Browse > Article
http://dx.doi.org/10.1080/12298093.2019.1660297

Fungal Endophytes of Alnus incana ssp. rugosa and Alnus alnobetula ssp. crispa and Their Potential to Tolerate Heavy Metals and to Promote Plant Growth  

Lalancette, Steve (Departement de Biologie, Universite de Sherbrooke)
Lerat, Sylvain (Departement de Biologie, Universite de Sherbrooke)
Roy, Sebastien (Departement de Biologie, Universite de Sherbrooke)
Beaulieu, Carole (Departement de Biologie, Universite de Sherbrooke)
Publication Information
Mycobiology / v.47, no.4, 2019 , pp. 415-429 More about this Journal
Abstract
Soil contamination by metals is of particular interest, given that their retention times within the profile can be indefinite. Thus, phytostabilization can be viewed as a means of limiting metal toxicity in soils. Due to their ability to grow on contaminated soils, alders have repeatedly been used as key species in phytostabilization efforts. Alder ability to grow on contaminated sites stems, in part, from its association with microbial endophytes. This work emphasizes the fungal endophytes populations associated with Alnus incana ssp. rugosa and Alnus alnobetula ssp. crispa (previously A. viridis ssp. crispa) under a phytostabilization angle. Fungal endophytes were isolated from alder trees that were growing on or near disturbed environments; their tolerances to Cu, Ni, Zn, and As, and acidic pH (4.3, 3, and 2) were subsequently assessed. Cryptosporiopsis spp. and Rhizoscyphus spp. were identified as fungal endophytes of Alnus for the first time. When used as inoculants for alder, some isolates promoted plant growth, while others apparently presented antagonistic relationships with the host plant. This study reports the first step in finding the right fungal endophytic partners for two species of alder used in phytostabilization of metal-contaminated mining sites.
Keywords
Alder; dark septate endophyte; ericoid mycorrhizae; phytostabilization;
Citations & Related Records
연도 인용수 순위
  • Reference
1 Regvar M, Likar M, Piltaver A, et al. Fungal community structure under goat willows (Salix caprea L.) growing at metal polluted site: the potential of screening in a model phytostabilisation study. Plant Soil. 2010;330(1-2):345-356.   DOI
2 Zhang Y, Li T, Zhao Z. Colonization characteristics and composition of dark septate endophytes (DSE) in a lead and zinc slag heap in Southwest China. Soil Sediment Contam. 2013;22(5):532-545.   DOI
3 Colpaert JV, Wevers JHL, Krznaric E, et al. How metal-tolerant ecotypes of ectomycorrhizal fungi protect plants from heavy metal pollution. Ann For Sci. 2011;68(1):17-24.   DOI
4 Deram A, Languereau F, Haluwyn C. Mycorrhizal and endophytic fungal colonization in Arrhenatherum elatius L. roots according to the soil contamination in heavy metals. Soil Sediment Contam. 2011;20(1):114-127.   DOI
5 Likar M, Regvar M. Isolates of dark septate endophytes reduce metal uptake and improve physiology of Salix caprea L. Plant Soil. 2013;370(1-2):593-604.   DOI
6 Berthelot C, Blaudez D, Leyval C. Differential growth promotion of poplar and birch inoculated with three dark septate endophytes in two trace element-contaminated soils. Int J Phytorem. 2017;11:1118-1125.   DOI
7 MDDEP. Directive 019 sur l'industrie miniere. Ministere du developpement durable, de l'environnement et des parcs. Gouvernement du quebec. 2012 [accessed 2019 May 21]. Available from: http://www.mddelcc.gouv.qc.ca/milieu_ind/directive019/directive019.pdf
8 Molina R, Palmer JG. Isolation, maintenance and pure culture manipulation of ectomycorrhizal fungi. In: Schenck NC, editor. Methods and principles of mycorrhizal research. St Paul (MN): American Phytopathological Society; 1982. p. 115-129.
