Abstract
In the last few years the application of modern techniques to the study of arbuscular mycorrhizas has greatly increased our understanding of the mechanisms underlying carbon metabolism in these mutualistic symbioses. Arbuscular mycorrhizal (AM) monoxenic cultures, nuclear magnetic resonance spectroscopy together with isotopic labeling, and analyses of expressed sequence tags (ESTs) have shed light on the metabolic processes taking place in these interactions, particularly in the case of the mycobiont. More recently, in vivo multiphoton microscopy has provided us with some new insights in the allocation and translocation processes which play crucial roles in the distribution of host plant-derived C throughout the fungal colony. In this mini-review we highlight recent advances in these fields, with special attention to the visualization of oleosomes (i.e., lipid bodies) as they move along the long, coenocytic AM fungal hyphae. Volumetric measurements of such oleosomes have allowed us to estimate the flux of triacylglycerides from the intraradical to the extraradical phase of the AM fungal colony. We raise questions and postulate regulatory mechanisms for C metabolism and translocation within the arbuscular mycorrhizal fungal colony.
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References
Aström H, Giovannetti M and Raudaskoski M 1994 Cytoskeletal components in the arbuscular mycorrhizal fungus Glomus mosseae. MPMI 7, 309-312.
Bago, B 2000 Putative sites for nutrient uptake in arbuscular mycorrhizal fungi. Plant Soil 226, 263-274.
Bago B, Azcón-Aguilar C and Piché Y 1998a Architecture and developmental dynamics of the external mycelium of the arbuscular mycorrhizal fungus Glomus intraradices grown under monoxenic conditions. Mycologia 90, 52-62.
Bago B, Azcón-Aguilar C, Goulet A and Piché Y 1998b Branched absorbing structures (BAS): a feature of the extraradical mycelium of symbiotic arbuscular mycorrhizal fungi. New Phytol. 139, 375-388.
Bago B, Zipfel W, Williams RC and Piché Y 1999a Nuclei of symbiotic arbuscular mycorrhizal fungi as revealed by in vivo two-photon microscopy. Protoplasma 209, 77-89.
Bago B, Pfeffer PE, Douds DD Jr, Brouillette J, Bécard G and Shachar-Hill Y 1999b Carbon metabolism in arbuscular mycorrhizal spores as revealed by NMR spectroscopy. Plant Physiol. 121, 263-271.
Bago B, Zipfel W, Williams RC, Chamberland H, Lafontaine J-G, Webb WW and Piché Y 1998c In vivo studies on the nuclear behavior of the arbuscular mycorrhizal fungus Gigaspora rosea grown under axenic conditions. Protoplasma 203, 1-15.
Bago B, Pfeffer PE and Shachar-Hill Y 2000 Carbon metabolism and transport in arbuscular mycorrhizas. Plant Physiol. 124, 949-957.
Bago B, Pfeffer PE and Shachar-Hill Y 2001 Could the urea cycle be translocating nitrogen in arbuscular mycorrhizal fungi? New Phytol. 149, 4-8.
Bago B, Zipfel W, Williams RC, Jun J, Arreola R, Pfeffer PE, Lammers PJ and Shachar-Hill Y 2002 Translocation and utilization of fungal lipid in the arbuscular mycorrhizal symbiosis. Plant Physiol 128, 108-124.
Balestrini R, Bianciotto V and Bonfante-Fasolo P 1992 Nuclear architecture and DNA location in two VAM fungi. Mycorrhiza 1, 105-112.
Bécard G and Fortin A 1988 Early events of vesicular-arbuscular mycorrhiza formation on Ri T-DNA transformed roots. New Phytol. 108, 211-218.
Beilby JP 1983 Effects of inhibitors on early protein, RNA, and lipid synthesis in germinating vesicular-arbuscular mycorrhizal fungal spores of Glomus caledonium. Can. J. Bot. 29, 596-601.
Beilby JP and Kidby DK 1980 Biochemistry of ungerminated and germinated spores of the vesicular-arbuscular mycorrhizal fungus Glomus caledonium: changes in neutral and polar lipids. J. Lipid Res. 21, 739-750.
Burleigh S H and Ellegaard Bechman I 2002 Plant nutrient transporter regulation in arbuscular mycorrhiza. Plant Soil 244, 247-251.
Bütehorn B, Gianinazzi-Pearson V and Franken P 1999 Quanti-fication of beta-tubulin RNA expression during asymbiotic and symbiotic development of the arbuscular mycorrhizal fungus Glomus mosseae. Mycol. Res. 103, 360-364.
