Molecular and cellular aspects of the arbuscular mycorrhizal symbiosis

Annual Review of Plant Biology

Volumn 50, Issue , 1999, Pages 361-389

  Harrison, Maria J ^a  

^a PLANT BIOLOGY DIVISION   (United States)

Author keywords

Fungus; Interaction; Phosphate transport; Plant microbe; Rhizobium legume symbiosis; Root

Indexed keywords

ARBUSCULAR MYCORRHIZAE; BRYOPHYTA; BRYOPHYTES; FUNGI; GLOMERALES; GYMNOSPERMAE; MAGNOLIOPHYTA; MYCORRHIZAE; PTERIDOPHYTA; RHIZOBIUM;

EID: 0033505252     PISSN: 15435008     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.arplant.50.1.361     Document Type: Article

References (214)

1. Abbas JD, Hetrick BAD, Jurgenson JE. 1996. Isolate specific detection of mycorrhizal fungi using genome specific primer pairs, Mycologia 88:939-46
2. Albrecht C, Geurts R, Lapeyrie F, Bisseling T. 1998. Endomycorrhizae and rhizobial nod factors activate signal transduction pathways inducing PsENOD5 and PsENOD12 expression in which Sym8 is a common step. Plant J. 15:605-15
3. Alexander D, Goodman RM, Gut-Rella M, Glascock C, Weymann K, et al. 1993. Increased tolerance to two oomycete pathogens in transgenic tobacco expressing pathogenesis-related protein1a. Proc. Natl. Acad. Sci. USA 90:7327-31
4. Alexander T, Meier R, Toth R, Weber HC. 1988. Dynamics of arbuscule development and degeneration in my corrhizas of Triticum aestivum L. and Avena sativa L. with reference to Zea mays L. New Phytol. 110:363-70
5. Alexander T, Toth R, Meier R, Weber HC. 1989. Dynamics of arbuscule development and degeneration in onion, bean and tomato with reference to vesicular-arbuscular mycorrhizae in grasses. Can. J. Bot. 67:2505-13
6. Allen MF. 1996. The ecology of arbuscular mycorrhizas: a look back into the 20th century and a peek into the 21st. Mycol. Res. 100:769-82
7. Allen MF, Allen EB, Friese CF. 1989. Responses of the non-mycotrophic plant Salsola kali to invasion by vesicular-arbuscular mycorrhizal fungi. New Phytol. 111:45-49
8. Arines J, Palma JM, Vilarino A. 1993. Comparison of protein patterns in nonmycorrhizal and vesicular-arbuscular myeorrhizal roots of red clover. New Phytol. 123;763-68
9. Ayling SM, Smith SE, Smith FA, Kolesik P. 1997. Transport processes at the plant-fungus interface in mycorrhizal associations: physiological studies. Plant Soil 196:305-10
10. Azcon-Aguilar C, Barea JM, eds. 1996. Mycorrhizas in Integrated Systems from Genes to Plant Development. Brussels: Eur. Comm.
11. Bago B, Azcón-Aguilar C, Goulet A, Piché Y. 1998. Branched absorbing structures (BAS): a feature of the extraradical mycelium of symbiotic arbuscular mycorrhizal fungi. New Phytol. 139:375-88
12. Bago B, Azcón-Aguilar C, Piché Y. 1998. Architecture and developmental dynamics of the external mycelium of the arbuscular mycorrhizal fungus Glomus intraradices grown under monoxenic conditions. Mycologia 90:52-62
13. Bago B, Chamberland H, Goulet A, Vierheilig H, Lafontaine J-G, Piché Y. 1996. Effect of Nikkomycin Z, a chitin-synthase inhibitor, on hyphal growth and cell wall structure of two arbuscular-mycorrhizal fungi. Protoplasma 192:80-92
14. Bago B, Vierheilig H, Piché Y, Azcón-Aguilar C. 1996. Nitrate depletion and pH changes induced by the extraradical mycelium of the arbuscular mycorrhizal fungus Glomus intraradices grown in monoxenic culture. New Phytol. 133:273-80
15. Balaji B, Ba AM, LaRue TA, Tepfer D, Piché Y. 1994. Pisum sativum mutants insensitive to nodulation are also insensitive to invasion in vitro by the mycorrhizal fungus, Gigaspora margarita. Plant Sci. 102:195-203