9 Yamada A, Ogura T, Degawa Y, et al. Isolation of Tricholoma matsutake and T. bakamatsutake cultures from field collected ectomycorrhizas. Mycoscience. 2001;42(1):43-50.   DOI
10 Fogarty RV, Tobin JM. Fungal melanins and their interaction with metals. Enzyme Microb Tech. 1996;19(4):311-317.   DOI
11 Bellion M, Courbot M, Jacob C, et al. Extracellular and cellular mechanisms sustaining metal tolerance in ectomycorrhizal fungi. FEMS Microbiol Lett. 2006;254(2):173-181.   DOI
12 Molina R. Ectomycorrhizal specificity in the genus Alnus. Can J Bot. 1981;59(3):325-334.   DOI
13 Kuznetsova T, Lukjanova A, Mandre M, et al. Aboveground biomass and nutrient accumulation dynamics in young black alder, silver birch and Scots pine plantations on reclaimed oil shale mining areas in Estonia. Forest Ecol Manag. 2011;262(2):56-64.   DOI
14 Giardina CP, Huffman S, Binkley D, et al. Alders increase soil phosphorus availability in a Douglasfir plantation. Can J For Res. 1995;25(10):1652-1657.   DOI
15 Walker JKM, Cohen H, Higgins LM, et al. Testing the link between community structure and function for ectomycorrhizal fungi involved in a global tripartite symbiosis. New Phytol. 2014;202(1):287-296.   DOI
16 Godbout AC, Fortin JA. Morphological features of synthesized ectomycorrhizae of Alnus crispa and A. rugosa. New Phytol. 1983;94(2):249-262.   DOI
17 Kabata-Pendias A, Pendias H. Trace elements in soils and plants. 3rd ed. Boca Raton (FL): CrC Press; 2001.
18 Likar M, Regvar M. Application of temporal temperature gradient gel electrophoresis for characterisation of fungal endophyte communities of Salix caprea L. in a heavy metal polluted soil. Sci Total Environ. 2009;407(24):6179-6187.   DOI
19 Tchounwou PB, Yedjou CG, Patlolla AK, et al. Heavy metal toxicity and the environment. Exp Suppl. 2012;101:133-164.
20 Ngu M, Moya E, Magan N. Tolerance and uptake of cadmium, arsenic and lead by Fusarium pathogens of cereals. Int Biodeter Biodegr. 1998;42(1):55-62.   DOI
21 Buckova M, Godocikova J, Polek B. Responses in the mycelial growth of Aspergillus niger isolates to arsenic contaminated environments and their resistance to exogenic metal stress. J Basic Microbiol. 2007;47(4):295-300.   DOI
22 Adeyemi AO. Bioaccumulation of arsenic by fungi. Am J Environ Sci. 2009;5(3):364-370.   DOI
23 Mohammadi-Bardbori A, Rannug A. Arsenic, cadmium, mercury and nickel stimulate cell growth via NADPH oxidase activation. Chem Biol Interact. 2014;224:183-188.   DOI
24 Xu R, Li T, Cui H, et al. Diversity and characterization of Cd-tolerant dark septate endophytes (DSEs) associated with the roots of Nepal alder (Alnus nepalensis) in a metal mine tailing of southwest China. App Soil Ecol. 2015;93:11-18.   DOI
25 Tedersoo L, Suvi T, Jairus T, et al. Revisiting ectomycorrhizal fungi of the genus Alnus: differential host specificity, diversity and determinants of the fungal community. New Phytol. 2009;182(3):727-735.   DOI
26 Kennedy P, Nguyen N, Cohen H, et al. Missing checkerboards? An absence of competitive signal in Alnus-associated ectomycorrhizal fungal communities. Peer J. 2014;2:e686.   DOI
27 Kennedy PG, Walker JKM, Bogar LM. Interspecific mycorrhizal networks and non-networking hosts: exploring the ecology of the host genus Alnus. In: Horton TR, editor. Mycorrhizal networks. Dordrecht, Netherlands: Springer; 2015. p. 227-254.