Cooper KM and Lösel DM 1978 Lipid physiology of vesicular arbuscular mycorrhiza. New Phytol. 80, 143-151.
Denk W, Strickler JH and Webb WW 1990 Two-photon laser scanning fluorescence microscopy. Science 248, 73-76.
Denk W, Piston DN and Webb WW 1995 Two-photon molecular excitation in laser scanning fluorescence microscopy. In Handbook of Biological Confocal Microscopy. Ed. JB Pawley. pp 445-458. Plenum Pres, New York.
Ferrol N, Barea J M and Azcón-Aguilar 2002 Mechanisms of nutrient transport across interfaces in arbuscular mycorrhizas. Plant Soil 244, 231-237.
Friese CF and MF Allen 1991 The spread of VA mycorrhizal fungal hyphae in the soil: inoculum types and external hyphal architecture. Mycologia 83, 409-418.
Gaspar ML, Pollero RJ and Cabello MN 1994 Triacylglycerol consumption during spore germination of vesicular-arbuscular mycorrhizal fungi. JAOCS 71, 449-452.
Gaspar L, Pollero R and Cabello M 1997 Partial purification and characterization of a lipolytic enzyme from spores of the arbuscular mycorrhizal fungus Glomus versiforme. Mycologia 89, 610-614.
George E, Marschner H and Jakobsen I 1995 Role of arbuscularmycorrhizal fungi in uptake of phosphorus and nitrogen from soil. Crit. Rev. Biotechnol. 15, 257-270.
Gianinazzi-Pearson V, Smith SE, Gianinazzi S and Smith FA 1991 Enzymatic studies on the metabolism of vesicular-arbuscular mycorrhizas. V. Is H+-ATPase a component of ATP-hydrolysing enzyme activities in plant-fungus interfaces? New Phytol. 117, 61-74.
Gow NAR and Gadd GM 1984 The Growing Fungus. Chapman &; Hall, London, UK. 472 pp.
Greenspan P, Mayer EP and Fowler SD 1985 Nile Red: a selective fluorescent stain for intracellular lipid droplets. J Cell Biol 100, 965-973.
Harrier LA, Wright F and Hooker JE 1998 Isolation of the 3-phosphoglycerate kinase gene of the arbuscular mycorrhizal fungus Glomus mosseae (Nicol. &; Gerd.) Gerdemann &; Trappe. Curr. Genet. 34, 386-392.
Ho I, Trappe JM 1973 Translocation of 14C from Festuca plants to their endomycorrhizal fungi. Nature 244, 30-31.
Jabaji-Hare S 1988 Lipid and fatty acid profiles of some vesiculararbuscular mycorrhizal fungi: contribution to taxonomy. Mycologia 80, 622-629.
Jakobsen I 1999 Transport of phosphorus and carbon in VA mycorrhizas. In Mycorrhiza: Structure, Function, Molecular Biology and Biotechnology, 2nd Edition. Eds. A Varma, B Hock. pp. 305-332. Springer, Berlin.
Jennings DH 1995 The Physiology of Fungal Nutrition. Cambridge University Press, Cambridge.
Jun J, Abubaker J, Rehrer C, Pfeffer P E, Schachar-Hill Y and Lammers P J 2002 Expression in an arbuscular mycorrhizal fungus of genes putatively involved in metabolism, transport, the cyto skeleton and the cell cycle. Plant Soil 244, 141-148.
Koide RT and Schreiner RP 1992 Regulation of the vesiculararbuscular mycorrhizal symbiosis. Annu. Rev. Plant. Physiol. Mol. Biol. 43, 557-581.
Lammers P, Jun J, Abubaker J, Arreola R, Gopalan A, Bago B, Hernández C, Allen J, Douds DD, Pfeffer PE and Shachar-Hill Y 2001 Gene expression and glyoxylate cycle activity during of an arbuscular mycorrhizal fungus. Plant Physiol. 127, 1287-1298.
Lösel DM and Cooper KM 1979 Incorporation of 14C-labelled substrates by uninfected and VA mycorrhizal roots of onions. New Phytol. 834.
Martin F, Canet D and Marchal P 1985 13C NMR study of the mannitol cycle and trehalose synthesis during glucose utilization by ectomycorrhizal ascomycete Cenococcum graniforme. Plant Physiol. 77, 449-502.