16. Balaji B, Poulin MJ, Vierheilig H, Piché Y. 1995. Responses of an arbuscular mycorrhizal fungus, Gigaspora margarita, to exudates and volatiles from the Ri T-DNA-transformed roots of nonmycorrhizal and mycorrhizal mutants of Pisum sativum L. sparkle. Exp. Mycol. 19:275-83
17. Deleted in proof
18. Balestrini R, Berta G, Bonfante P. 1992. The plant nucleus in mycorrhizal roots: positional and structural modifications. Biol. Cell 75:235-43
19. Balestrini R, Hahn MG, Faccio A, Mendgen K, Bonfante P. 1996. Differential localization of carbohydrate epitopes in plant cell walls in the presence and absence of arbuscular mycorrhizal fungi. Plant Physiol. 111:203-13
20. Balestrini R, José-Estanyol M, Puigdoménech P, Bonfante P. 1997. Hydroxyproline-rich glycoprotein mRNA accumulation in maize root cells colonized by an arbuscular mycorrhizal fungus as revealed by in situ hybridization. Protoplasma 198:36-42
21. Balestrini R, Romera C, Puigdoménech P, Bonfante P. 1994. Location of a cell-wall hydroxyproline-rich glycoprotein, cellulose and β-1,3-glucans in apical and differentiated regions of maize mycorrhizal roots. Planta 195:201-9
22. Barker SJ, Stummer B, Gao L, Dispain I, O'Connor PJ, Smith SE. 1998. A mutant in Lycopersicon esculentum Mill with highly reduced VA mycorrhizal colonisation: isolation and preliminary characterisation. Plant J. 15:791-99
23. 2 and flavonols. Appl. Environ. Microbiol. 58:821-25
24. Bécard G, Fortin JA. 1988. Early events of vesicular-arbuscular mycorrhiza formation on Ri T-DNA transformed roots. New Phytol. 108:211-18
25. Bécard G, Pfeffer PE. 1993. Status of nuclear division in arbuscular mycorrhizal fungi during in vitro development. Protoplasma 174:62-68
26. 2 and root exudates in vesicular-arbuscular mycorrhizal symbiosis. Appl. Environ. Microbiol. 55:2320-25
27. Bécard G, Taylor LP, Douds DD Jr, Pfeffer PE, Doner LW. 1995. Flavonoids are not necessary plant signals in arbuscular mycorrhizal symbiosis. Mol. Plant-Microbe Interact. 8:252-58
28. Bentivenga SP, Morton JB. 1994. Systematics of Glomalean endomycorrhizal fungi: current views and future direction. In Mycorrhizae and Plant Health, ed. FL Pfleger, RG Linderman, pp. 283-308. St. Paul, MN: APS Press
29. Bevege DI, Bowen GD, Skinner MF. 1975. Comparative carbohydrate physiology of ecto and endomycorrhizas. In Endomycorrhizas, ed. FE Saunders, B Mossae, PB Tinker, pp. 149-74. London: Academic
30. Bianciotto V, Barbiero G, Bonfante P. 1995. Analysis of the cell cycle in arbuscular mycorrhizal fungus by flow cytometry and bromodeoxyuridine labelling. Protoplasma 188:161-69
31. Bianciotto V, Bonfante P. 1992. Quantification of the nuclear DNA content of two arbuscular mycorrhizal fungi. Mycol. Res. 96:1071-76
32. Blee KA, Anderson AJ. 1996. Defense-related transcript accumulation in Phaseolus vulgaris L. colonized by the arbuscular mycorrhizal fungus Glomus intraradices. Plant Physiol. 110:675-88
33. Bonfante P, Bergero R, Uribe X, Romera C, Rigau J, Puigdoménech P. 1996. Transcriptional activation of a maize α-tubulin gene in mycorrhizal maize and transgenic tobacco plants. Plant J. 9:737-43
34. Bonfante P, Perotto S. 1995. Strategies of arbuscular mycorrhizal fungi when infecting host plants. New Phytol. 130:3-21
35. Bonfante-Fasolo P. 1984. Anatomy and morphology of VA mycorrhizae. In VA Mycorrhizae, ed. CL Powell, DJ Bagyaraj, pp. 5-33. Boca Raton, FL: CRC Press