28 Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987;4:406-425.
29 Marx DH. The influence of ectotrophic mycorrhizal fungi on the resistance of pine roots to pathogenic infections: antagonism of mycorrhizal fungi to root pathogenic fungi and soil bacteria. Phytopathology. 1969;59:153-163.
30 White TJ, Bruns TD, Lee SB, et al. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: PCR protocols: a guide to methods and applications. New York (NY): Academic Press; 1990. p. 315-322.
31 Hoagland DR, Arnon DI. The water-culture method for growing plants without soil. Calif Agric Exp Stan Circ. 1950;347:1-32.
32 Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol. 2016;33(7):1870-1874.   DOI
33 Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol. 1980;16(2):111-120.   DOI
34 Belanger P-A, Bissonnette C, Berneche-D'Amours A, et al. Assessing the adaptability of the actinorhizal symbiosis in the face of environmental change. Environ Exp Bot. 2011;74:98-105.   DOI
35 Vierheilig H, Coughlan AP, Wyss U, et al. Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Appl Environ Microbiol. 1998;64(12):5004-5007.   DOI
36 Blaudez D, Jacob C, Turnau K, et al. Differential responses of ectomycorrhizal fungi to heavy metals in vitro. Mycol Res. 2000;104(11):1366-1371.   DOI
37 Zijlstra JD, Van't Hof P, Baar J, et al. Diversity of symbiotic root endophytes of the Helotiales in ericaceous plants and the grass, Deschampsia flexuosa. Stud Mycol. 2005;53:147-162.   DOI
38 Wilcox HE, Wang C. Mycorrhizal and pathological associations of dematiaceous fungi in roots of 7-month-old tree seedlings. Can J For Res. 1987;17(8):884-899.   DOI
39 Jumpponen A, Trappe JM. Dark-septate root endophytes: a review with special reference to facultative biotrophic symbiosis. New Phytol. 1998;140(2):295-310.   DOI
40 Mandyam K, Loughin T, Jumpponen A. Isolation and morphological and metabolic characterization of common endophytes in annually burned tallgrass. Mycologia. 2010;102(4):813-821.   DOI
41 Stoyke G, Currah RS. Resynthesis in pure culture of a common subalpine fungus-root association using Phialocephala fortinii and Menziesia ferruginea (Ericaceae). Arctic Alpine Res. 1993;25(3):189-193.   DOI
42 Newsham KK. Phialophora graminicola, a dark septate fungus, is a beneficial associate of the grass Vulpia ciliata ssp. ambigua. New Phytol. 1999;144(3):517-524.   DOI
43 Tellenbach C, Grunig CR, Sieber TN. Negative effects on survival and performance of Norway spruce seedlings colonized by dark septate root endophytes are primarily isolate-dependent. Environ Microbiol. 2011;13(9):2508-2517.   DOI
44 Reininger V, Grunig CR, Sieber TN. Host species and strain combination determine growth reduction of spruce and birch seedlings colonized by root-associated dark septate endophytes. Environ Microbiol. 2012;14(4):1064-1076.   DOI
45 Mayerhofer MS, Kernaghan G, Harper KA. The effects of fungal root endophytes on plant growth: a meta-analysis. Mycorrhiza. 2013;23(2):119-128.   DOI
46 Newsham KK. A meta-analysis of plant responses to dark septate root endophytes. New Phytol. 2011;190(3):783-793.   DOI
47 Upson R, Read DJ, Newsham KK. Nitrogen form influences the response of Deschampsia antarctica to dark septate root endophytes. Mycorrhiza. 2009;20(1):1-11.   DOI
48 Adriaensen K, Vangronsveld J, Colpaert JV. Zinctolerant Suillus bovinus improves growth of Znexposed Pinus sylvestris seedlings. Mycorrhiza. 2006;16(8):553-558.   DOI
49 Garbaye J. La symbiose mycorhizienne: une association entre les plantes et les champignons. 1st ed. Collection: Syntheses. Versaille: Editions Quae. 2013;1-280.
