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Review | Open Access

In vitro interactions between the ectomycorrhizal Pisolithus tinctorius and the saprotroph Hypholoma fasciculare fungi: morphological aspects and volatile production

Paula Baptistaa( ), Paula Guedes de Pinhob, Nathalie Moreirab, Ricardo Malheiroa, Francisca Reisc, Jorge Padrãoc, Rui Tavaresc, Teresa Lino-Netoc
Centro De Investigação De Montanha (CIMO), Instituto Politécnico De Bragança, Campus De Santa Apolónia, Bragança, Portugal
UCIBIO-REQUIMTE/Laboratory of Toxicology, Faculty of Pharmacy, University of Porto, Porto, Portugal
BioSystems & Integrative Sciences Institute (Bioisi), Plant Functional Biology Centre, University of Minho, Campus De Gualtar, Braga, Portugal
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Abstract

Ectomycorrhizal fungi are crucial for forests sustainability. For Castanea sativa, ectomycorrhizal fungus Pisolithus tinctorius is an important mutualist partner. Saprotrophic fungi Hypholoma fasciculare, although used for biocontrol of Armillaria root disease, it negatively affected the interaction between the P. tinctorius and plant host roots, by compromise the formation of P. tinctorius-C. sativa mycorrhizae. In this work, fungal morphology during inhibition of H. fasciculare against P. tinctorius was elucidated. P. tinctorius growth was strongly affected by H. fasciculare, which was significantly reduced after six days of co-culture and become even more significant through time. During this period, P. tinctorius developed vesicles and calcium oxalate crystals, which were described as mechanisms to stress adaption by fungi. H. fasciculare produced different volatile organic compounds in co-cultures over time and differ between single or in dual-species. H. fasciculare highly produced sesquiterpenes (namely, α-muurolene) and nitrogen-containing compounds, which are recognised as having antimicrobial activity.

Keywords

Interactionfungiantagonismectomycorrhizalsaprotroph

References

 

Al-Salihi SAA, Bull I, Al-Salhi RA, Gates PJ, Salih K, Bailey AM, Foster GD. 2020. Further biochemical profiling of Hypholoma fasciculare metabolome reveals its chemogenetic diversity. bioRxiv. 122176
Crossref Google Scholar
 

Aqueveque P, Becerra J, Palfner G, Silva M, Alarcón J, Anke T, Sterner O. 2006. Antimicrobial activity of metabolites from mycelial cultures of Chilean basidiomycetes. J Chil Chi Soc. 51:1057–1060.
Crossref Google Scholar
 

Bagamboula CF, Uyttendaele M, Debevere J. 2004. Inhibitory effect of thyme and basil essential oils, carvacrol, thymol, estragol, linalool and p-cymene towards Shigella sonnei and S. flexneri. Food Microbiol. 21:(1):33–42. doi:10.1016/S0740-0020(03)00046-7.
Crossref Google Scholar
 

Baptista P, Martins A, Tavares RM, Lino-Neto T. 2010. Diversity and fruiting pattern of macrofungi associated with chestnut (Castanea sativa) in the Trás-os-Montes region (Northeast Portugal). Fungal Ecol. 3(1):9–19. doi:10.1016/j.funeco.2009.06.002.
Crossref Google Scholar
 

Baptista P, Reis F, Pereira E, Tavares R, Richard F, Selosse M, Lino-Neto T, Lino-Neto T. 2015. Soil DNA pyrosequencing fruitbodies surveys reveal contrasting diversity for various fungal ecological guilds in chestnut orchards. Environ Microbiol Rep. 7(6):946–954. doi:10.1111/1758-2229.12336.
Crossref Google Scholar
 

Boddy L. 2000. Interspecific combative interactions between wood-decaying basidiomycetes. FEMS Microbiol Ecol. 31(3):185–194. doi:10.1111/j.1574-6941.2000.tb00683.x.
Crossref Google Scholar
 

Carvalho LM, Carvalho F, Bastos ML, Baptista P, Moreira N, Monforte AR, Silva Ferreira AC, Guedes de Pinho P. 2014. Non-targeted and targeted analysis of wild toxic and edible mushrooms using Gas Chromatography-Ion Trap Mass Spectrometry. Talanta. 118::292–303. doi:10.1016/j.talanta.2013.09.038.
Crossref Google Scholar
 

Casarrubia S, Sapienza S, Fritz H, Daghino S, Rosenkranz M, Schnitzler J-P, Martin F, Perotto S, Martino E. 2016. Ecologically different fungi affect Arabidopsis development: contribution of soluble and volatile compounds. PloS One. 11:e0168236. doi:10.1371/journal.pone.0168236.
Crossref Google Scholar
 
Chapman B, Emile B, Curran M 2001. Using Hypholoma fasciculare inoculation as a means to control Armillaria root disease on calcareous soils: trial establisment and monitoring. Cariboo For Reg. - Res Sect 4.
 

