High-resolution secondary ion mass spectrometry analysis of carbon dynamics in mycorrhizas formed by an obligately myco-heterotrophic orchid

Plant, Cell and Environment

Volumn 37, Issue 5, 2014, Pages 1223-1230

  Bougoure, Jeremy ^a   Ludwig, Martha ^a   Brundrett, Mark ^b   Cliff, John ^a   Clode, Peta ^a   Kilburn, Matt ^a   Grierson, Pauline ^a  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^b Crop Variety Testing Group   (Australia)

Author keywords

Achlorophyllous orchid; Mycorrhiza; nanoSIMS; nanoSIP; Rhizanthella gardneri

Indexed keywords

HETEROTROPHY; MASS SPECTROMETRY; MONOCOTYLEDON; MYCORRHIZA; NUTRIENT DYNAMICS;

FUNGI; ORCHIDACEAE; RHIZANTHELLA GARDNERI;

CARBON;

CYTOLOGY; FLOWER; HETEROTROPHY; MASS SPECTROMETRY; METABOLISM; MICROBIOLOGY; MYCORRHIZA; NANOTECHNOLOGY; ORCHIDACEAE; PHYSIOLOGY; PROCEDURES; ULTRASTRUCTURE;

CARBON; CARBON ISOTOPES; FLOWERS; HETEROTROPHIC PROCESSES; MYCORRHIZAE; NANOTECHNOLOGY; ORCHIDACEAE; SPECTROMETRY, MASS, SECONDARY ION;

EID: 84898059069     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/pce.12230     Document Type: Article

References (39)

