Stable isotope cellular imaging reveals that both live and degenerating fungal pelotons transfer carbon and nitrogen to orchid protocorms

New Phytologist

Volumn 202, Issue 2, 2014, Pages 594-605

  Kuga, Yukari ^a   Sakamoto, Naoya ^b   Yurimoto, Hisayoshi ^b  

^a HIROSHIMA UNIVERSITY   (Japan)

^b HOKKAIDO UNIVERSITY   (Japan)

Author keywords

Carbon (C) transport; Nitrogen (N) transport; Orchid symbiosis; Secondary ion mass spectrometry (SIMS); Stable isotope imaging

Indexed keywords

CARBON CYCLE; CYTOPLASM; DICOTYLEDON; FUNGUS; MASS SPECTROMETRY; NITROGEN CYCLE; SENESCENCE; SPATIAL RESOLUTION; STABLE ISOTOPE; SYMBIONT; SYMBIOSIS;

CERATOBASIDIUM; FUNGI; ORCHIDACEAE; SPIRANTHES SINENSIS;

CARBON; NITROGEN;

ARTICLE; BASIDIOMYCETES; CARBON (C) TRANSPORT; FUNGUS HYPHAE; METABOLISM; MYCORRHIZA; NITROGEN (N) TRANSPORT; ORCHID SYMBIOSIS; ORCHIDACEAE; PLANT STRUCTURES; SECONDARY ION MASS SPECTROMETRY (SIMS); STABLE ISOTOPE IMAGING; SYMBIOSIS;

CARBON (C) TRANSPORT; NITROGEN (N) TRANSPORT; ORCHID SYMBIOSIS; SECONDARY ION MASS SPECTROMETRY (SIMS); STABLE ISOTOPE IMAGING;

BASIDIOMYCOTA; CARBON; CARBON ISOTOPES; HYPHAE; MYCORRHIZAE; NITROGEN; NITROGEN ISOTOPES; ORCHIDACEAE; PLANT STRUCTURES; SYMBIOSIS;

EID: 84896546298     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12700     Document Type: Article

References (41)