50 Vohn M, Mrnka L, Sov TL, et al. The cultivable endophytic community of Norway spruce ectomycorrhizas from microhabitats lacking ericaceous hosts is dominated by ericoid mycorrhizal Meliniomyces variabilis. Fungal Ecol. 2013;6:281-292.   DOI
51 Bois G, Piche Y, Fung MYP, et al. Mycorrhizal inoculum potentials of pure reclamation materials and revegetated tailing sands from the Canadian oil sand industry. Mycorrhiza. 2005;15(3):149-158.   DOI
52 Polme S, Bahram M, Yamanaka T, et al. Biogeography of ectomycorrhizal fungi associated with alders (Alnus spp.) in relation to biotic and abiotic variables at the global scale. New Phytol. 2013;198(4):1239-1249.   DOI
53 Roy M, Rochet J, Manzi S, et al. What determines Alnus-associated ectomycorrhizal community diversity and specificity? A comparison of host and habitat effects at a regional scale. New Phytol. 2013;198(4):1228-1238.   DOI
54 Kennedy PG, Hill LT. A molecular and phylogenetic analysis of the structure and specificity of Alnus rubra ectomycorrhizal assemblages. Fungal Ecol. 2010;3(3):195-204.   DOI
55 Bogar LM, Kennedy PG. New wrinkles in an old paradigm: neighborhood effects can modify the structure and specificity of Alnus-associated ectomycorrhizal fungal communities. FEMS Microbiol Ecol. 2013;83(3):767-777.   DOI
56 Berthelot C, Leyval C, Foulon J, et al. Plant growth promotion, metabolite production and metal tolerance of dark septate endophytes isolated from metal-polluted poplar phytomanagement sites. FEMS Microbiol Ecol. 2016;92:1-14.
57 Massicotte HB, Melville LH, Peterson RL, et al. Comparative studies of ectomycorrhiza formation in Alnus glutinosa and Pinus resinosa with Paxillus involutus. Mycorrhiza. 1999;8(5):229-240.   DOI
58 Mandyam K, Jumpponen A. Seeking the elusive function of the root-colonising dark septate endophytic fungi. Stud Mycol. 2005;53:173-189.   DOI
59 Jumpponen A, Mattson KG, Trappe JM. Mycorrhizal functioning of Phialocephala fortinii with Pinus contorta on glacier forefront soil: interactions with soil nitrogen and organic matter. Mycorrhiza. 1998;7(5):261-265.   DOI
60 Della Monica IF, Saparrat MCN, Godeas AM, et al. The co-existence between DSE and AMF symbionts affects plant P pools through P mineralization and solubilization processes. Fungal Ecol. 2015;17:10-17.   DOI
61 Rajkumar M, Sandhya S, Prasad MNV, et al. Perspectives of plant-associated microbes in heavy metal phytoremediation. Biotechnol Adv. 2012;30(6):1562-1574.   DOI
62 Belanger P-A, Bellenger J-P, Roy S. Heavy metal stress in alders: tolerance and vulnerability of the actinorhizal symbiosis. Chemosphere. 2015;138:300-308.   DOI
63 Godbold DL, Jentschke G, Winter S, et al. Ectomycorrhizas and amelioration of metal stress in forest trees. Chemosphere. 1998;36(4-5):757-762.   DOI
64 Jentschke G, Godbold DL. Metal toxicity and ectomycorrhizas. Physiol Plant. 2000;109(2):107-116.   DOI
65 Schutzendubel A, Polle A. Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J Exp Bot. 2002;53(372):1351-1365.   DOI
66 Vralstad T, Schumacher T, Taylor A. Mycorrhizal synthesis between fungal strains of the Hymenoscyphus ericae aggregate and potential ectomycorrhizal and ericoid hosts. New Phytol. 2002;153(1):143-152.   DOI
67 Pourrut B, Lopareva-Pohu A, Pruvot C, et al. Assessment of fly ash-aided phytostabilisation of highly contaminated soils after an 8-year field trial part 2. Influence on plants. Sci Total Environ. 2011;409(21):4504-4510.   DOI
68 Roy S, Khasa DP, Greer CW. Combining alders, frankiae, and mycorrhizae for the revegetation and remediation of contaminated ecosystems. Can J Bot. 2007;85(3):237-251.   DOI
69 Ledin M. Accumulation of metals by microorganisms - processes and importance for soil systems. Earth Sci Rev. 2000;51(1-4):1-31.   DOI
70 Khan MS, Zaidi A, Wani PA, et al. Role of plant growth promoting rhizobacteria in the remediation of metal contaminated soils. Environ Chem Lett. 2009;7(1):1-19.   DOI
71 Lorenc-Plucinska G, Walentynowicz M, Niewiadomska A. Capabilities of alders (Alnus incana and A. glutinosa) to grow in metal-contaminated soil. Ecol Eng. 2013;58:214-227.   DOI
72 Hibbs DE, Cromack K. Actinorhizal plants in Pacific Northwest forests. In: Schwintzer CR, Tjepkema JD, editors. The biology of Frankia and actinorhizal plants. London: Academic Press; 1990. p. 343-363.
