Skip to main content
Log in

Flavonoids induce germination of basidiospores of the ectomycorrhizal fungus Suillus bovinus

  • Original Paper
  • Published:
Mycorrhiza Aims and scope Submit manuscript

Abstract

Under laboratory conditions, spores of ectomycorrhizal fungi usually germinate very poorly or not at all. In a previous study, we showed that spores of the ectomycorrhizal fungus Suillus bovinus germinated through the combination of activated charcoal treatment of media and co-culture with seedlings of Pinus densiflora, which suggested that some substances contained in root exudates induced the germination. Among the compounds reported from root exudates, flavonoids have been elucidated to play various and substantial roles in plant–microbe interactions; we therefore investigated the effects of flavonoids on basidiospore germination of S. bovinus by the diffusion gradient assay on water agar plates pretreated with charcoal powder. Seven out of the 11 flavonoids tested, hesperidin, morin, rutin, quercitrin, naringenin, genistein, and chrysin, had greater effects than controls, whereas flavone, biochanin A, luteolin, and quercetin showed no positive effects. The effective concentration presumably corresponded to several micromolar levels, which was equivalent to those effective for pollen development, nod gene induction, and spore germination of F. solani f. sp. pisi and AM fungi. The results suggest that flavonoids play a role as signaling molecules in symbiotic relationships between woody plants and ectomycorrhizal fungi.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Aguilar JMM, Ashby AM, Richards AJM, Loake, GJ, Watson MD, Shaw CH (1988) Chemotaxis of Rhizobium leguminosarum biovar phaseoli towards flavonoid inducers of the symbiotic nodulation genes. J Gen Microbiol 134:2741–2746

    Google Scholar 

  • Ali NA, Jackson RM (1988) Effects of plant roots and their exudates on germination of spores of ectomycorrhizal fungi. Trans Br Mycol Soc 91:253–260

    Article  Google Scholar 

  • Armitage JP, Gallagher A, Johnson AWB (1988) Comparison of the chemotactic behaviour of Rhizobium leguminosarum with and without the nodulation plasmid. Mol Microbiol 2:743–748

    Article  CAS  PubMed  Google Scholar 

  • Barbour WM, Hattermann DR, Stacey G (1991) Chemotaxis of Bradyrhizobium japonicum to soybean exudates. Appl Environ Microbiol 57:2635–2639

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bauer WD, Caetano-Anollés G (1990) Chemotaxis, induced gene expression and competitiveness in the rhizosphere. Plant Soil 129:45–52

    Article  CAS  Google Scholar 

  • Bergemann SE, Miller SL (2002) Size, distribution, and persistence of genets in local populations of the late-stage ectomycorrhizal basidiomycete, Russula brevipes. New Phytol 156:313–320

    Article  CAS  Google Scholar 

  • Birraux D, Fries N (1981) Germination of Thelephora terrestris basidiospores. Can J Bot 59:2062–2064

    Article  Google Scholar 

  • Bjurman J (1984) An organic acid, inhibitory to spore germination of mycorrhizal fungi, formed from agar during autoclaving. Microbios 39:109–116

    Google Scholar 

  • Bjurman J, Fries N (1984) Purification and properties of the germination-inducing factor in the ectomycorrhizal fungus Leccinum aurantiacum (Boletaceae). Physiol Plant 62:465–471

    Article  CAS  Google Scholar 

  • Bowen GD, Theodorou C (1973) Growth of ectomycorrhizal fungi around seeds and roots. In: Marx GC, Kozlowski TT (eds) Ectomycorrhizae: their ecology and physiology. Academic, New York, USA, pp 107–150

    Chapter  Google Scholar 

  • Brencic A, Winans SC (2005) Detection of and response to signals involved in host–microbe interactions by plant-associated bacteria. Microbiol Mol Biol Rev 69:155–194

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burg D, Guillaume J, Tailliez R (1982) Chemotaxis by Rhizobium meliloti. Arch Microbiol 133:162–163

    Article  CAS  Google Scholar 

  • Caetano-Anollés G, Crist-Estes DK, Bauer WD (1988) Chemotaxis of Rhizobium meliloti to the plant flavone luteolin requires functional nodulation genes. J Bacteriol 170:3164–3169

