Carbon Transfer from the Host to Tuber melanosporum Mycorrhizas and Ascocarps Followed Using a 13C Pulse-Labeling Technique

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Le Tacon, François ^a,b   Zeller, Bernd ^c   Plain, Caroline ^b,d   Hossann, Christian ^b,d   Bréchet, Claude ^b,d   Robin, Christophe ^b,e  

^a UNIVERSITÉ DE LORRAINE   (France)

^b UNIVERSITÉ DE LORRAINE   (France)

^c Centre INRA de Nancy   (France)

^d LERFoB   (France)

^e UNIVERSITÉ DE LORRAINE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON 13;

ARTICLE; ASCOCARP; CARBON FIXATION; CARBON METABOLISM; CARBON TRANSFER; CHEMICAL LABELING; CONTROLLED STUDY; FRANCE; LOW TEMPERATURE; MYCORRHIZA; NONHUMAN; PLANT LEAF; PLANT ROOT; SOIL; TUBER (GENUS); TUBER MELANOSPORUM;

ASCOMYCOTA; BIOLOGICAL TRANSPORT; CARBON; CARBON ISOTOPES; CORYLUS; FRANCE; MYCORRHIZAE; PLANT LEAVES; SOIL; SYMBIOSIS; TEMPERATURE;

CORYLUS AMERICANA; TUBER (TRUFFLE); TUBER MELANOSPORUM;

EID: 84878619729     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0064626     Document Type: Article

References (50)

