Abstract
Arbuscular mycorrhizal (AM) fungi form mutualistic, symbiotic associations with the roots of more than 80% of land plants1. The fungi are incapable of completing their life cycle in the absence of a host root. Their spores can germinate and grow in the absence of a host, but their hyphal growth is very limited. Little is known about the molecular mechanisms that govern signalling and recognition between AM fungi and their host plants. In one of the first stages of host recognition, the hyphae of AM fungi show extensive branching in the vicinity of host roots before formation of the appressorium2,3,4, the structure used to penetrate the plant root. Host roots are known to release signalling molecules that trigger hyphal branching5,6,7, but these branching factors have not been isolated. Here we have isolated a branching factor from the root exudates of Lotus japonicus and used spectroscopic analysis and chemical synthesis to identify it as a strigolactone, 5-deoxy-strigol. Strigolactones are a group of sesquiterpene lactones, previously isolated as seed-germination stimulants for the parasitic weeds Striga and Orobanche8. The natural strigolactones 5-deoxy-strigol, sorgolactone and strigol, and a synthetic analogue, GR24, induced extensive hyphal branching in germinating spores of the AM fungus Gigaspora margarita at very low concentrations.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Smith, S. E. & Read, D. J. Mycorrhizal Symbiosis (Academic, San Diego, 1997)
Mosse, B. & Hepper, C. Vesicular-arbuscular mycorrhizal infections in root organ cultures. Physiol. Plant Pathol. 5, 215–223 (1975)
Giovannetti, M., Sbrana, C., Avio, L., Citernesi, A. S. & Logi, C. Differential hyphal morphogenesis in arbuscular mycorrhizal fungi during preinfection stages. New Phytol. 125, 587–593 (1993)
Giovannetti, M., Sbrana, C. & Logi, C. Early process involved in host recognition by arbuscular mycorrhizal fungi. New Phytol. 127, 703–709 (1994)
Giovannetti, M., Sbrana, C., Silvia, A. & Avio, L. Analysis of factors involved in fungal recognition response to host-derived signals by arbuscular mycorrhizal fungi. New Phytol. 133, 65–71 (1996)
Buee, M., Rossignol, M., Jauneau, A., Ranjeva, R. & Bécard, G. The pre-symbiotic growth of arbuscular mycorrhizal fungi is induced by a branching factor partially purified from plant root exudates. Mol. Plant Microbe Interact. 13, 693–698 (2000)
Nagahashi, G. & Douds, D. D. Partial separation of root exudate compounds and their effects upon the growth of germinated spores of AM fungi. Mycol. Res. 104, 1453–1464 (2000)
Bouwmeester, H. J., Matusova, R., Zhongkui, S. & Beale, M. H. Secondary metabolite signalling in host-parasitic plant interactions. Curr. Opin. Plant Biol. 6, 358–364 (2003)
Schussler, A., Schwarzott, D. & Walker, C. A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol. Res. 105, 1413–1421 (2001)
Nagahashi, G. & Douds, D. D. A rapid and sensitive bioassay with practical application for studies on interactions between root exudates and arbuscular mycorrhizal fungi. Biotechnol. Tech. 13, 893–897 (1999)
Tamasloukht, M. et al. Root factors induce mitochondrial-related gene expression and fungal respiration during the developmental switch from asymbiosis to presymbiosis in the arbuscular mycorrhizal fungus Gigaspora rosea. Plant Physiol. 131, 1468–1478 (2003)
Cook, C. E., Whichard, L. P., Turner, B., Wall, M. E. & Egley, G. H. Germination of witchweed (Striga lutea Lour.): Isolation and properties of a potent stimulant. Science 154, 1189–1190 (1966)
Cook, C. E. et al. Germination stimulants. II. The structure of strigol—A potent seed germination stimulant for witchweed (Striga lutea Lour.). J. Am. Chem. Soc. 94, 6198–6199 (1972)
Hauck, C., Müller, S. & Schildknecht, H. A germination stimulant for parasitic flowering plants from Sorghum bicolor, a genuine host plant. J. Plant Physiol. 139, 474–478 (1992)
Müller, S., Hauck, C. & Schildknecht, H. Germination stimulants produced by Vigna unguiculata Walp cv Saunders Upright. J. Plant Growth Regul. 11, 77–84 (1992)