    Article  PubMed  PubMed Central  Google Scholar 

  • Carlile MJ (1983) Motility, taxis, and tropism in Phytophthora. In: Erwin DC, Bartnicki-Garcia S, Tsao PH (eds) Phytophthora—its biology, taxonomy, ecology and pathology. APS, St. Paul, USA, pp 95–107

    Google Scholar 

  • Cooper JE (2004) Multiple responses of rhizobia to flavonoids during legume root infection. Adv Bot Res 41:1–62

    Article  CAS  Google Scholar 

  • Dharmatilake AJ, Bauer WD (1992) Chemotaxis or Rhizobium meliloti towards nodulation gene inducer compounds from alfalfa roots. Appl Environ Microbiol 58:1153–1158

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fiore-Donno A-M, Martin F (2001) Populations of ectomycorrhizal Laccaria amethystina and Xerocomos spp. show contrasting colonization patterns in a mixed forest. New Phytol 152:533–542

    Article  CAS  Google Scholar 

  • Fries N (1976) Spore germination in Boletus induced by amino acids. Proc K Ned Akad Wet Ser C 79:142–146

    Google Scholar 

  • Fries N (1978) Basidiospore germination in some mycorrhiza-forming hymenomycetes. Trans Br Mycol Soc 70:319–324

    Article  Google Scholar 

  • Fries N (1983a) Spore germination, homing reaction, and intersterility groups in Laccaria laccata (Agaricales). Mycologia 75:221–227

    Article  Google Scholar 

  • Fries N (1983b) Basidiospore germination in species of Boletaceae. Mycotaxon 18:345–354

    Google Scholar 

  • Fries N (1984) Spore germination in the higher Basidiomycetes. Proc Indian Acad Sci Plant Sci 93:205–222

    Google Scholar 

  • Fries N (1987) Ecological and evolutionary aspects of spore germination in the higher basidiomycetes. Trans Br Mycol Soc 88:1–7

    Article  Google Scholar 

  • Fries N (1988) Specific effects of diterpene resin acids on spore germination of ectomycorrhizal basidiomycetes. Experientia 44:1027–1030

    Article  CAS  Google Scholar 

  • Fries N (1989) The influence of tree roots on spore germination of ectomycorrhizal fungi. Agric Ecosyst Environ 28:139–144

    Article  Google Scholar 

  • Fries N, Birraux D (1980) Spore germination in Hebeloma stimulated by living plant roots. Experientia 36:1056–1057

    Article  Google Scholar 

  • Fries N, Swedjemark G (1986) Specific effects of tree roots on spore germination in the ectomycorrhizal fungus, Hebeloma mesophaeum (Agaricales). In: Gianninazzi-Pearson V, Gianninazzi S (eds) Physiological and genetical aspects of mycorrhizae. INRA, Paris, France, pp 725–730

    Google Scholar 

  • Fries N, Serck-Hanssen K, Dimberg LH, Theander O (1987) Abietic acid, an activator of basidiospore germination in ectomycorrhizal species of the genus Suillus (Boletaceae). Exp Mycol 11:360–363

    Article  Google Scholar 

  • Gherbi H, Delaruelle C, Selosse M-A, Martin F (1999) High genetic diversity in a population of the ectomycorrhizal basidiomycete Laccaria amethystina in a 150-year-old beech forest. Mol Ecol 8:2003–2013

    Article  CAS  PubMed  Google Scholar 

  • Gianinazzi-Pearson V, Branzanti B, Gianinazzi S (1989) In vitro enhancement of spore germination and early hyphal growth of a vesicular–arbuscular mycorrhizal fungus by host root exudates and plant flavonoids. Symbiosis 7:243–255

    CAS  Google Scholar 

  • Gould KS, Lister C (2005) Flavonoid functions in plants. In: Andersen ØM, Markham KR (eds) Flavonoids—chemistry, biochemistry and applications. Taylor & Francis, Boca Raton, USA, pp 397–441

    Chapter  Google Scholar 

  • Gryta H, Debaud J-C, Effosse A, Gay G, Marmeisse R (1997) Fine-scale structure of populations of the ectomycorrhizal fungus Hebeloma cylindrosporum in coastal sand dune forest ecosystems. Mol Ecol 6:353–364

    Article  Google Scholar 

  • Hartwig UA, Joseph CM, Phillips DA (1991) Flavonoids released naturally from alfalfa seeds enhance growth rate of Rhizobium meliloti. Plant Physiol 95:797–803