1. Paolocci F, Rubini A, Riccioni C, Arcioni S, (2006) Re-evaluation of the life cycle of Tuber magnatum. Appl Environ Microbiol 72: 2390-2393.
2. Riccioni C, Belfiori B, Rubini A, Passeri V, Arcioni S, et al. (2008) Tuber melanosporum outcrosses: analysis of the genetic diversity within and among its natural populations under this new scenario. New Phytol 180: 466-478.
3. Teramoto M, Wu B, Hogetsu T, (2012) Transfer of 14C-photosynthate to the sporocarp of an ectomycorrhizal fungus Laccaria amethystina. Mycorrhiza 22: 219-225.
4. Olivier J-M, Savignac J-C, Sourzat P (2012) Truffe et trufficulture, Fanlac editor, Périgueux, France.
5. Barry D, Staunton S, Callot G, (1994) Mode of the absorption of water and nutrients by ascocarps of Tuber melanosporum and Tuber aestivum. A radioactive tracer technique. Can J Bot 72: 317-322.
6. Callot G, Byé P, Raymond M, Fernandez D, Pargney JC, et al. (1999) La truffe, la terre, la vie: Quae, INRA. 210 p.
7. Mamoun M, Olivier JM, (1991) Influence du substrat carboné et de la forme d'azote minéral sur la croissance de T. melanosporum Vittad. en culture pure. Application à la production de biomasse mycélienne. Agronomie 11: 521-527.
8. Martin F, Kohler A, Murat C, Balestrini R, Coutinho PM, et al. (2010) Perigord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis. Nature 464: 1033-1038.
9. Zeller B, Bréchet C, Maurice JP, Le Tacon F, (2008) Saprotrophic versus symbiotic strategy during truffle ascocarp development under holm oak. A response based on 13C and 15N natural abundance. Ann For Sci 65: 607-614.
10. Rouquerolle T, Payre H, (1975) Conséquences de quelques particularités biologiques des Tuber sur les caractères des cultures de mycélium et sur la formation des truffes. Rev Mycol 29: 213-224.
11. Robin C, Vaillant V, Vansuyt G, Zinsou C, (1990) Assimilate partitioning in Pachyrhizus erosus L. during long-day vegetative development. Plant Physiol Biochem 28: 343-349.
12. Leake JR, Ostle NJ, Rangel-Castro IJ, Johnson D, (2006) Carbon fluxes from plants through soil organisms determined by field 13CO2 pulse-labelling in an upland grassland. Applied Soil Ecology 33: 152-175.
13. NGuyen C, Todorovic C, Robin C, Christophe A, Guckert A, (1999) Continuous monitoring of rhizosphere respiration after labelling of plant shoots with 14CO2. Plant Soil 212: 189-199.
14. Johnson D, Leake JR, Ostle N, Ineson P, Read DJ, (2002) In situ 13CO2 pulse-labelling of upland grassland demonstrates a rapid pathway of carbon flux from arbuscular mycorrhizal mycelia to the soil. New Phythol 153: 327-334.
15. Ek H, (1997) The influence of nitrogen fertilization on the carbon economy of Paxillus involutus in ectomycorrhizal association with Betula pendula. New Phytol 135: 133-142.
16. Finlay RD, Read DJ, (1986) The structure and function of the vegetative mycelium of ectomycorrhizal plants. 1. The translocation of 14C-labelled carbon between plants interconnected by a common mycelium. New Phytol 103: 143-156.
17. Horwath WR, Pregitzer KS, Paul EA, (1994) 14C Allocation in tree-soil systems. Tree Physiol 14: 1163-1176.
18. Leake JR, Donnelly DP, Saunders EM, Boddy L, Read DJ, (2001) Rates and quantities of carbon flux to ectomycorrhizal mycelium following 14C pulse labeling of Pinus sylvestris seedlings: effects of litter patches and interaction with a wood-decomposer fungus. Tree Physiol 21: 71-82.
19. Leanne JP, Simard SW, (2008) Minimum pulses of stable and radioactive carbon isotopes to detect belowground carbon transfer between plants. Plant Soil 308: 23-35.
20. Miller SL, Durall DM, Rygiewicz PT, (1989) Temporal allocation of 14C to extramatrical hyphae of ectomycorrhizal ponderosa pine seedlings. Tree Physiol 5: 239-249.
21. Norton JM, Smith JL, Firestone MK, (1990) Carbon flow in the rhizosphere of Ponderosa pine seedlings. Soil Biol Biochem 22: 449-455.
22. Ostle N, Whiteley AS, Bailey MJ, Sleep D, Ineson P, et al. (2003) Active microbial RNA turnover in a grassland soil estimated using a 13CO2 spike. Soil Biol Biochem 35: 877-885.
23. Rygiewicz PT, Andersen CP, (1994) Mycorrhizae alter quality and quantity of carbon allocated below ground. Nature 369: 58-60.
24. Simard SW, Durall DM, Jones MD, (1997) Carbon allocation and carbon transfer between Betula papyrifera and Pseudotsuga menziesii seedlings using a 13C pulse-labeling method. Plant Soil 191: 41-55.
25. Högberg P, Högberg MN, Gottlicher SG, Betson NR, Keel SG, et al. (2008) High temporal resolution tracing of photosynthate carbon from the tree canopy to forest soil microorganisms. New Phytol 177: 220-228.
26. Epron D, Ngao J, Dannoura M, Bakker MR, Zeller B, et al. (2011) Seasonal variations of belowground carbon transfer assessed by in situ 13CO2 pulse labelling of trees. Biogeosciences 8: 1153-1168.