Siame, B. A., Weerasuriya, Y., Wood, K., Ejeta, G. & Butler, L. Isolation of strigol, a germination stimulant for Striga asiatica, from host plants. J. Agric. Food Chem. 41, 1486–1491 (1993)
Yokota, T., Sakai, H., Okuno, K., Yoneyama, K. & Takeuchi, Y. Alectrol and orobanchol, germination stimulants for Orobanche minor, from its host red clover. Phytochemistry 49, 1967–1973 (1998)
Johnson, A. W. et al. The preparation of synthetic analogues of strigol. J. Chem. Soc. Perkin Trans. I 1981, 1734–1743 (1981)
Frischmuth, K. et al. Routes to derivatives of strigol (the witchweed germination factor) modified in the 5-position. Tetrahedron 47, 9793–9806 (1991)
Bergmann, C. et al. Stimulation of Orobanche crenata seed germination by (+ )-strigol and structural analogues dependence on constitution and configuration of the germination stimulants. J. Plant Physiol. 142, 338–342 (1993)
Sugimoto, Y., Wigchert, S. C. M., Thuring, J. W. J. F. & Zwanenburg, B. Synthesis of all eight stereoisomers of the germination stimulant sorgolactone. J. Org. Chem. 63, 1259–1267 (1998)
Nakano, S., Todoroki, Y., Hirai, N. & Ohigashi, H. Synthesis and biological activity of 7′-, 8′-, and 9′-alkyl analogues of abscisic acid. Biosci. Biotechnol. Biochem. 59, 1699–1706 (1995)
Brooks, D. W., Bevinakatti, H. S. & Powell, D. R. The absolute structure of (+ )-strigol. J. Org. Chem. 50, 3779–3781 (1985)
Yasuda, N., Sugimoto, Y., Kato, M., Inanaga, S. & Yoneyama, K. (+ )-Strigol, a witchweed seed germination stimulant, from Menispermum dauricum root culture. Phytochemistry 62, 1115–1119 (2003)
Mangnus, E. M. & Zwanenburg, B. Tentative molecular mechanisms for germination stimulation of Striga and Orobanche seeds by strigol and its synthetic analogues. J. Agric. Food Chem. 40, 1066–1070 (1992)
Westwood, J. H. Characterization of the Orobanche-Arabidopsis system for studying parasite-host interactions. Weed Sci. 48, 742–748 (2000)
Sato, D. et al. Analysis of strigolactones, germination stimulants for Striga and Orobanche, by high-performance liquid chromatography/tandem mass spectrometry. J. Agric. Food Chem. 51, 1162–1168 (2003)
Yoneyama, K., Takeuchi, Y. & Yokota, T. Production of clover broomrape seed germination stimulants by red clover requires nitrate but is inhibited by phosphate and ammonium. Physiol. Plant. 112, 25–30 (2001)
Parniske, M. Molecular genetics of the arbuscular mycorrhizal symbiosis. Curr. Opin. Plant Biol. 7, 414–421 (2004)
Bécard, G. & Fortin, J. A. Early events of vesicular-arbuscular mycorrhiza formation on Ri T-DNA transformed roots. New Phytol. 108, 211–218 (1998)
Acknowledgements
We thank M. Kawaguchi for discussions and critical reading of the manuscript, Y. Sugimoto for providing (± )-sorgolactone, GR24 and (+ )-strigol, and K. Yoneyama for discussions and critical reading of the manuscript. This work was supported by Core Research for Evolutional Science and Technology (CREST), Japan Science and Technology Agency, and a Grant-in-Aid for Scientific Research from the Ministry of Education, Science, Sports and Culture of Japan.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.
Supplementary information
Supplementary Table S1
Table of physicochemical data for synthetic (±)-5-deoxy-strigol. (DOC 20 kb)
Rights and permissions
About this article
Cite this article
Akiyama, K., Matsuzaki, Ki. & Hayashi, H. Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435, 824–827 (2005). https://doi.org/10.1038/nature03608
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1038/nature03608
This article is cited by
-
Role of soil abiotic processes on phosphorus availability and plant responses with a focus on strigolactones in tomato plants
Plant and Soil (2024)
-
Strigolactones and abscisic acid interactions affect plant development and response to abiotic stresses
BMC Plant Biology (2023)
-
Fertilization controls tiller numbers via transcriptional regulation of a MAX1-like gene in rice cultivation
Nature Communications (2023)
-
Plant latent defense response against compatibility
The ISME Journal (2023)
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.