Chen H, Xiao X, Wang J, Wu L, Zheng Z, Yu Z. 2008. Antagonistic effects of volatiles generated by Bacillus subtilis on spore germination and hyphal growth of the plant pathogen, Botrytis cinerea. Biotechnol Lett. 30(5):919–923. doi:10.1007/s10529-007-9626-9.
Crossref Google Scholar
 

Courty PE, Buee M, Diedhiou AG, Frey-Klett P, Le Tacon F, Rineau F, Turpault MP, Uroza S, Garbaye J. 2010. The role of ectomycorrhizal communities in forest ecosystem processes: new perspectives and emerging concepts. Soil Biol Biochem. 42(5):679–698. doi:10.1016/j.soilbio.2009.12.006.
Crossref Google Scholar
 

Cox KD, Scherm H. 2006. Interaction dynamics between saprobic lignicolous fungi and Armillaria in controlled environments: exploring the potential for competitive exclusion of Armillaria on peach. Biol Control. 37(3):291–300. doi:10.1016/j.biocontrol.2006.01.012.
Crossref Google Scholar
 

de Boer W, Folman LB, Gunnewiek PJAK, Svensson T, Bastviken D, Öberg G, Del Rio JC, Boddy L. 2010. Mechanism of antibacterial activity of the white-rot fungus Hypholoma fasciculare colonizing wood. Can J Microbiol. 56(5):380–388. doi:10.1139/W10-023.
Crossref Google Scholar
 

Ditengou F, Müller A, Rosenkranz M, Felten J, Lasok H, van Doorn MM, Legué V, Palme K, Schnitzler JP, Polle A. 2015. Volatile signalling by sesquiterpenes from ectomycorrhizal fungi reprogrammes root architecture. Nat Commun. 6(1):6279. doi:10.1038/ncomms7279.
Crossref Google Scholar
 

Dutton MV, Evans CS. 1996. Oxalate production by fungi: its role in pathogenicity and ecology in the soil environment. Can J Microbiol. 42(9):881–895. doi:10.1139/m96-114.
Crossref Google Scholar
 

Evans J, Eyre C, Rogers HJ, Boddy L, Müller CT. 2008. Changes in volatile production during interspecific interactions between four wood rotting fungi growing in artificial media. Fungal Ecol. 1(2–3):57–68. doi:10.1016/j.funeco.2008.06.001.
Crossref Google Scholar
 

Gadgil RL, Gadgil PD. 1975. Suppression of litter decomposition by mycorrhizal roots of Pinus radiata. New Zeal J For Sci. 5:33–41.
Google Scholar
 

Glass NL, Jacobson DJ, Shiu PKT. 2000. The genetics of hyphal fusion and vegetative incompatibility in filamentous ascomycete fungi. Ann Rev Genet. 34:(1):165–186. doi:10.1146/annurev.genet.34.1.165.
Crossref Google Scholar
 

Haidar R, Roudet J, Bonnard O, Dufour MC, Corio-Costet MF, Fert M, Gautier T, Deschamps A, Fermaud M. 2016. Screening and modes of action of antagonistic bacteria to control the fungal pathogen Phaeomoniella chlamydospora involved in grapevine trunk diseases. Microbiol Res. 192:172–184. doi:10.1016/j.micres.2016.07.003.
Crossref Google Scholar
 

Hiltpold I, Turlings TCJ. 2008. Belowground chemical signaling in maize: When simplicity rhymes with efficiency. J Chem Ecol. 34(5):628–635. doi:10.1007/s10886-008-9467-6.
Crossref Google Scholar
 

Hiscox J, Boddy L. 2017. Armed and dangerous – Chemical warfare in wood decay communities. Fungal Biol Rev. 31(4):169–184. doi:10.1016/j.fbr.2017.07.001.
Crossref Google Scholar
 

Hiscox J, Savoury M, Vaughan IP, Muller CT, Boddy L. 2015. Antagonistic fungal interactions influence carbon dioxide evolution from decomposing wood. Fungal Ecol. 14::24–32. doi:10.1016/j.funeco.2014.11.001.
Crossref Google Scholar
 

Hynes J, Müller CT, Jones TH, Boddy L. 2007. Changes in volatile production during the course of fungal mycelial interactions between Hypholoma fasciculare and Resinicium bicolor. J Chem Ecol. 33(1):43–55. doi:10.1007/s10886-006-9209-6.
Crossref Google Scholar
 

Inoue K, Kanematsu S, Park P, Ikeda K. 2011. Cytological analysis of mycelial incompatibility in Helicobasidium mompa. FEMS Microbiol Lett. 315(2):94–100. doi:10.1111/j.1574-6968.2010.02174.x.
Crossref Google Scholar
 