73 Genre A, Russo G. Does a common pathway transduce symbiotic signals in plant-microbe interactions? Front Plant Sci. 2016;7:1-8.
74 Yu T, Nassuth A, Peterson RL. Characterization of the interaction between the dark septate fungus Phialocephala fortinii and Asparagus officinalis roots. Can J Microbiol. 2001;47(8):741-753.   DOI
75 Oldroyd G. Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat Rev Microbiol. 2013;11(4):252-263.   DOI
76 Daguerre Y, Plett JM, Venneault-Fourrey C. Signaling pathways driving the development of ectomycorrhizal symbiosis. In: Martin F, editor. Molecular mycorrhizal symbiosis. Hoboken (NJ): Wiley; 2016. p. 141-157.
77 Hambleton S, Sigler L. Meliniomyces, a new anamorph genus for root-associated fungi with phylogenetic affinities to Rhizoscyphus ericae ( Hymenoscyphus ericae), Leotiomycetes. Stud Mycol. 2005;53:1-27.   DOI
78 Bhatti JS, Foster NW, Hazlett PW. Fine root biomass and nutrient content in a black spruce peat soil with and without alder. Can J Soil Sci. 1998;78(1):163-169.   DOI
79 Bissonnette C, Fahlman B, Peru KM, et al. Symbiosis with Frankia sp. benefits the establishment of Alnus viridis ssp. crispa and Alnus incana ssp. rugosa in tailings sand from the Canadian oil sands industry. Ecol Eng. 2014;68:167-175.   DOI
80 Diem HG. Les mycorhizes des plantes actinorhiziennes. Act Bot Gallica. 1996;143(7):581-592.   DOI
81 Adle DJ, Sinani D, Kim H, et al. A cadmiumtransporting P1B-type ATPase in yeast Saccharomyces cerevisiae. J Biol Chem. 2007;282(2):947-955.   DOI
82 Egerton-Warburton LM, Griffin BJ. Differential responses of Pisolithus tinctorius isolates to aluminum in vitro. Can J Bot. 1995;73(8):1229-1233.   DOI
83 Hartley J, Cairney JWG, Meharg AA. Do ectomycorrhizal fungi exhibit adaptive tolerance to potentially toxic metals in the environment? Plant Soil. 1997;189(2):303-319.   DOI
84 Ban Y, Tang M, Chen H, et al. The response of dark septate endophytes (DSE) to heavy metals in pure culture. PLoS One. 2012;7(10):e47968-11.   DOI
85 Arguello JM, Eren E, Gonzalez-Guerrero M. The structure and function of heavy metal transport P1B-ATPases. BioMetals. 2007;20(3-4):233-248.   DOI
86 Kramer U, Talke IN, Hanikenne M. Transition metal transport. FEBS Lett. 2007;581(12):2263-2272.   DOI