36. Bonfante-Fasolo P, Perotto S. 1990. My-corrhizal and pathogenic fungi: Do they share any features? In Electron Microscopy Applied in Plant Pathology, ed. K Mendgen, DE Lesemann, pp. 265-75. Berlin: Springer-Verlag
37. Bonfante-Fasolo P, Perotto S. 1992. Plant and endomycorrhizal fungi: the cellular and molecular basis of their interaction. In Molecular Signals in Plant-Microbe Communications, ed. DPS Verma, pp. 445-70. Boca Raton, FL: CRC Press
38. Bradbury SM, Peterson RL, Bowley SR. 1991. Interaction between three alfalfa nodulation genotypes and two Glomus species. New Phytol. 119:115-20
39. Bradbury SM, Peterson RL, Bowley SR. 1993. Further evidence for a correlation between nodulation genotypes in alfalfa (Medicago sativa L.) and mycorrhiza formation. New Phytol. 124:665-73
40. Broglie K, Chet I, Holliday M, Cressman R, Biddle P, et al. 1991. Transgenic plants with enhanced resistance to the fungal pathogen, Rhizoctonia solani. Science 254:1194-97
41. Burggraaf AJP, Beringer JE. 1988. Absence of nuclear DNA synthesis in vesicular-arbuscular mycorrhizal fungi during in vitro development. New Phytol. 111:25-37
42. Burleigh SH, Harrison MJ. 1997. A novel gene whose expression in Medicago truncatula roots is suppressed in response to colonization by vesicular-arbuscular mycorrhizal (VAM) fungi and to phosphate nutrition. Plant Mol. Bol. 34:199-208
43. Burleigh SH, Harrison MJ. 1998. A cDNA from the arbuscular mycorrhizal fungus Glomus versiforme with homology to a cruciform DNA-binding protein from Ustilago maydis. Mycorrhiza 7:301-6
44. Büschges R, Hollricher K, Panstruga R, Simons G, Wolter M, et al. 1997. The barley Mlo gene: a novel control element of plant pathogen resistance. Cell 88:695-705
45. Deleted in proof
46. Cairney JGW, Smith SE. 1993. Efflux of phosphate from the ectomycorrhizal basidiomycete Pisolithus tinctorius: general characteristics and the influence of intracellular phosphorus concentration. Mycol. Res. 97:1261-66
47. Carling DE, Brown MF. 1982. Anatomy and physiology of vesicular-arbuscular and nonmycorrhizal roots. Phytopathology 72:1108-14
48. 2-enriched conditions. New Phytol. 122:461-67
49. Chen X-Y, Hampp R. 1993. Sugar uptake by protoplasts of the ectomycorrhizal fungus Amanita muscaria. New Phytol. 125:601-8
50. Clapp JP, Young JPW, Merryweather JW, Fitter AH. 1995. Diversity of fugal symbionts in arbuscular mycorrhizas from a natural community. New Phytol 130:259-65
51. Cox G, Tinker PB. 1976. Translocation and transfer of nutrients in vesicular-arbuscular mycorrhizas. I. The arbuscule and phosphorus transfer: a quantitative ultrastructural study. New Phytol. 77:371-78
52. Dassi B, Dumas-Gaudot E, Asselin A, Richard C, Gianinazzi S. 1996. Chitinase and β-1,3-glucanase isoforms expressed in pea roots inoculated with arbuscular mycorrhizal or pathogenic fungi. Eur. J. Plant Pathol. 102:105-8
53. David R, Itzhaki H, Ginzberg I, Gafni Y, Galili G, Kapulnik Y. 1998. Suppression of tobacco basic chitinase gene expression in response to colonization by the arbuscular mycorrhizal fungus Glomus intraradices. Mol. Plant-Microbe Interact. 11:489-97
54. Dean JV, Devarenne TP, Lee I-S, Orlofsky LE. 1995. Properties of a maize glutathione S-transferase that conjugates coumaric acid and other phenylpropanoids. Plant Physiol. 108:985-94
55. Declerck S, Strullu DG, Plenchette C. 1996. In vitro mass-production of the arbuscular mycorrhizal fungus, Glomus versiforme, associated with Ri T-DNA transformed carrot roots. Mycol. Res. 100:1237-42
