Abstract
Ectomycorrhizal (ECM) symbiosis plays a major role in nutrient cycling and the functioning of forest ecosystems. Trees with well-developed ectomycorrhizas are more resistant to environmental stresses such as drought and to biotic stresses such as root pathogens. The establishment of ECM symbiosis is triggered by signals produced by both partners. These signals lead to morphological changes and a complex development of specific structures in both the plant root and the fungus. The development of the ECM fungi, Paxillus involutus and Pisolithus arhizus, in the presence and the absence of the symbiont—Pinus pinaster—was evaluated as well as their antioxidant properties and phenolic compounds composition in response to the symbiotic association. ECM fungi grew less in the presence of P. pinaster, with P. arhizus being less affected in growth and thus being more adapted to this association. Protocatechuic acid was found only in P. involutus, while P. pinaster roots, both in association and isolated, proved to have other phenolic acids, such as p-hydroxybenzoic and p-coumaric acids. The symbiosis between P. involutus and P. pinaster had no major effects on the symbionts, while the association between P. arhizus and P. pinaster seems to generally decrease the antioxidant effects of both symbionts, despite the increase in p-coumaric and cinnamic acids in the ECM fungi.
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References
Amarowicz R, Pegg RB, Rahimi-Moghaddam P, Barl B, Weil JA (2004) Free-radical scavenging capacity and antioxidant activity of selected plant species from the Canadian prairies. Food Chem 84:551–562
Baptista P, Martins A, Pais MS, Tavares RM, Lino-Neto T (2007) Involvement of reactive oxygen species during early stages of ectomycorrhiza establishment between Castanea sativa and Pisolithus tinctorius. Mycorrhiza 17:185–193
Barros L, Dueñas M, Ferreira ICFR, Baptista P, Santos-Buelga C (2009) Phenolic acids determination by HPLC-DAD-ESI/MS in sixteen different Portuguese wild mushrooms species. Food Chem Toxicol 47:1076–1079
Benguria RL (1985) Mil setas ibéricas. In: Bilbao (ed) Flash composition
Ditengou FA, Lapeyrie F (2000) Hypaphorine from the ectomycorrhizal fungus Pisolithus tinctorius counteracts activities of indole-3-acetic acid and ethylene but not synthetic auxins in eucalypt seedlings. Mol Plant Microbe Inter 13:151–158
Ebel J (1986) Phytoalexin synthesis: the biochemical analysis of the induction process. Annu Rev Phytopathol 24:235–264
Ferreira ICFR, Barros L, Abreu RMV (2009) Antioxidants in wild mushrooms. Curr Med Chem 16:1543–1560
Finlay R, Lindahl B, Taylor AFS (2008) Responses of mycorrhizal fungi to stress. In: Avery SV, Stratford M, van West P (eds) Stress in yeasts and filamentous fungi. Macmillan, United Kingdom
Gutierrez RMP, Luna HH, Garrido SH (2006) Antioxidant activity of Tagetes erecta essential oil. J Chil Chem Soc 51:883–886
Haars A, Chet J, Hüttermann A (1981) Effect of phenolic compounds and tannin on growth and laccase activity of Fomes annosus. Eur J Plant Pathol 11:6–76
Heleno SA, Barros L, Sousa MJ, Martins A, Ferreira ICFR (2010) Tocopherols composition of Portuguese wild mushrooms with antioxidant capacity. Food Chem 119:1443–1450
Heller G, Adomas A, Li G, Osborne J, Zyl L, Sederoff R, Finlay RD, Stenlid J, Asiegbu FO (2008) Transcriptional analysis of Pinus sylvestris roots challenged with the ectomycorrhizal fungus Laccaria bicolor. BMC Plant Biol 8:19
Karadag A, Ozcelik B, Saner S (2009) Review of methods to determine antioxidant capacities. Food Anal Methods 2:41–60
Lamb C, Dixon RA (1997) The oxidative burst in plant disease resistance. Annu Rev Plant Physiol Plant Mol Biol 48:251–275
Lindeberg G (1948) On the occurrence of polyphenol oxidase in soil inhabiting basidiomycetes. Physiol Plant 1:196–205
Macheix J, Fleuriet A (1998) Flavonoids in health and disease. Marcel Dekker, New York
Magalhães LM, Segundo MA, Reis S, Lima JLFC (2008) Methodological aspects about in vitro evaluation of antioxidant properties. Anal Chim Acta 613:1–19
Malajczuk N, Molina R, Trappe JM (1984) Ectomycorrhiza formation in Eucalyptus. II. The ultrastructure of compatible and incompatible mycorrhizal fungi and associated roots. New Phytol 96:43–53
Martin F, Duplessis S, Ditengou F, Lagrange H, Voiblet C, Lapeyrie F (2001) Developmental cross talking in the ectomycorrhizal symbiosis: signals and communication genes. New Phytol 151:145–154
Marx DH (1969) The influence of ectotrophic fungi on the resistance of pine roots to pathogenic infections. I. Antagonism of mycorrhizal fungi to root pathogenic fungi and soil bacteria. Phytopathology 59:153–163
Molina R, Trappe J (1984) Mycorrhiza Management in Bareroot Nurseries. In: Duryea ML, Landis TD (eds) Forest nursery manual: production of bareroot seedlings. M. Nijhoff/Dr W. Junk Publishers. The Hague/Boston/Lancaster, for Forest Research Laboratory, Oregon State University. Corvallis
Münzenberger B, Heilemann J, Strack D, Kottke I, Oberwinkler F (1990) Phenolics of mycorrhizas and non-mycorrhizal roots of Norway spruce. Planta 182:142–148
Münzenberger B, Kottke I, Oberwinkler F (1995) Reduction of phenolics in mycorrhizas of Larix decidua Mill. Tree Physiol 15:191–196
Münzenberger B, Otter T, Wüstrich D, Polle A (1997) Peroxidase and laccase activities in mycorrhizal and non-mycorrhizal fine roots of Norway spruce (Picea abies) and larch (Larix decidua). Can J Bot 78:932–938
Mysore KS, Ryu C-M (2004) Nonhost resistance: how much do we know? Trends Plant Sci 9:97–104
Olsen RA, Odham G, Lindeberg G (1971) Aromatic substances in leaves of Populus tremula as inhibitors of mycorrhizal fungi. Physiol Plant 25:122–129
Podila GK (2002) Signalling in mycorrhizal symbioses—elegant mutants lead the way. New Phytol 154:541–551
Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic Press, San Diego
Wacker TL, Safir GR, Stephens CT (1990) Effects of ferulic acid on Glomus fasciculatum and associated effects on phosphorus uptake and growth of asparagus (Asparagus officinalis L.). J Chem Ecol 16:901–909
Acknowledgments
The authors are grateful to the Foundation for Science and Technology (Portugal) and COMPETE/QREN/UE for financial support through the research project PTDC/AGR-ALI/110062/2009 and L. Barros grant (SFRH/BPD/4609/2008). The GIP-USAL is financially supported by the Spanish Ministerio de Ciencia e Innovación through the Consolider-Ingenio 2010 Programme (FUN-C-FOOD, CSD2007-00063), and Junta de Castilla y León (Grupo de Investigación de Excelencia, GR133).
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Reis, F.S., Ferreira, I.C.F.R., Barros, L. et al. Mycorrhizal induction of phenolic compounds and antioxidant properties of fungi and seedlings during the early steps of symbiosis. Chemoecology 21, 151–159 (2011). https://doi.org/10.1007/s00049-011-0079-1
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DOI: https://doi.org/10.1007/s00049-011-0079-1