Plugging into the network: Belowground connections between germlings and extraradical mycelium of arbuscular mycorrhizal fungi

Mycologia

Volumn 103, Issue 2, 2011, Pages 307-316

  Sbrana, Cristiana ^a   Fortuna, Paola ^a   Giovannetti, Manuela ^a  

^a UNIVERSITY OF PISA   (Italy)

Author keywords

Anastomosis; Arbuscular mycorrhizal fungi (AMF); Glomus mosseae; Nuclear mingling; Survival strategy; Vegetative compatibility and incompatibility

Indexed keywords

ARBUSCULAR MYCORRHIZA; FUNGUS; GENETIC VARIATION; HOST PLANT; RECOMBINATION; SPORE; SURVIVAL; SYMBIONT;

ARBUSCULAR; BACTERIA (MICROORGANISMS); FUNGI; GLOMUS MOSSEAE;

ARTICLE; AUBERGINE; GLOMEROMYCOTA; GROWTH, DEVELOPMENT AND AGING; MICROBIOLOGY; MYCELIUM; MYCORRHIZA; PARSLEY; PHYSIOLOGY; PLANT ROOT; SYMBIOSIS;

GLOMEROMYCOTA; MYCELIUM; MYCORRHIZAE; PETROSELINUM; PLANT ROOTS; SOLANUM MELONGENA; SYMBIOSIS;

EID: 79955961876     PISSN: 00275514     EISSN: 15572536     Source Type: Journal    
DOI: 10.3852/10-125     Document Type: Article

References (60)

