01098-15
  42. Zhou K, Wang W, Peng Y, et al. Endophytic fungi from Nicotiana tabacum L. and their antibacterial activity. Nat Prod Res Develop. 2015;11:10-15.
  43. Reininger V, Sieber TN. Mycorrhiza reduces adverse effects of dark septate endophytes (DSE) on growth of conifers. PLoS One. 2012;7:e42865. 1371/journal.pone.0042865. Epub 2012 Aug 10. https://doi.org/10.1371/journal.pone.0042865
  44. Iotti M, Leonardi M, Lancellotti E, et al. Spatiotemporal dynamic of Tuber magnatum mycelium in natural truffle grounds. PLoS One. 2014;9:e115921. eCollection 2014. https://doi.org/10.1371/journal.pone.0115921
  45. Wang Y, Zhao X, Yi B, et al. Biochemical defenses induced by mycorrhizae fungi glomus mosseae in controlling strawberry fusarium wilt. Open Biomed Eng J. 2015;9:301-304. https://doi.org/10.2174/1874120701509010301
  46. Runnel K, Tamm H, Lohmus A. Surveying woodinhabiting fungi: Most molecularly detected polypore species form fruit-bodies within short distances. Fungal Ecol. 2015;18:93-99. https://doi.org/10.1016/j.funeco.2015.08.008
  47. Leonardi M, Iotti M, Oddis M, et al. Assessment of ectomycorrhizal fungal communities in the natural habitats of Tuber magnatum (Ascomycota, Pezizales). Mycorrhiza. 2013;23:349-358. https://doi.org/10.1007/s00572-012-0474-7
  48. Iotti M, Piattoni F, Leonardi P, et al. First evidence for truffle production from plants inoculated with mycelial pure cultures. Mycorrhiza. 2016;26:1-6. https://doi.org/10.1007/s00572-015-0641-8
  49. Wan S, Yu F, Tang L, et al. Ectomycorrhizae of Tuber huidongense and T. liyuanum with Castanea mollissima and Pinus armandii. Mycorrhiza. 2015;26:1-8.
  50. Marozzi G, Sanchez S, Benucci GM, et al. Mycorrhization of pecan (Carya illinoinensis) with black truffles: Tuber melanosporum and Tuber brumale. Mycorrhiza. 2017;27:303-309. https://doi.org/10.1007/s00572-016-0743-y
  51. De Miguel AM, Agueda B, Sanchez S, et al. Ectomycorrhizal fungus diversity and community structure with natural and cultivated truffle hosts: applying lessons learned to future truffle culture. Mycorrhiza. 2014;24:5-18. Epub 2014 Jan 15. https://doi.org/10.1007/s00572-013-0554-3

Cited by

  1. Tuber melanosporum shapes nir S-type denitrifying and ammonia-oxidizing bacterial communities in Carya illinoinensis ectomycorrhizosphere soils vol.8, 2019, https://doi.org/10.7717/peerj.9457
  2. Colonization by Tuber melanosporum and Tuber indicum affects the growth of Pinus armandii and phoD alkaline phosphatase encoding bacterial community in the rhizosphere vol.239, 2019, https://doi.org/10.1016/j.micres.2020.126520
  3. Insight to shape of soil microbiome during the ternary cropping system of Gastradia elata vol.20, 2019, https://doi.org/10.1186/s12866-020-01790-y
  4. Truffle species strongly shape their surrounding soil mycobiota in a Pinus armandii forest vol.203, pp.10, 2021, https://doi.org/10.1007/s00203-021-02598-8