1. Alexander C. & Hadley G. (1985) Carbon movement between host and mycorrhizal endophyte during the development of the orchid Goodyera repens Br. New Phytologist 101, 657-665.
2. Bevington P.R. & Robinson D.K. (2002) Data Reduction and Error Analysis for the Physical Sciences 3rd edn, McGraw-Hill, New York.
3. Bonnardeaux Y., Brundrett M., Batty A., Dixon K., Koch J. & Sivasithamparam K. (2007) Diversity of mycorrhizal fungi of terrestrial orchids: compatibility webs, brief encounters, lasting relationships and alien invasions. Mycological Research 182, 2069-2085.
4. Bougoure J.J., Brundrett M., Brown A. & Grierson P.F. (2008) Habitat characteristics of the rare underground orchid. Australian Journal of Botany 56, 501-511.
5. Bougoure J.J., Ludwig M., Brundrett M. & Grierson P.F. (2009) Identity and specificity of the fungi forming mycorrhizas with rare, mycoheterotrophic Rhizanthella gardneri (Orchidaceae). Mycological Research 113, 1097-1106.
6. Bougoure J.J., Brundrett M. & Grierson P.F. (2010) Carbon and nitrogen supply to the underground orchid. New Phytologist 186, 947-956.
7. Cameron D.D., Leake J.R. & Read D.J. (2006) Mutualistic mycorrhizas in orchids: evidence from plant-fungus carbon and nitrogen transfers in the green-leaved terrestrial orchid Goodyera repens. New Phytologist 171, 405-416.
8. Cameron D.D., Johnson I., Leake J.R. & Read D.J. (2007) Mycorrhizal acquisition of inorganic phosphorus by the green-leaved terrestrial orchid Goodyera repens. Annals of Botany 99, 831-834.
9. Cameron D.D., Johnson I., Read D.J. & Leake J.R. (2008) Giving and receiving: measuring the carbon cost of mycorrhizas in the green orchid, Goodyera repens. New Phytologist 180, 176-184.
10. Dearnaley J.D.W., Martos F. & Selosse M.A. (2012) Orchid mycorrhizas: molecular ecology, physiology, evolution and conservation aspects. In The Mycota Volume IX - Fungal Associations (ed. K. Esser ) Second edn, pp. 207-230. Springer-Verlag, Berlin.
11. Delannoy E., Fuji S., des Francs C.C., Brundrett M. & Small I. (2011) Rampant gene loss in the underground orchid Rhizanthella gardneri highlights evolutionary constraints on plastid genomes. Molecular Biology and Evolution 28, 2077-2086.
12. Dixon K.W., Pate J.S. & Kuo J. (1990) The Western Australian subterranean orchid Rhizanthella gardneri Rogers, the underground orchid of Western Australia. In Orchid Biology, Reviews and Perspectives (ed. J. Arditti ), pp. 37-62. Timber Press, Oregon.
13. Dressler R.L. (1993) Phylogeny and Classification of the Orchid Family. Dioscorides Press, Portland, OR.
14. Ellers J., Kiers E.T., Currie C.R., McDonald B.R. & Visser B. (2012) Ecological interactions drive evolutionary loss of traits. Ecology Letters 15, 1071-1082.
15. 13C natural abundance of autotrophic and mycoheterotrophic orchids provides insight into nitrogen and carbon gain from fungal associations. New Phytologist 160, 209-223.
16. Hadley G. & Williamson B. (1971) Analysis of post infection growth stimulus in orchid mycorrhizas. New Phytologist 70, 445-455.
17. Hynson N.A., Madsen T.P., Selosse M.-A., Adam I.K.U., Ogura-Tsujita Y., Roy M. & Gebauer G. (2013) The physiological ecology of mycoheterotrophy. In Mycoheterotrophy - the Biology of Plants Living on Fungi (ed. V.S.F.T. Merckx ), pp. 297-342. Springer, New York.
18. Johnson L. & Nylund J.E. (1979) Favolaschia dybowskyana (Singer) Singer (Aphyllophorales), a new orchid mycorrhizal fungus from tropical Africa. New Phytologist 83, 121-128.
19. Leake J.R. (1994) The biology of myco-heterotrophic ('saprotrophic') plants. New Phytologist 127, 171-216.
20. McDonald K.L., Morphe M., Verkade P. & Müller-Reichert T. (2007) Recent advances in high pressure freezing: equipment and specimen loading methods. In Methods in Molecular Biology, vol. 369, Electron Microscopy: Methods and Protocols (ed. J. Kuo ) 2nd edn, pp. 143-173. Humana Press Inc., Totowa.
21. McDonnell L.A. & Heeran R.M.A. (2007) Imaging mass spectrometry. Mass Spectrometry Reviews 26, 606-643.
22. Marshall A.T. (1980) Freeze-substitution as a preparation technique for biological x-ray microanalysis. Scanning and Electron Microscopy 2, 395-408.
23. Molvray M., Kores P.J. & Chase M.W. (2000) Polyphyly of mycoheterotrophic orchids and functional influences on floral and molecular characters. In Monocots: Systematics and Evolution (eds K.L. Wilson & D.A. Morrison ), pp. 441-448. CSIRO Publishing, Canberra.
24. Moore K.L., Lombi E., Zhao F.J. & Grovenor C.R.M. (2012) Elemental imaging at the nanoscale: NanoSIMS and complimentary techniques for element loacalisation in plants. Analytical and Bioanalytical Chemistry 402, 3263-3273.
25. Peterson R.L. & Currah R.S. (1990) Synthesis of mycorrhizae between protocorms of Goodyera repens (Orchidaceae) and Ceratobasidium cereale. Canadian Journal of Botany 68, 1117-1125.
26. Peterson R.L., Uetake Y. & Zelmer C. (1998) Fungal symbiosis with orchid protocorms. Symbiosis 25, 29-55.
27. Purves S. & Hadley G. (1975) Movement of carbon compounds between the partners in orchid mycorrhizas. In Endomycorrhizas (eds F.E. Sanders, B. Mosse & P.B. Tinker ), pp. 175-194. Academic Press, London.
28. Rasmussen H.N. (2004) Recent developments in the study of orchid mycorrhiza. Plant and Soil 244, 149-163.
29. Rasmussen H.N. & Rasmussen F.N. (2009) Orchid mycorrhizas: implications of a mycophagous life style. Oikos 118, 334-345.
30. Roy M., Watthana S., Stier A., Richard F., Vessabutr S. & Selosse M.-A. (2009) Two mycoheterotrophic orchids from Thailand tropical dipterocarpacean forests associate with broad diversity of ectomycorrhizal fungi. BMC Biology 7, 1-17.
31. Roy M., Gonneau C., Rocheteau A., Berveiller D., Thomas J.-C., Damesin C. & Selosse M.-A. (2013) Why do mixotrophic plants stay green? A comparison between green and achlorophyllous orchid individuals in situ. Ecological Monographs 83, 95-117.
32. Simard S.W., Perry D.A., Jones M.D., Myrold D.D., Durall D.M. & Molina R. (1997) Net transfer of carbon between ectomycorrhizal tree species in the field. Nature 388, 579-582.
33. Slodzian G., Chaintreau M., Dennebuoy R. & Rousse G. (2001) Precise in situ measurements of isotopic abundances with pulse counting of sputtered ions. European Physical Journal Applied Physics 14, 199-231.
34. Slodzian G., Hillion F., Stadermann F.J. & Zinner E. (2004) QSA influences on isotopic ratio measurements. Applied Surface Science 231, 874-877.
35. Smith S.E. (1967) Carbohydrate translocation in orchid mycorrhizas. New Phytologist 66, 371-378.
36. Smith S.E. & Read D.J. (2008) Mycorrhizal Symbiosis. Academic Press, Cambridge, UK.
37. Spurr A.R. (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. Journal of Ultrastructural Research 26, 31-43.
38. Tedersoo L., Pellet P., Koljalg U. & Selosse M.-A. (2007) Parallel evolutionary paths to mycoheterotrophy in understorey Ericaceae and Orchidaceae: ecological evidence for mixotrophy in Pyrolaceae. Oecologia 151, 206-217.
39. Zhang D.S., Piazza V., Perrin J.P., Rzadzinska A.K., Poczatek J.C., Wang M., .. Lechene C.P. (2012) Multi-isotope imaging mass spectrometry reveals slow protein turnover in hair-cell sterocilia. Nature 481, 520-524.