Seasonal and environmental changes of mycorrhizal associations and heterotrophy levels in mixotrophic Pyrola japonica (Ericaceae) growing under different light environments

American Journal of Botany

Volumn 99, Issue 7, 2012, Pages 1177-1188

  Matsuda, Yosuke ^a   Shimizu, Shoko ^a   Mori, Manami ^a   Ito, Shin Ichiro ^a   Selosse, Marc André ^b  

^a MIE UNIVERSITY   (Japan)

^b CENTRE D ECOLOGIE FONCTIONNELLE ET EVOLUTIVE   (France)

Author keywords

Arbutoid mycorrhiza; Ericaceae; Hyphal coils; ITS barcoding; Partial mycoheterotrophy; Plant response to light; Pyrola japonica; Russula; Stable isotopes

Indexed keywords

CARBON;

BROAD-LEAVED FOREST; COLONIZATION; DECIDUOUS FOREST; DICOTYLEDON; ECTOMYCORRHIZA; ENVIRONMENTAL CHANGE; HETEROTROPHY; LIGHT AVAILABILITY; MIXOTROPHY; PHOTOSYNTHESIS; SEASONAL VARIATION; STABLE ISOTOPE;

ARTICLE; AUTOTROPHY; CYTOLOGY; DARKNESS; ERICACEAE; GENETICS; HETEROTROPHY; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; MYCORRHIZA; SEASON; SYMBIOSIS;

AUTOTROPHIC PROCESSES; CARBON ISOTOPES; DARKNESS; ERICACEAE; HETEROTROPHIC PROCESSES; MYCORRHIZAE; SEASONS; SYMBIOSIS;

ERICACEAE; FUNGI; ORTHILIA; PYROLA; PYROLA JAPONICA; PYROLEAE; RUSSULA;

EID: 84863871011     PISSN: 00029122     EISSN: None     Source Type: Journal    
DOI: 10.3732/ajb.1100546     Document Type: Article

References (61)