1. Akiyama K, Matsuzaki KI, Hayashi H. 2005. Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824-827, doi:10.1038/ nature03608
2. Avio L, Sbrana C, Giovannetti M. 1990. The response of different species of Lupinus to VAM endophytes. Symbiosis 9:321-323.
3. Bago B, Zipfel W, Williams RM, Jun J, Arreola R, Lammers PJ, Pfeffer PE, Shachar Hill Y. 2002. Translocation and utilization of fungal storage lipid in the arbuscular mycorrhizal symbiosis. Plant Physiol 128:108-124, doi:10.1104/pp.010466
4. 2 and root exudates in vesicular-arbuscular mycorrhizal symbiosis. Appl Environ Microb 55:2320-2325.
5. Beilby JP, 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.
6. Bever JD, Wang M. 2005. Arbuscular mycorrhizal fungihyphal fusion and multigenomic structure. Nature 433: E3-E4, doi:10.1038/nature03294
7. Blair JE. 2009. Fungi. In: Hedges SB, Kumar S, eds. The timetree of life. Oxford, UK: Oxford Univ. Press. p 215-219.
8. Breuninger M, Requena N. 2004. Recognition events in AM symbiosis: analysis of fungal gene expression at the early appressorium stage. Fungal Genet Biol 41:794-804, doi:10.1016/j.fgb.2004.04.002
9. Buee M, Rossignol M, Jauneau A, Ranjeva R, Bécard G. 2000. The pre-symbiotic growth of arbuscular mycorrhizal fungi is induced by a branching factor partially purified from plant root exudates. MPMI 13:693-698, doi:10.1094/MPMI.2000.13.6.693
10. Buller AHR. 1933. Researches on fungi. London: Longmans, Green & Co. p 33-49.
11. Calonge FD. 1968. Origin and development of intrahyphal hyphae in Sclerotinia fructigena. Mycologia 60:932-942, doi:10.2307/3757395
12. Croll D, Giovannetti M, Koch AM, Sbrana C, Ehinger M, Lammers PJ, Sanders IR. 2009. Nonself vegetative fusion and genetic exchange in the arbuscular mycorrhizal fungus Glomus intraradices. New Phytol 181:924-937, doi:10.1111/j.1469-8137.2008.02726.x
13. David Schwartz R, Badani H, Smadar W, Levy AA, Galili G, Kapulnik Y. 2001. Identification of a novel genetically controlled step in mycorrhizal colonization: plant resistance to infection by fungal spores but not extraradical hyphae. Plant J 27:561-569, doi:10.1046/ j.1365-313X.2001.01113.x
14. Gardes M, Wong KKY, Fortin JA. 1990. Interactions between monokaryotic and dikaryotic isolates of Laccaria bicolor on roots of Pinus banksiana. Symbiosis 8:233-250.
15. Giovannetti M. 2001. Survival strategies in arbuscular mycorrhizal symbionts. In: Seckbach J, ed. Symbiosis mechanisms and model systems. Dordrecht, the Netherlands: Academic Publisher. p 185-196.
16. Giovannetti M, Avio L, Sbrana C, Citernesi AS. 1993a. Factors affecting appressorium development in the vesiculararbuscular mycorrhizal fungus Glomus mosseae (Nicol. & Gerd.) Gerd. & Trappe. New Phytol 123:114-122.
17. Giovannetti M, Azzolini D, Citernesi AS. 1999. Anastomosis formation and nuclear and protoplasmic exchange in arbuscular mycorrhizal fungi. Appl Environ Microb 65: 5571-5575.
18. Giovannetti M, Fortuna P, Citernesi AS, Morini S, Nuti MP. 2001. The occurrence of anastomosis formation and nuclear exchange in intact arbuscular mycorrhizal networks. New Phytol 151:717-724, doi:10.1046/j.0028-646x.2001. 00216.x
19. Giovannetti M, Sbrana C. 2001. Self and non-self responses in hyphal tips of arbuscular mycorrhizal fungi. In: Geitmann A, Cresti M, eds. Cell biology of plant and fungal tip growth, NATO Science Series I: life and behavioural sciences. Vol. 328. Amsterdam, the Netherlands: IOS Press. p 221-231.
20. Giovannetti M, Sbrana C, Avio L, Citernesi AS, Logi C. 1993b. Differential hyphal morphogenesis in arbuscular mycorrhizal fungi during pre-infection stages. New Phytol 125:587-594, doi:10.1111/j.1469-8137.1993.tb03907.x
21. Giovannetti M, Sbrana C, Avio L, Strani P. 2004. Patterns of belowground plant interconnections established by means of arbuscular mycorrhizal networks. New Phytol 164:175-181, doi:10.1111/j.1469-8137.2004.01145.x