Itoo ZA, Reshi ZA. 2013. The multifunctional role of ectomycorrhizal associations in forest ecosystem processes. Bot Rev. 79(3):371–400. doi:10.1007/s12229-013-9126-7.
Crossref Google Scholar
 

Johansson EM, Fransson PMA, Finlay RD, Hees PAW. 2008. Quantitative analysis of exudates from soil-living basidiomycetes in pure culture as a response to lead, cadmium and arsenic stress. Soil Biol Biochem. 40(9):2225–2236. doi:10.1016/j.soilbio.2008.04.016.
Crossref Google Scholar
 

Kramer R, Abraham WR. 2012. Volatile sesquiterpenes from fungi: what are they good for? Phytochem Rev. 11(1):15–37. doi:10.1007/s11101-011-9216-2.
Crossref Google Scholar
 

Li X, Garbeva P, Liu X, Klein Gunnewiek PJ, Clocchiatti A, Hundscheid MP, Wang X, de Boer W. 2020. Volatile-mediated antagonism of soil bacterial communities against fungi. Environ Microbiol. 22:(3):1025–1035. doi:10.1111/1462-2920.14808.
Crossref Google Scholar
 

Lindahl B, Tunlid A. 2015. Ectomycorrhizal fungi – potential organic matter decomposers, yet not saprotrophs. New Phytol. 205:1443–1447.
Crossref Google Scholar
 

Michael G, Bahri-Esfahani J, Li Q, Rhee YJ, Wei Z, Fomina M, Liang X. 2014. Oxalate production by fungi: significance in geomycology, biodeterioration and bioremediation. Fungal Biol Rev. 28(2–3):36–55. doi:10.1016/j.fbr.2014.05.001.
Crossref Google Scholar
 

Minerdi D, Bossi S, Gullino ML, Garibaldi A. 2009. Volatile organic compounds: a potential direct long-distance mechanism for antagonistic action of Fusarium oxysporum strain MSA 35. Environ Microbiol. 11(4):844–854. doi:10.1111/j.1462-2920.2008.01805.x.
Crossref Google Scholar
 

Müller A, Faubert P, Hagen M, Castell W, Polle A, Schnitzler J-P, Rosenkranz M. 2013. Volatile profiles of fungi-chemotyping of species and ecological functions. Fungal Genet Biol. 54:25–33. doi:10.1016/j.fgb.2013.02.005.
Crossref Google Scholar
 

Nicolotti G, Paolo G, Varese GC. 1999. Effectiveness of some biocontrol and chemical treatments against. Eur J For Pathol. 29(5):339–346. doi:10.1046/j.1439-0329.1999.00159.x.
Crossref Google Scholar
 

Nicolotti G, Varese GC. 1996. Screening of antagonistic fungi against air-borne infection by Heterobasidion annosum on Norway spruce. For Ecol Manage. 88(3):249–257. doi:10.1016/S0378-1127(96)03844-3.
Crossref Google Scholar
 

Pereira E, Coelho V, Tavares RM, Lino-Neto T, Baptista P. 2011. Effect of competitive interactions between ectomycorrhizal and saprotrophic fungi on Castanea sativa performance. Mycorrhiza. 22(1):41–49. doi:10.1007/s00572-011-0379-x.
Crossref Google Scholar
 

Pereira E, Santos A, Reis F, Tavares RM, Baptista P, Lino-Neto T, Almeida-Aguiar C. 2013. A new effective assay to detect antimicrobial activity of filamentous fungi. Microbiol Res. 168(1):1–5. doi:10.1016/j.micres.2012.06.008.
Crossref Google Scholar
 

Plamboeck AH, Dawson TE, Egerton-Warburton LM, North M, Bruns TD, Querejeta JI. 2007. Water transfer via ectomycorrhizal fungal hyphae to conifer seedlings. Mycorrhiza. 17(5):439–447. doi:10.1007/s00572-007-0119-4.
Crossref Google Scholar
 

Schalchli H, Hormazabal E, Becerra J, Birkett M, Alvear M, Vidal J, Quiroz A. 2011. Antifungal activity of volatile metabolites emitted by mycelial cultures of saprophytic fungi. Chem Ecol. 27(6):503–513. doi:10.1080/02757540.2011.596832.
Crossref Google Scholar
 

Schenkel D, Maciá-Vicente JG, Bissell A, Splivallo R. 2018. Fungi indirectly affect plant root architecture by modulating soil volatile organic compounds. Front Microbiol. 9:1847. doi:10.3389/fmicb.2018.01847.
Crossref Google Scholar
 