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Horio T, Kawabata Y, Takayama T, Tahara S, Kawabata J, Fukushi Y, Nishimura H, Mizutani J (1992) A potent attractant of zoospores of Aphanomyces cochlioides isolated from its host, Spinacia oleracea. Experientia 48:410–414

    Article  CAS  Google Scholar 

  • Huai W-X, Guo L-D, He W (2003) Genetic diversity of an ectomycorrhizal fungus Tricholoma terreum in a Larix principis-rupprechtii stand assessed using random amplified polymorphic DNA. Mycorrhiza 13:265–270

    Article  PubMed  Google Scholar 

  • Iwase K (1992) Induction of basidiospore germination by gluconic acid in the ectomycorrhizal fungus Tricholoma robustum. Can J Bot 70:1234–1238

    Article  CAS  Google Scholar 

  • Kape R, Parniske M, Werner D (1991) Chemotaxis and nod gene activity of Bradyrhizobium japonicum in response to hydroxycinnamic acids and isoflavonoids. Appl Environ Microbiol 57:316–319

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kikuchi K, Matsushita N, Suzuki K (2006) Germination of Suillus bovinus spores in vitro. Nippon Kingakukai Kaiho 47:37–40 (in Japanese with summary in English)

    Google Scholar 

  • Kope HH, Fortin JA (1990) Germination and comparative morphology of basidiospores of Pisolithus arhizus. Mycologia 82:350–357

    Article  Google Scholar 

  • Lagrange H, Jay-Allgmand C, Lapeyrie F (2001) Rutin, the phenolglycoside from eucalyptus root exudates, stimulates Pisolithus hyphal growth at picomolar concentrations. New Phytol 149:349–355

    Article  CAS  Google Scholar 

  • Liang Y, Guo L, Ma K (2005) Population genetic structure of an ectomycorrhizal fungus Amanita manginiana in a subtropical forest over two years. Mycorrhiza 15:137–142

    Article  PubMed  Google Scholar 

  • Melin E (1962) Physiological aspects of mycorrhizae of forest trees. In: Kozlowski TT (ed) Tree growth. Ronald Press, New York, USA, pp 247–263

    Google Scholar 

  • Miller SL, Torres P, McClean TM (1993) Basidiospore viability and germination in ectomycorrhizal and saprotrophic basidiomycetes. Mycol Res 97:141–149

    Article  Google Scholar 

  • Mo Y, Nagel C, Taylor LP (1992) Biochemical complementation of chalcone synthase mutants defines a role for flavonoids in functional pollen. Proc Natl Acad Sci U S A 89:7213–7217

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morris PF, Ward EWB (1992) Chemoattraction of zoospores of the soybean pathogen, Phytophthora sojae, by isoflavones. Physiol Mol Plant Pathol 40:17–22

    Article  CAS  Google Scholar 

  • Nagahashi G, Douds DD Jr (1999) Rapid and sensitive bioassay to study signals between root exudates and arbuscular mycorrhizal fungi. Biotechnol Tech 13:893–897

    Article  CAS  Google Scholar 

  • Ohta A (1986) Basidiospore germination of Tricholoma matsutake (I). Effects of organic acids on swelling and germination of the basidiospores. Trans Mycol Soc Jpn 27:167–173

    CAS  Google Scholar 

  • Ohta A (1988) Effects of butyric acid and related compounds on basidiospore germination of some ectomycorrhizal fungi. Trans Mycol Soc Jpn 29:375–381

    CAS  Google Scholar 

  • Oort AJP (1974) Activation of spore germination in Lactarius species by volatile compounds of Ceratocystis fagacearum. Proc K Ned Akad Wet Ser C 77:301–307

    Google Scholar 

  • Parke D, Rivelli M, Ornston LN (1985) Chemotaxis to aromatic and hydroaromatic acids: comparison of Bradyrhizobium japonicum and Rhizobium trifolii. J Bacteriol 163:417–422

    CAS  PubMed  PubMed Central  Google Scholar 

  • Peck MC, Fisher RF, Long SR (2006) Diverse flavonoids stimulate NodD1 binding to nod gene promoters in Sinorhizobium meliloti. J Bacteriol 188:5417–5427

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peters NK, Long SR (1988) Alfalfa root exudate and compounds which promote or inhibit induction of Rhizobium meliloti nodulation genes. Plant Physiol 88:396–400

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peters NK, Frost JW, Long SR (1986) A plant flavone, luteolin, induces expression of Rhizobium meliloti nodulation genes. Science 233:977–980