22. Giovannetti M, Sbrana C, Logi C. 1994. Early processes involved in host recognition by arbuscular mycorrhizal fungi. New Phytol 127:703-709, doi:10.1111/j.1469-8137.1994. tb02973.x
23. Giovannetti M, Sbrana C, Strani P, Agnolucci M, Rinaudo V, Avio L. 2003. Genetic diversity of isolates of Glomus mosseae from different geographic areas detected by vegetative compatibility testing and biochemical and molecular analysis. Appl Environ Microb 69:616-624, doi:10. 1128/AEM.69.1.616-624.2003
24. Glass NL, Jacobson DJ, Shiu PKT. 2000. The genetics of hyphal fusion and vegetative incompatibility in filamentous ascomycete fungi. Annu Rev Genet 34:165-186, doi:10.1146/annurev.genet.34.1.165
25. Glass NL, Rasmussen C, Roca MG, Read ND. 2004. Hyphal homing, fusion and mycelial interconnectedness. Trends Microbiol 12:135-141, doi:10.1016/j.tim.2004. 01.007
26. Glenn MG, Chew FS, Williams PH. 1988. Influence of glucosinolate content of Brassica (Cruciferae) roots on growth of vesicular-arbuscular mycorrhizal fungi. New Phytol 110:217-225, doi:10.1111/j.1469-8137.1988. tb00255.x
27. - mutant of Pisum sativum L. Planta 191:112-122, doi:10.1007/BF00240902
28. Hamel C, Flyes H, Smith DL. 1990. Measurement of development of endomycorrhizal mycelium using three different vital stains. New Phytol 115:297-302, doi:10.1111/j.1469-8137.1990.tb00455.x
29. Harrison MJ, van Buuren ML. 1995. A phosphate transporter from the mycorrhizal fungus Glomus versiforme. Nature 378:626-629, doi:10.1038/378626a0
30. Helgason T, Watson IJ, Young JPW. 2003. Phylogeny of the Glomerales and Diversisporales (Fungi: Glomeromycota) from actin and elongation factor 1-alpha sequences. FEMS Microbiol Lett 229:127-132, doi:10.1016/S0378-1097(03)00802-4
31. Hepper CM. 1983. Limited independent growth of a vesicular-arbuscular mycorrhizal fungus in vitro. New Phytol 93:537-542, doi:10.1111/j.1469-8137.1983. tb02704.x
32. Hijri M, Sanders IR. 2005. Low gene copy number shows that arbuscular mycorrhizal fungi inherit genetically different nuclei. Nature 433:160-163, doi:10.1038/ nature03069
33. Koch AM, Kuhn G, Fontanillas P, Fumagalli L, Goudet I, Sanders IR. 2004. High genetic variability and low local diversity in a population of arbuscular mycorrhizal fungi. Proc Natl Acad Sci USA 101:2369-2374, doi:10.1073/pnas.0306441101
34. Koske RE. 1981. Gigaspora gigantea: observations on spore germination of a VA- mycorrhizal fungus. Mycologia 73: 288-300, doi:10.2307/3759650
35. Kuhn G, Hijri M, Sanders IR. 2001. Evidence for the evolution of multiple genomes in arbuscular mycorrhizal fungi. Nature 414:745-748, doi:10.1038/414745a
36. Kytoviita MM. 2000. Do symbiotic fungi refresh themselves by incorporating their own or closely related spores into existing mycelium? Oikos 90: 606-608, doi:10.1034/j.1600-0706.2000.900318.x
37. Lim LL, Fineran BA, Cole ALJ. 1983. Ultrastructure of intrahyphal hyphae of Glomus fasciculatum (thaxter) Gerdemann & Trappe in roots of white clover (Trifolium repens L.). New Phytol 95:231-239, doi:10.1111/j.1469-8137.1983.tb03489.x
38. Lloyd-Macgilp SA, Chambers SM, Dodd JC, Fitter AH, Walker C, Young JPW. 1996. Diversity of the ribosomal internal transcribed spacers within and among isolates of Glomus mosseae and related mycorrhizal fungi. New Phytol 133:103-111, doi:10.1111/j.1469-8137.1996. tb04346.x
39. Logi C, Sbrana C, Giovannetti M. 1998. Cellular events involved in survival of individual arbuscular mycorrhizal symbionts growing in the absence of the host. Appl Environ Microb 64:3473-3479.
40. Morton JB. 1990. Evolutionary relationships among arbuscular mycorrhizal fungi in the Endogonaceae. Mycologia 82:192-207, doi:10.2307/3759848