Shah F, Nicols C, Bentzer J, Ellstrom M, Smits M, Rineau F, Canbäck B, Floudas D, Carleer R, Lackner G, et al. 2015. Ectomycorrhizal fungi decompose soil organic matter using oxidative mechanisms adapted from saprotrophic ancestors. New Phytol. 209(4):1705–1719. doi:10.1111/nph.13722.
Crossref Google Scholar
 

Summerbell RC. 1987. The inhibitory effect of Trichoderma species and other soil microfungi on formation of mycorrhiza by Laccaria bicolor in vitro. New Phytol. 105(3):437–448. doi:10.1111/j.1469-8137.1987.tb00881.x.
Crossref Google Scholar
 

Ünal MÜ, Uçan F, Şener A, Dinçer S. 2012. Research on antifungal and inhibitory effects of DL-limonene on some yeasts. Turkish J Agric For. 36:576–582.
Google Scholar
 

Troncoso C, Becerra J, Bittner M, Perez C, Sáez K, Sánchez-Olate M, Ríos D. 2011. Chemical defense responses in Eucalyptus globulus (Labill) plants. J Chil Chem Soc. 56(3):768–770. doi:10.4067/S0717-97072011000300010.
Crossref Google Scholar
 

Tsuruta K, Yoshida Y, Kusumoto N, Sekine N, Ashitani T, Takahashi K. 2011. Inhibition activity of essential oils obtained from Japanese trees against Skeletonema costatum. J Wood Sci. 57(6):520–525. doi:10.1007/s10086-011-1209-7.
Crossref Google Scholar
 

Ujor VC, Monti M, Peiris DG, Clements MO, Hedger JN. 2012. The mycelial response of the white-rot fungus, Schizophyllum commune to the biocontrol agent, Trichoderma viride. Fungal Biol. 116(2):332–341. doi:10.1016/j.funbio.2011.12.008.
Crossref Google Scholar
 

Uwamori T, Inoue K, Kida C, Morita Y, Park P, Nakayashiki H, Kanematsu S, Ikeda K. 2015. Self- and nonself recognition during hyphal interactions in Rosellinia necatrix. J Gen Plant Pathol. 81(6):420–428. doi:10.1007/s10327-015-0622-y.
Crossref Google Scholar
 

van der Wal A, Geydan TD, Kuyper TW, De Boer W. 2013. A thready affair: linking fungal diversity and community dynamics to terrestrial decomposition processes. FEMS Microbiol Rev. 37(4):477–494. doi:10.1111/1574-6976.12001.
Crossref Google Scholar
 

Viant MR, Kurland IJ, Jones MR, Dunn WB. 2017. How close are we to complete annotation of metabolomes? Curr Opin Chem Biol. 36:64–69. doi:10.1016/j.cbpa.2017.01.001.
Crossref Google Scholar
 

Werner A, Zadworny M, Idzikowska K. 2002. Interaction between Laccaria laccata and Trichoderma virens in co-culture and in the rhizosphere of Pinus sylvestris grown in vitro. Mycorrhiza. 12(3):139–145. doi:10.1007/s00572-002-0159-8.
Crossref Google Scholar
 

Werner S, Polle A, Brinkmann N. 2016. Belowground communication: impacts of volatile organic compounds (VOCs) from soil fungi on other soil-inhabiting organisms. Appl Microbiol Biotechnol. 100(20):8651–8665. doi:10.1007/s00253-016-7792-1.
Crossref Google Scholar
 

Woods CM, Woodward S, Redfern DB. 2005. In vitro interactions in artificial and wood-based media between fungi colonizing stumps of Sitka spruce. For Pathol. 35(3):213–229. doi:10.1111/j.1439-0329.2005.00403.x.
Crossref Google Scholar
 

Zadworny M, Tuszyńska S, Samardakiewicz S, Werner A. 2007. Effects of mutual interaction of Laccaria laccata with Trichoderma harzianum and T. virens on the morphology of microtubules and mitochondria. Protoplasma. 232(1–2):45–53. doi:10.1007/s00709-007-0276-5.
Crossref Google Scholar
 

Zadworny M, Werner A, Idzikowska K. 2004. Behaviour of the hyphae of Laccaria laccata in the presence of Trichoderma harzianum in vitro. Mycorrhiza. 14:(6):401–405. doi:10.1007/s00572-004-0323-4.
Crossref Google Scholar
Mycology
Volume 12 Issue 3,
September 2021
Pages 216-229
DOI: 10.1080/21501203.2021.1876778
Cite this article:
Baptista P, de Pinho PG, Moreira N, et al. In vitro interactions between the ectomycorrhizal Pisolithus tinctorius and the saprotroph Hypholoma fasciculare fungi: morphological aspects and volatile production. Mycology, 2021, 12(3): 216-229. https://doi.org/10.1080/21501203.2021.1876778

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Received: 02 August 2020
Accepted: 11 January 2021
Published: 27 February 2021
© 2021 The Author(s).

This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
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