1. Abadie, J. C., Ü. Püttsepp, G. Gebauer, A. Faccio, P. Bonfante, and M.-A. Selosse. 2006. Cephalanthera longifolia (Neottieae, Orchidaceae) is mixotrophic: A comparative study between green and nonphotosynthetic individuals. Canadian Journal of Botany 84: 1462-1477.
2. Altschul, S. F., T. L. Madden, A. A. Schaffer, J. Zhang, Z. Zhang, W. Miller, and D. J. Lipman. 1997. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Research 25: 3389-3402.
3. Bidartondo, M. I., and T. D. Bruns. 2001. Extreme specificity in epiparasitic Monotropoideae (Ericaceae): Widespread phylogenetic and geographical structure. Molecular Ecology 10: 2285-2295.
4. Bidartondo, M. I., and T. D. Bruns. 2002. Fine-level mycorrhizal specificity in the Monotropoideae (Ericaceae): Specificity for fungal species groups. Molecular Ecology 11: 557-569.
5. Bidartondo, M. I., B. Burghardt, G. Gebauer, T. D. Bruns, and D. J. Read. 2004. Changing partners in the dark: Isotopic and molecular evidence of ectomycorrhizal liaisons between forest orchids and trees. Proceedings of the Royal Society of London, B, Biological Sciences 271: 1799-1806.
6. Bougoure, D. S., P. I. Parkin, J. W. G. Cairney, I. J. Alexander, and I. C. Anderson. 2007. Diversity of fungi in hair roots of Ericaceae varies along a vegetation gradient. Molecular Ecology 16: 4624-4636.
7. Broadmeadow, M. S. J., H. Griffiths, C. Maxwell, and A. M. Borland. 1992. The carbon isotope ratio of plant organic material reflects temporal and spatial variations in CO 2 within tropical forest formations in Trinidad. Oecologia 89: 435-441.
8. Cameron, D. D., K. Preiss, G. Gebauer, and D. J. Read. 2009. The chlorophyll-containing orchid Corallorhiza trifida derives little carbon through photosynthesis. New Phytologist 183: 358-364.
9. Dearnaley, J. D. W., F. Martos, and M.-A. Selosse. 2012. Orchid mycorrhizas: Molecular ecology, physiology, evolution and conservation aspects. In B. Hock [ed.], The Mycota IX, Fungal associations, 2nd ed., in press. Springer-Verlag, Berlin, Germany.
10. Farquhar, G. D., J. R. Ehleringer, and K. T. Hubick. 1989. Carbon isotope discrimination and photosynthesis. Annual Review of Plant Physiology 40: 503-537.
11. Felsenstein, J. 1985. Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39: 783-791.
12. Freudenstein, J. V. 1999. Relationships and character transformation in Pyroloideae (Ericaceae) based on ITS sequences, morphology, and development. Systematic Botany 24: 398-408.
13. Gardes, M., and T. D. Bruns. 1993. ITS primers with enhanced specificity for basidiomycetes: Application to the identification of mycorrhizae and rusts. Molecular Ecology 2: 113-118.
14. Gebauer, G., and M. Meyer. 2003. 15 N and 13 C natural abundance of autotrophic and mycoheterotrophic orchids provides insight into nitrogen and carbon gain from fungal association. New Phytologist 160: 209-223.
15. Girlanda, M., M.-A. Selosse, D. Cafasso, F. Brilli, S. Delfine, R. Fabbian, S. Ghignone, et al. 2006. Inefficient photosynthesis in the Mediterranean orchid Limodorum abortivum is mirrored by specific association to ectomycorrhizal Russulaceae. Molecular Ecology 15: 491-504.
16. Hashimoto, Y., S. Fukukawa, A. Kunishi, H. Suga, M. Sauve, F. Richard, and M.-A. Selosse. 2012. Mycoheterotrophic germination of Pyrola asarifolia dust seeds reveals convergences with germination in orchids. New Phytologist 56: in press. doi: 10.1111/j.1469-8137.2012.04174.x
17. Hashimoto, Y., A. Kunishi, and S. H asegawa. 2005. Interspecific C transfers from Larix kampferi Carr. to Pyrola incarnate Fischer by way of mycorrhizal fungi. Inoculum 56: 23-24 (Supplement to Mycologia).
18. Henderson, M. W. 1919. A comparative study of the structure and saprophytism of the Pyrolaceae and the Monotropaceae with reference to their derivation from the Ericaceae. Contributions of the Botanical Laboratory of the University of Pennsylvania 5: 42-109.
19. Hopple, J. S., and R. Vilgalys. 1994. Phylogenetic relationships among coprinoid taxa and allies based on data from restriction site mapping of nuclear rDNA. Mycologia 86: 96-107.
