Browse > Article
http://dx.doi.org/10.1080/12298093.2019.1615297

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)
Publication Information
Mycobiology / v.47, no.2, 2019 , pp. 180-190 More about this Journal
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
Tuber borchii; ectomycorrhizae; microbial communities; Corylus avellane; soil;
Citations & Related Records
Times Cited By KSCI : 1  (Citation Analysis)
연도 인용수 순위
1 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.   DOI
2 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.
3 Bertini L, Rossi I, Zambonelli A, et al. Molecular identification of Tuber magnatum ectomycorrhizae in the field. Microbiol Res. 2006;161:59-64.   DOI
4 Mello A, Murat C, Bonfante P. Truffles: much more than a prized and local fungal delicacy. FEMS Microbiol Lett. 2006;260:1-8.   DOI
5 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.   DOI
6 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.   DOI
7 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.
8 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.
9 Wang B, Qiu Y. Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza. 2006;16:299-363.   DOI
10 Guo L, Tian C. Progress of the function of mycorrhizal fungi in the cycle of carbon and nitrogen. Microbiology China. 2013;40:158-171.
11 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.
12 Duponnois R, Garbaye J. Some mechanisms involved in growth stimulation of ectomycorrhizal fungi by bacteria. Can J Bot. 1990;68:2148-2152.   DOI
13 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.   DOI
14 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.   DOI
15 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.
16 Splivallo R, Deveau A, Valdez N, et al. Bacteria associated with truffle-fruiting bodies contribute to truffle aroma. Environ Microbiol. 2015;17:2647-2660.   DOI
17 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.   DOI
18 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.   DOI
19 Zambonelli A, Iotti M, Barbier E, et al. The microbial communities and fruiting of edible ectomycorrhizal mushrooms. Acta Botanica Yunnanica. 2009;31:81-85.
20 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.   DOI
21 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.   DOI
22 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.   DOI
23 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.   DOI
24 Ludwig-Muller J. Plants and endophytes: equal partners in secondary metabolite production?. Biotechnol Lett. 2015;37:1325-1334.   DOI
25 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.   DOI
26 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.   DOI
27 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.   DOI
28 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.   DOI
29 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.   DOI
30 Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 2010;26:2460-2461.   DOI
31 Asnicar F, Weingart G, Tickle TL, et al. Compact graphical representation of phylogenetic data and metadata with Graphlan. PeerJ. 2015;3:e1029.   DOI
32 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.   DOI
33 Streiblova E, Gryndlerova H, Gryndler M. Truffle br^ule: an efficient fungal life strategy. FEMS Microbiol Ecol. 2012;80:1-8.   DOI
34 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.   DOI
35 Napoli C, Mello A, Borra A, et al. Tuber melanosporum, when dominant, affects fungal dynamics in truffle grounds. New Phytol. 2010;185:237-247.   DOI
36 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.   DOI
37 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.
38 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.   DOI
39 Kues U, Martin F. On the road to understanding truffles in the underground. Fungal Genet Biol. 2011;48:555-560.   DOI
40 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.   DOI
41 Iotti M, Lancellotti E, Hall I, et al. The ectomycorrhizal community in natural Tuber borchii grounds. FEMS Microbiol Ecol. 2010;72:250-260.   DOI
42 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.   DOI
43 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.   DOI
44 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.   DOI
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.   DOI
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.   DOI
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.   DOI
48 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.
49 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.   DOI
50 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.   DOI
51 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.