41. Mosse B. 1959. The regular germination of resting spores and some observations on the growth requirements of an Endogone sp. causing vesicular-arbuscular mycorrhiza. Trans Br Mycol Soc 42:273-286, doi:10.1016/S0007-1536(56)80033-8
42. Phipps CJ, Taylor TN. 1996. Mixed arbuscular mycorrhizae from the Triassic of Antarctica. Mycologia 88:707-714, doi:10.2307/3760964
43. Pirozynski KA. 1981. Interactions between fungi and plants through the ages. Can J Bot 59:1824-1827.
44. Pirozynski KA, Malloch DW. 1975. The origin of land plants: a matter of mycotrophism. Bio Syst 6:153, doi:10.1016/ 0303-2647(75)90023-4
45. Redecker D, Kodner R, Graham LE. 2000. Glomalean fungi from the Ordovician. Science 289: 1920-1921, doi:10.1126/science.289.5486.1920
46. Remy W, Taylor TN, Hass H, Kerp H. 1994. Four hundred million-year-old vesicular arbuscular mycorrhizae. P Natl Acad Sci USA 91:11841-11843, doi:10.1073/ pnas.91.25.11841
47. Requena N, Breuninger M, Franken P, Ocon A. 2003. Symbiotic status, phosphate and sucrose regulate the expression of two plasma membrane H+ -ATPase genes from the mycorrhizal fungus Glomus mosseae. Plant Physiol 132:1540-1549, doi:10.1104/pp.102.019042
48. Requena N, Mann P, Franken P. 2000. A homolog of the cell cycle check point TOR2 from Saccharomyces cerevisiae exists in the arbuscular mycorrrhizal fungus Glomus mosseae. Protoplasma 212: 89-98, doi:10.1007/BF01279350
49. Requena N, Mann P, Hampp R, Franken P. 2002. Early develop- mentally regulated genes in the arbuscular mycorrhizal fungus Glomus mosseae: identification of GmGIN1, a novel gene with homology to the C-terminus of metazoan hedgehog proteins. Plant Soil 244:129-139, doi:10.1023/A:1020249932310
50. Sanders IR, Alt M, Groppe K, Boller T, Wiemken A. 1995. Identification of ribosomal DNA polymorphisms among and within spores of the Glomales: application to studies on the genetic diversity of arbuscular mycorrhizal fungal communities. New Phytol 130:419-427, doi:10.1111/j.1469-8137.1995.tb01836.x
51. Saupe SJ. 2000. Molecular genetics of heterokaryon incompatibility in filamentous ascomycetes. Microbiol Mol Biol Rev 64:489-502, doi:10.1128/MMBR.64.3. 489-502.2000
52. Sbrana C, Avio L, Giovannetti M. 1995. The occurrence of calcofluor and lectin binding polysaccharides in the outer wall of AM fungal spores. Mycol Res 99:1249-1252, doi:10.1016/S0953-7562(09)80287-6
53. Schubert A, Marzachí C, Mazzitelli M, Cravero MC, Bonfante-Fasolo P. 1987. Development of total and viable extraradical mycelium in the vesicular-arbuscular mycorrhizal fungus Glomus clarum Nicol. & Schenck. New Phytol 107:183-190, doi:10.1111/j.1469-8137. 1987.tb04892.x
54. Simon L, Bousquet J, Levesque RC, Lalonde M. 1993. Origin and diversification of endomycorrhizal fungi and coincidence with vascular land plants. Nature 363: 67-69, doi:10.1038/363067a0
55. Smith SE, Gianinazzi-Pearson V. 1990. Phosphate uptake and arbuscular activity in mycorrhizal Allium cepa L.: effects of photon irradiance and phosphate nutrition. Aust J Plant Physiol 17:177-188, doi:10.1071/PP9900177
56. Smith SE, Read DJ. 2008. Mycorrhizal simbiosis. London:Academic Press. 787 p.
57. States JS. 1975. Intrahyphal hyphae in the Basidiomycete Gloeophyllum (Lenzites) saepiarium. Mycologia 67:417-420, doi:10.2307/3758433
58. Tommerup IC. 1984. Persistence of infectivity by germinated spores of vesicular-arbuscular mycorrhizal fungi in soil. Trans Br Mycol Soc 82:275-282, doi:10.1016/S0007-1536(84)80069-8
59. van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR. 1998. Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69-72, doi:10.1038/23932
60. Vierheilig H, Böckenhoff A, Knoblauch M, Juge C, van Bel A, Piché Y, Grundler FMW, Wyss U. 1999. In vivo observations of the arbuscular mycorrhizal fungus Glomus mosseae in roots by confocal laser scanning microscopy. Mycol Res 103:311-314, doi:10.1017/S0953756298007576