20. Hunt, R., and J. F. Hope-Simpson. 1990. Growth of Pyrola rotundifolia ssp. maritima in relation to shade. New Phytologist 114: 129-137.
21. Hynson, N. A., and T. D. Bruns. 2009. Evidence of a myco-heterotroph in the plant family Ericaceae that lacks mycorrhizal specificity. Proceedings of the Royal Society of London, B, Biological Sciences 276: 4053-4059.
22. Hynson, N. A., S. Mambelli, A. S. Amend, and T. E. Dawson. 2012. Measuring carbon gains from fungal networks in understory plants from the tribe Pyroleae (Ericaceae): A field manipulation and stable isotope approach. Oecologia 169: 307-317.
23. Hynson, N. A., K. Preiss, G. Gebauer, and T. D. Bruns. 2009. Isotopic evidence of full and partial myco-heterotrophy in the plant tribe Pyroleae (Ericaceae). New Phytologist 182: 719-726.
24. Julou, T., B. Burghardt, G. Gebauer, D. Berveiller, C. Damesin, and M.-A. Selosse. 2005. Mixotrophy in orchids: Insights from a comparative study of green individuals and non-photosynthetic individuals of Cephalanthera damasonium. New Phytologist 166: 639-653.
25. Kitamura, S., G. Murata, and M. Hori. 1957. Colored illustrations of herbaceous plants of Japan, vol. I (Sympetalae). Hoikusha, Osaka, Japan.
26. Koizumi, H. 1985. Studies on the life history of an evergreen herb, Pyrola japonica, population on a forest floor in warm temperate region 1. Growth, net production and matter economy. Botanical Magazine, Tokyo 98: 383-392.
27. Kranabetter, J. M., and W. H. MacKenzie. 2010. Contrasts among mycorrhizal plant guilds in foliar nitrogen concentration and d 15 N along productivity gradients of a boreal forest. Ecosystems 13: 108-117.
28. Kron, K. A., W. S. Judd, P. F. Stevens, D. M. Crayn, A. A. Anderberg, P. A. Gadek, C. J. Quinn, and J. L. Luteyn. 2002. Phylogenic classification of Ericaceae: Molecular and morphological evidence. Botanical Review 68: 335-423.
29. Leake, J. R. 2004. Myco-heterotroph/epiparasitic plant interactions with ectomycorrhizal and arbuscular mycorrhizal fungi. Current Opinion in Plant Biology 7: 422-428.
30. Lihnell, D. 1942. Keimungsversuche mit Pyrolasamen. Symbolae Botanicae Upsalienses 6: 1-37.
31. Liu, Z. W., J. Zhou, E.-D. Liu, and H. Peng. 2010. A molecular phylogeny and a new classification of Pyrola (Pyroleae, Ericaceae). Taxon 59: 1690-1700.
32. Martos, F., M. Dulormne, T. Pailler, P. Bonfante, A. Faccio, J. Fournel, M. P. Dubois, and M.-A. Selosse. 2009. Independent recruitment of saprotrophic fungi as mycorrhizal partners by tropical achlorophyllous orchids. New Phytologist 184: 668-681.
33. Massicotte, H. B., L. H. Melville, L. E. Tackaberry, and R. L. Peterson. 2008. A comparative study of mycorrhizas in several genera of Pyroleae (Ericaceae) from western Canada. Botany 86: 610-622.
34. Matsuda, Y., A. Amiya, and S. Ito. 2009. Colonization patterns of mycorrhizal fungi associated with two rare orchids, Cephalanthera falcata and C. erecta. Ecological Research 24: 1023-1031.
35. Matsuda, Y., and N. Hijii. 2004. Ectomycorrhizal fungal communities in an Abies firma forest, with special reference to ectomycorrhizal associations between seedlings and mature trees. Canadian Journal of Botany 82: 822-829.
36. Matsuda, Y., S. Okochi, T. Katayama, A. Yamada, and S. Ito. 2011. Mycorrhizal fungi associated with Monotropastrum humile (Ericaceae) in central Japan. Mycorrhiza 21: 569-576.
37. Motomura, H., M.-A. S elosse, F. M artos, A. K agawa, and T. Y ukawa. 2010. Mycoheterotrophy evolved from mixotrophic ancestors: Evidence in Cymbidium (Orchidaceae). Annals of Botany 106: 573-581.
38. Nei, M., and S. Kumar. 2000. Molecular evolution and phylogenetics. Oxford University Press, New York, New York, USA.
39. Ogura-Tsujita, Y., G. Gebauer, T. Hashimoto, H. Umata, and T. Yukawa. 2009. Evidence for novel and specialized mycorrhizal parasitism: The orchid Gastrodia confusa gains carbon from saprotrophic Mycena. Proceedings of the Royal Society of London, B, Biological Sciences 276: 761-767.
40. Preiss, K., I. K. U. Adam, and G. Gerhard. 2010. Irradiance governs exploitation of fungi: Fine-tuning of carbon gain by two partially mycoheterotrophic orchids. Proceedings of the Royal Society, B, Biological Sciences 277: 1333-1336.