1. Bougoure JJ, Brundrett MC, Grierson PF. 2010. Carbon and nitrogen supply to the underground orchid, Rhizanthella gardneri. New Phytologist 186: 947-956.
2. Burgeff H. 1959. Mycorrhiza of orchid. In: Withner CL, ed. The orchids: a scientific survey. New York, NY, USA: Ronald Press, 361-395.
3. Burges A. 1939. The defensive mechanism in orchid mycorrhiza. New Phytologist 38: 273-283.
4. Cameron DD, Johnson I, Leake JR, Read DJ. 2007. Mycorrhizal acquisition of inorganic phosphorus by the green-leaved terrestrial orchid Goodyera repens. Annals of Botany 99: 831-834.
5. Cameron DD, Johnson I, Read DJ, Leake JR. 2008. Giving and receiving: measuring the carbon cost of mycorrhizas in the green orchid, Goodyera repens. New Phytologist 180: 176-184.
6. Cameron DD, Leake JR, Read DJ. 2006. Mutualistic mycorrhiza in orchids: evidence from plant-fungus carbon and nitrogen transfers in the green-leaved terrestrial orchid Goodyera repens. New Phytologist 171: 405-416.
7. Clements MA. 1988. Orchid mycorrhizal associations. Lindleyana 3: 73-86.
8. Clode PL, Kilburn MR, Jones DL, Stockdale EA, Cliff JBIII, Herrmann AM, Murphy DV. 2009. In situ mapping of nutrient uptake in the rhizosphere using nanoscale secondary ion mass spectrometry. Plant Physiology 151: 1751-1757.
9. Clode PL, Stern RA, Marchall AT. 2007. Subcellular imaging of isotopically labeled carbon compounds in a biological sample by ion microprobe (NanoSIMS). Microscopy Research and Technique 70: 220-229.
10. Hadley G. 1982. Orchid mycorrhiza. In: Arditti J, ed. Orchid biology - reviews and perspectives, II. Ithaca, NY, USA: Cornell University Press, 84-118.
11. Hadley G, Johnson RPC, John DA. 1971. Fine structure of the host-fungus interface in orchid mycorrhiza. Planta 100: 191-199.
12. Hadley G, Williamson B. 1971. Analysis of the post-infection growth stimulus in orchid mycorrhiza. New Phytologist 70: 445-455.
13. Harvais G, Hadley G. 1967. The relation between host and endophyte in orchid mycorrhiza. New Phytologist 66: 205-215.
14. Hynson NA, Madsen TP, Selosse M-A, Adam IKU, Ogura-Tsujita Y, Roy M, Gebauer G. 2013. The physiological ecology of mycoheterotrophy. In: Merckx VSFT, ed. Mycoheterotrophy: the biology of plants living on fungi. New York, NY, USA: Springer, 297-344.
15. Kunihiro T, Nagashima K, Yurimoto H. 2005. Microscopic oxygen isotopic homogeneity/heterogeneity in the matrix of the Vigarano CV3 chondrite. Geochimica et Cosmochimica Acta 69: 763-773.
16. Lechene C, Hillion F, McMahon G, Benson D, Kleinfeld AM, Kampf JP, Distel D, Luyten Y, Bonventre J, Hentschel D et al. 2006. High-resolution quantitative imaging of mammalian and bacterial cells using stable isotope mass spectrometry. Journal of Biology 5: 20.
17. Lechene CP, Luyten Y, McMahon G, Distel DL. 2007. Quantitative imaging of nitrogen fixation by individual bacteria within animal cells. Science 317: 1563-1566.
18. Li T, Wu T-D, Mazéas L, Toffin L, Guerquin-Kern J-L, Leblon G, Bouchez T. 2008. Simultaneous analysis of microbial identity and function using NanoSIMS. Environmental Microbiology 10: 580-588.
19. Merckx VSFT. 2013. Mycoheterotrophy: an introduction. In: Merckx VSFT, ed. Mycoheterotrophy: the biology of plants living on fungi. New York, NY, USA: Springer, 1-17.
20. Mollison JE. 1943. Goodyera repens and its endophyte. Transactions of the Botanical Society of Edinburgh 33: 391-403.
21. Moore KL, Chen Y, Meene AMLvd, Hughes L, Liu W, Geraki T, Mosselmans F, McGrath SP, Grovenor C, Zhao F-J. 2013. Combined NanoSIMS and synchrotron X-ray fluorescence reveal distinct cellular and subcellular distribution patterns of trace elements in rice tissues. New Phytologist 201: 104-105.
22. Nagashima K, Krot AN, Yurimoto H. 2004. Stardust silicates from primitive meteorites. Nature 428: 921-924.
23. Peterson RL, Bonfante P, Faccio A, Uetake Y. 1996. The interface between fungal hyphae and orchid protocorm cells. Canadian Journal of Botany 74: 1861-1870.
24. Peterson RL, Currah RS. 1990. Synthesis of mycorrhizae between protocorms of Goodyera repens (Orchidaceae) and Ceratobasidium cereale. Canadian Journal of Botany 68: 1117-1125.
25. Peterson RL, Massicotte HB, Melville LH. 2004. Mycorrhizas: anatomy and cell biology. Wallingford, UK: CABI Publishing.
26. Peterson RL, Uetake Y, Zelmer C. 1998. Fungal symbioses with orchid protocorms. Symbiosis 25: 29-55.
27. Rasmussen HN. 1990. Cell differentiation and mycorrhizal infection in Dactylorhiza majalis (Rchb. f.) Hunt & Summerh. (Orchidaceae) during germination in vitro. New Phytologist 116: 137-147.
28. Rasmussen HN. 1995. Terrestrial orchids from seed to mycotorophic plant. Cambridge, UK: Cambridge University Press.
29. Sakamoto N, Seto Y, Itoh S, Kuramoto K, Fujino K, Nagashima K, Krot AN, Yurimoto H. 2007. Remnants of the early solar system water enriched in heavy oxygen isotopes. Science 317: 231-233.
30. Selosse M-A, Boullard B, Richardson D. 2011. Noël Bernard (1874-1911): orchids to symbiosis in a dozen years, one century ago. Symbiosis 54: 61-68.
31. Senyo SE, Steinhauser ML, Pizzimenti CL, Yang VK, Cai L, MeiWang WuT-D, Guerquin-Kern J-L, Lechene CP, Lee RT. 2013. Mammalian heart renewal by pre-existing cardiomyocytes. Nature 493: 433-436.
32. Shaw P, Brown J. 2012. Nucleoli: composition, function, and dynamics. Plant Physiology 158: 44-51.
33. Smith SE. 1967. Carbohydrate translocation in orchid mycorrhizal fungi. New Phytologist 66: 371-378.
34. Smith SE, Read DJ. 2008. Mycorrhizal symbiosis, 3rd edn. Cambridge, UK: Academic Press.
35. Steinhauser ML, Bailey AP, Senyo SE, Guillermier C, Perlstein TS, Gould AP, Lee RT, Lechene CP. 2012. Multi-isotope imaging mass spectrometry quantifies stem cell division and metabolism. Nature 481: 516-519.
36. Uetake Y, Farquhar ML, Peterson RL. 1997. Changes in microtubule arrays in symbiotic orchid protocorms during fungal colonization and senescence. New Phytologist 135: 701-709.
37. Uetake Y, Ishizaka N. 1996. Cytochemical localization of adenylate cyclase activity in the symbiotic protocorms of Spiranthes sinensis. Mycological Research 100: 105-112.
38. Uetake Y, Kobayashi K, Ogoshi A. 1992. Ultrastructural changes during the symbiotic development of Spiranthes sinensis (Orchidaceae) protocorms associated with binucleate Rhizoctonia anastomosis group C. Mycological Research 96: 199-209.
39. Uetake Y, Peterson RL. 1998. Association between microtubules and symbiotic fungal hyphae in protocorm cells of orchid species, Spiranthes sinensis. New Phytologist 140: 715-722.
40. Williamson B, Hadley G. 1969. DNA content of nuclei in orchid protocorms symbiotically infected with Rhizoctonia. Nature 222: 582-583.
41. Yurimoto H, Nagashima K, Kunihiro T. 2003. High precision isotope micro-imaging of materials. Applied Surface Science 203-204: 793-797.