27. Plain C, Gerant D, Maillard P, Dannoura M, Dong Y, et al. (2009) Tracing of recently assimilated carbon in respiration at high temporal resolution in the field with a tuneable diode laser absorption spectrometer after in situ 13CO2 pulse labelling of 20-year-old beech trees. Tree Physiol 29: 1433-1445.
28. Subke JA, Vallack HW, Magnusson T, Keel SG, Metcalfe DB, et al. (2009) Short-term dynamics of abiotic and biotic soil 13CO2 effluxes after in situ 13CO2 pulse labelling of a boreal pine forest. New Phytol 183: 349-357.
29. Chevalier G, Poitou N, (1990) Study of important factors affecting the mycorrhizal development of the truffle fungus in the field using plants inoculated in nurseries. Agric Ecosyst Environ 28: 75-77.
30. Paolocci F, Rubini A, Granetti B, Arcioni S, (1999) Rapid molecular approach for a reliable identification of Tuber spp. ectomycorrhizae. FEMS Microbiol Ecol 28: 23-30.
31. Rubini A, Paolocci F, Granetti B, Arcioni S, (1998) Single step molecular characterization of morphologically similar black truffle species. FEMS Microbiol Lett 164: 7-12.
32. Murat C, Rubini A, Riccioni C, De la Varga H, Akroume E, et al. (2013) Fine scale spatial genetic structure of the black truffle (Tuber melanosporum) investigated with neutral microsatellites and functional mating type genes. New Phytol doi: 10.1111/nph.12264.
33. Box GEP, Cox DR, (1964) An analysis of transformation, Journal of the Royal Statistical Society. Series B (Methodological)26-2: 211-252.
34. Treseder KK, Torn MS, Masiello CA, (2006) An ecosystem-scale radiocarbon tracer to test use of litter carbon by ectomycorrhizal fungi. Soil Biol Biochem 38: 1077-1082.
35. Godbout C, Fortin JA, (1992) Effects of nitrogen fertilization and photoperiod on basidiome formation of Laccaria bicolor associated with container-grown jack pine seedlings. Can J Bot 70: 181-185.
36. Högberg P, Nordgren A, Buchmann N, Taylor AFS, Ekblad A, et al. (2001) Large-scale forest girdling shows that current photosynthesis drives soil respiration. Nature 41: 789-792.
37. Kuikka K, Härmä E, Markkola A, Rautio P, Roitto M, et al. (2003) Severe defoliation of Scots pine reduces reproductive investment by ectomycorrhizal symbionts. Ecology 84: 2051-2061.
38. Lamhamedi MS, Godbout C, Fortin JA, (1994) Dependence of Laccaria bicolor basidiome development on current photosyn- thesis of Pinus strobus seedlings. Can J For Res 24: 1797-1804.
39. Last FT, Pelham J, Mason PA, Ingleby K, (1979) Influence of leaves on sporophore production by fungi forming sheathing mycorrhizas with Betula spp. Nature 280: 168-169.
40. Pestaña M, Santolamazza-Carbone S, (2011) Defoliation negatively affects plant growth and the ectomycorrhizal community of Pinus pinaster in Spain. Oecologia 165: 723-733.
41. Hobbie EA, Quimette AP, Schuur EAG, Kierstead D, Trappe JM, et al. (2012) Radiocarbon evidence for the mining of organic nitrogen from soil by mycorrhizal fungi. Biogeochemistry doi: 10.1007/s10533-012-9779-z.
42. Essiamah S, Eschrich W, (1985) Changes of starch content in the storage tissues of deciduous trees during winter and spring. IAWA Bulletin 6: 97-106.
43. Sauter JJ, van Cleve B, (1994) Storage, mobilization and interrelations of starch, sugars, protein and fat in the ray storage tissue of poplar trees. Trees 8: 297-304.
44. Palonen P, Buszard D, Donnelly D, (2000) Changes in carbohydrates and freezing tolerance during cold acclimation of red raspberry cultivars grown in vitro and in vivo. Physiol Plant 110: 393-401.
45. Bollmark L, Sennerby-Forsse L, Ericsson T, (1999) Seasonal dynamics and effects of nitrogen supply rate on nitrogen and carbohydrate reserves in cutting-derived Salix viminalis plants. Can J For Res 29: 85-94.
46. Johansson T, (1993) Seasonal changes in contents of root starch and soluble carbohydrates in 4-6 year old Betula pubescens and Populus tremula. Scand J For Res 8: 94-106.
47. Landhäusser SM, Lieffers VJ, (2003) Seasonal changes in carbohydrate reserves in mature northern Populus tremuloides clones. Trees- Structure and Function 17: 471-476.
48. Kagawa A, Sugimoto A, Maximov TC, (2006a) 13CO2 pulse-labelling of photoassimilates reveals carbon allocation within and between tree rings. Plant Cell Environ 29: 1571-1584.
49. Kagawa A, Sugimoto A, Maximov TC, (2006b) Seasonal course of translocation, storage and remobilization of 13C pulse-labeled photoassimilate in naturally growing Larix gmelinii saplings. New Phytol 171: 793-803.
50. Maurel K, Leite GB, Bonhomme M, Guilliot A, Rageau R, et al. (2004) Trophic control of bud break in peach (Prunus persica) trees: a possible role of hexoses. Tree Physiol 24: 579-588.