41. Pyykko, M. 1968. Embryological and anatomical studies on Finnish species of Pyrolaceae. Annales Botanici Fennici 5: 153-165.
42. Rasmussen, H. N., and D. F. Whigham. 2002. Phenology of roots and mycorrhiza in five orchid species differing in phototrophic strategy. New Phytologist 154: 797-807.
43. Robertson, D. C., and J. A. Robertson. 1985. Ultrastructual aspects of Pyrola mycorrhizae. Canadian Journal of Botany 63: 1089-1098.
44. Roy, M., S. Whatthana, F. Richard, S. Vessabutr, and M.-A. Selosse. 2009a. Mycoheterotrophic orchids from Thailand tropical dipterocarpacean forests associate with a broad diversity of ectomycorrhizal fungi. BMC Biology 7: 51.
45. Roy, M., T. Yagame, M. Yamato, K. Iwase, C. Heinz, A. Faccio, P. Bonfante, and M.-A. Selosse. 2009b. Ectomycorrhizal Inocybe species associate with the mycoheterotrophic orchid Epipogium aphyllum but not its asexual propagules. Annals of Botany 104: 595-610.
46. Selosse, M.-A., A. Faccio, G. Scappaticci, and P. B onfante. 2004. Chlorophyllous and achlorophyllous specimens of Epipactis microphylla (Neottieae, Orchidaceae) are associated with ectomycorrhizal septomycetes, including truffles. Microbial Ecology 47: 416-426.
47. Selosse, M.-A., and F. Rousset. 2011. The plant-fungal marketplace. Science 333: 828-829.
48. Selosse, M.-A., and M. Roy. 2009. Green plants that feed on fungi: Facts and questions about mixotrophy. Trends in Plant Science 14: 64-70.
49. Smith, S. E., and D. J. Read. 2008. Mycorrhizal symbiosis, 3rd ed. Academic Press, New York, New York, USA.
50. Takahashi, H. 1991. Distribution of Japanese Pyrola and Orthilia, and a distribution pattern with a gap in the central to southern Tohoku district. Acta Phytotaxonomica et Geobotanica 42: 23-43.
51. Tamura, K., J. Dudley, M. Nei, and S. Kumar. 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24: 1596-1599.
52. Taylor, D. L., T. D. Bruns, J. R. Leake, and D. J. Read. 2002. Mycorrhizal specificity and function in myco-heterotrophic plants. In M. G. A. Van der Heijden and I. Sanders [eds.], Mycorrhizal ecology, 375-413. Springer Verlag, Berlin, Germany.
53. Tedersoo, L., and K. Nara. 2010. General latitudinal gradient of biodiversity is reversed in ectomycorrhizal fungi. New Phytologist 185: 351-354.
54. Tedersoo, L., P. Pellet, U. Kõljalg, and M.-A. Selosse. 2007. Parallel evolutionary paths to mycoheterotrophy in understorey Ericaceae and Orchidaceae: Ecological evidence for mixotrophy in Pyroleae. Oecologia 151: 206-217.
55. Toftegaard, T., G. R. Iason, I. J. Alexander, S. Rosendahl, and A. F. S. Taylor. 2010. The threatened plant intermediate wintergreen (Pyrola media Sw.) associates with a wide range of biotrophic fungi in native Scottish pine woods. Biodiversity and Conservation 19: 3963-3971.
56. Trudell, S. A., P. T. R ygiewicz, and R. L. E dmonds. 2003. Nitrogen and carbon stable isotope abundances support the myco-heterotrophic nature and host-specificity of certain achlorophyllous plants. New Phytologist 160: 391-401.
57. Vincenot, L., L. Tedersoo, F. Richard, H. Horcine, U. Kõljalg, and M.-A. Selosse. 2008. Fungal associates of Pyrola rotundifolia, a mixotrophic Ericaceae, from two Estonian boreal forests. Mycorrhiza 19: 15-25.
58. White, T. J., T. Bruns, S. Lee, and J. W. Taylor. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In M. A. Innis, D. H. Gelfand, J. J. Sninsky, and T. J. White [eds.], PCR protocols: A guide to methods and applications, 315-322. Academic Press, San Diego, California, USA.
59. Yagame, T., T. Orihara, M.-A. Selosse, M. Yamato, and K. Iwase. 2012. Mixotrophy of Platanthera minor, an orchid associated with ectomycorrhiza-forming Ceratobasidiaceae fungi. New Phytologist 193: 178-187.
60. Zimmer, K., N. A. Hynson, G. Gebauer, E. B. Allen, M. F. Allen, and D. J. Read. 2007. Wide geographical and ecological distribution of nitrogen and carbon gains from fungi in pyroloids and monotropoids (Ericaceae) and in orchids. New Phytologist 175: 166-175.
61. Zubkov, M. V., and G. A. Tarran. 2008. High bacterivory by the smallest phytoplankton in the North Atlantic Ocean. Nature 455: 224-226.