Martin F, Boiffin V and Pfeffer PE 1998 Carbohydrate and amino acid metabolism in the Eucalyptus globulus-Pisolithus tinctorius ectomycorrhiza during glucose utilization. Plant Physiol. 118, 627-635.
MacDonald RM and Lewis M 1978 The occurrence of some acid phosphatases and dehydrogenases in the vesicular-arbuscular mycorrhizal fungus Glomus mosseae. New Phytol. 80, 135-141.
Murphy DJ 1991 Storage lipid bodies in plants and other organisms. Prog. Lipid Res. 29, 299-324.
Nagy S, Nordby HE and Nemec S 1980 Composition of lipids in roots of six citrus cultivars infected with the vesicular-arbuscular mycorrhizal fungus Glomus mosseae. New Phytol. 85, 377-382.
Pfeffer PE and Shachar-Hill Y 1996 Plant/microbe symbioses. In Nuclear Magnetic Resonance in Plant Biology. Eds. Y Shachar-Hill and PE Pfeffer. pp. 77-107. APS Press, Rockville, MD.
Pfeffer PE, Douds DD, Bécard G and Shachar-Hill Y 1999 Carbon uptake and the metabolism and transport of lipids in an arbuscular mycorrhiza. Plant Physiol. 120, 587-598.
Pfeffer PE, Bago B and Shachar-Hill Y 2001 Exploring mycorrhizal function with NMR spectroscopy. New Phytol. 150, 548-554.
Requena N, Mann P and Franken P 2000 A homologue of the cell cycle check point TOR2 from Saccharomyces cerevisiae exists in the arbuscular mycorrrhizal fungus Glomus mosseae. Protoplasma 212, 89-98.
Saito M 1995 Enzyme activities of the internal hyphae and germinated spores of an arbuscular mycorrhizal fungus, Gigaspora margarita Becker &; Hall. New Phytol. 129, 425-431.
Séjalon-Delmas N, Rogister I, Jauneau A, Roux C and Bécard G 2001 Carbon uptake during symbiotic, asymbiotic and presymbiotic stages of the AMfungus Glomus intraradices. Proceedings of ICOM3, Adelaide, p. P2 137.
Shachar-Hill Y, Pfeffer PE, Douds D, Osman SF, Doner LW and Ratcliffe RG 1995 Partitioning of intermediate carbon metabolism in VAM colonized leek. Plant Physiol. 108, 7-15.
Smith SE, Read DJ 1997 Mycorrhizal Symbiosis. Academic Press, London. 605 pp.
Smith SE and Smith FA 1990 Structure and function of the interfaces in biotrophic symbioses as they relate to nutrient transport. New Phytol. 114, 1-38.
Smith FA and Smith SE 1997 Structural diversity in (vesicular)-arbuscular mycorrhizal symbioses. New Phytol. 137, 373-388.
Solaiman MD and Saito M 1997 Use of sugars by intraradical hyphae of arbuscular mycorrhizal fungi revealed by radiorespirometry. New Phytol. 136, 533-538.
St-Arnaud M, Hamel C, Vimard B, Caron M and Fortin JA 1996 Enhanced hyphal growth and spore production of the arbuscular mycorrhizal fungus G. intraradices in an in vitro system in the absence of host roots. Mycol. Res. 100, 328-332.
Timonen S, Smith FA and Smith SE 2001 Microtubules of mycorrhizal fungus Glomus intraradices in symbiosis with tomato roots. Can. J. Bot. 79, 307-313.
Williams RM, Piston DW and Webb WW 1994 Two-photon molecular excitation provides intrinsic 3-dimensional resolution for laser-based microscopy and microphotochemistry. FASEB J. 8, 804-813.
Xu C and Webb WW 1996 Measurement of two-photon excitation cross sections of molecular fluorophores with data from 690 to 1050 nm. J. Opt. Soc. Am. (B) 13, 481-491.
Xu C, Zipfel W, Shear JB, Williams RM and Webb WW 1996 Multiphoton fluorescence excitation: New spectral windows for biological non-linear microscopy. Proc. Natl. Acad. Sci. USA 93, 10763-10768.
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Bago, B., Pfeffer, P.E., Zipfel, W. et al. Tracking metabolism and imaging transport in arbuscular mycorrhizal fungi. Metabolism and transport in AM fungi. Plant and Soil 244, 189–197 (2002). https://doi.org/10.1023/A:1020212328955
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DOI: https://doi.org/10.1023/A:1020212328955