    Article  CAS  PubMed  Google Scholar 

  • R Development Core Team (2005) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org

  • Redecker D, Szaro TM, Bowman RJ, Bruns TD (2001) Small genets of Lactarius xanthogalactus, Russula cremoricolor and Amanita fracheti in late-stage ectomycorrhizal successions. Mol Ecol 10:1025–1034

    Article  CAS  PubMed  Google Scholar 

  • Redmond JW, Batley M, Djordjevic MA, Innes RW, Kuempel PL, Rolfe BG (1986) Flavones induce expression of nodulation genes in Rhizobium. Nature 323:632–635

    Article  CAS  Google Scholar 

  • Rolfe BG (1988) Flavones and isoflavones as inducing substances of legume nodulation. Biofactors 1:3–10

    CAS  PubMed  Google Scholar 

  • Ruan Y, Kotraiah V, Straney DC (1995) Flavonoids stimulate spore germination in Fusarium solani pathogenic on legumes in a manner sensitive to inhibitors of cAMP-dependent protein kinase. Mol Plant Microbe Interact 8:929–938

    Article  CAS  Google Scholar 

  • Scervino JM, Ponce MA, Erra-Bassells R, Vierheilig H, Ocampo JA, Godeas A (2005) Flavonoids exhibit fungal species and genus specific effects on the presymbiotic growth of Gigaspora and Glomus. Mycol Res 109:789–794

    Article  CAS  PubMed  Google Scholar 

  • Scheidemann P, Wetzel A (1997) Identification and characterization of flavonoids in the root exudate of Robinia pseudoacacia. Trees 11:316–321

    Google Scholar 

  • Sekizaki H, Yokosawa R (1988) Studies on zoospore-attracting activity. I. Synthesis of isoflavones and their attracting activity to Aphanomyces euteiches zoospore. Chem Pharm Bull 36:4876–4880

    Article  CAS  Google Scholar 

  • Sekizaki H, Yokosawa R, Chinen C, Adachi H, Yamane Y (1993) Studies on zoospore attracting activity. II. Synthesis of isoflavones and their attracting activity to Aphanomyces euteiches zoospore. Biol Pharm Bull 16:698–701

    Article  CAS  PubMed  Google Scholar 

  • Spaink HP, Kondorosi A, Hooykaas PJJ (eds) (1998) The rhizobiaceae. Kluwer, Dordrecht, Netherlands

    Google Scholar 

  • Theodorou C, Bowen GD (1987) Germination of basidiospores of mycorrhizal fungi in the rhizosphere of Pinus radiata D. Don. New Phytol 106:217–223

    Article  Google Scholar 

  • Uren NC (2001) Types, amounts, and possible functions of compounds released into the rhizosphere by soil-grown plants. In: Pinton R, Varanini Z, Nannipieri, P (eds) The rhizosphere. Marcel Decker, New York, USA, pp 19–40

    Google Scholar 

  • Vierheilig H, Bago B, Albrecht C, Poulin M-J, Piché Y (1998) Flavonoids and arbuscular-mycorrhizal fungi. In: Manthey J, Buslig B (eds) Flavonoids in the living system. Plenum, New York, USA, pp 9–33

    Chapter  Google Scholar 

  • Ylstra B, Touraev A, Bentino Moreno RM, Stöger E, van Tunen AJ, Vicente O, Mol JNM, Heberle-Bors E (1992) Flavonols stimulate development, germination, and tube growth of tobacco pollen. Plant Physiol 100:902–907

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yokosawa R, Kuninaga S, Sekizaki H (1986) Aphanomyces euteiches zoospore attractant isolated from pea root: prunetin. Ann Phytopathol Soc Jpn 52:809–816

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank Mr. Masahiro Kake and Mr. Yasuharu Kake of Nisshin Ringyo Ltd. for kindly providing the research site. This research was financially supported in part by Grants-in-Aid from the Ministry of Education, Culture, Sports, Science, and Technology of Japan.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kensuke Kikuchi.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kikuchi, K., Matsushita, N., Suzuki, K. et al. Flavonoids induce germination of basidiospores of the ectomycorrhizal fungus Suillus bovinus . Mycorrhiza 17, 563–570 (2007). https://doi.org/10.1007/s00572-007-0131-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00572-007-0131-8

Keywords

Navigation