56. Di Bonito R, Elliott ML, Des Jardin EA. 1995. Detection of an arbscular mycorrhizal fungus in roots of different plant species with the PCR. Appl. Environ. Microbiol. 61:2809-10
57. Diop TA, Bécard G, Piché Y. 1992. Long-term in vitro culture of an endomycorrhizal fungus, Gigaspora margarita, on Ri T-DNA transformed roots of carrot. Symbiosis 12:249-59
58. Diop TA, Plenchette C, Strullu DG. 1994. Dual axenic culture of shearedroot inocula of vesicular-arbuscular mycorrhizal fungi associated with tomato roots. Mycorrhiza 5:17-22
59. Dixon RA, Harrison MJ, Lamb CJ. 1994. Early events in the activation of plant defense responses. Annu Rev. Phytopathol. 32:479-501
60. Dodd JC, Rosendahl S, Giovannetti M, Broome A, Lanfranco L, Walker C. 1996. Inter- and intraspecific variation within the morphologically-similar arbuscular mycorrhizal fungi Glomus mosseae and Glomus coronatum. New Phytol. 133:113-22
61. Douds DD Jr. 1997. A procedure for the establishment of Glomus mosseae in dual culture with Ri T-DNA-transformed carrot roots. Mycorrhiza 7:57-61
62. Douds DD Jr, Galvez L, Becard G, Kapulnik Y. 1998. Regulation of arbuscular mycorrhizal development by plant host and fungus species in alfalfa. New Phytol. 138:27-35
63. Douds DD Jr, Nagahashi G, Abney GD. 1996. The differential effects of cell wall-associated phenolics, cell walls, and cytosolic phenolics of host and nonhost roots on the growth of two species of AM fungi. New Phytol. 133:289-94
64. Duc G, Trouvelot A, Gianinazzi-Pearson V, Gianinazzi S. 1989. First report of non-mycorrhizal mutants (Myc-) obtained in pea (Pisum sativum L.) and Fababean (Vicia faba L.). Plant Sci. 60:215-22
65. Dumas-Gaudot E, Furlan V, Grenier J, Asselin A. 1992. New acidic chitinase isoforms induced in tobacco roots by vesicular-arbuscular mycorrhizal fungi. Mycorrhiza 1:133-36
66. Dumas-Gaudot E, Guillaume P, Tahiri-Alaoui A, Gianinazzi-Pearson V, Gianinazzi S. 1994. Changes in polypeptide patterns in tobacco roots colonized by two Glomus species. Mycorrhiza 4:215-21
67. Edwards SG, Fitter AH, Young JPW. 1997. Quantification of an arbuscular mycorrhizal fungus, Glomus mosseae, within plant roots by competitive polymerase chain reaction. Mycol. Res. 101:1440-44
68. Forbes PJ, Millam S, Hooker JE, Harrier LA. 1998. Transformation of the arbuscular mycorrhizal fungus Gigaspora rosea by particle bombardment. Mycol. Res. 102:497-501
69. Frank B. 1885. Ueber die auf Wurzelsymbiose beruhende Ernährung gewisser Bäume durch unterirdische Pilze. Ber. Dtsch. Bot. Ges. 3:128-45
70. Franken P, Gianinazzi-Pearson V. 1996. Construction of genomic phage libraries of the arbuscular mycorrhizal fungi Glomus mosseae and Scutellospora castanea and isolation of ribosomal RNA genes. Mycorrhiza 6:167-73
71. Franken P, Gnädinger F. 1994. Analysis of parsley arbuscular endomycorrhiza: infection development and mRNA levels of defense-related genes. Mol. Plant-Microbe Interact. 7:612-20
72. Franken P, Lapopin L, Meyer-Gauen G, Gianinazzi-Pearson V. 1997. RNA accumulation and genes expressed in spores of the arbuscular mycorrhizal fungus, Gigaspora rosea. Mycologia 89:293-97
73. Freialdenhoven A, Peterhänsel C, Kurth J, Kreuzaler F, Schulze-Lefert P. 1996. Identification of genes required for the function of non-race-specific mlo resistance to powdery mildew in barley. Plant Cell 8:5-14
74. Friese CF, Allen MF. 1991. The spread of VA mycorrhizal fungal hyphae in the soil: inoculum types and external hyphal architecture. Mycologia 83:409-18
75. Frühling M, Roussel H, Gianinazzi-Pearson V, Fühler A, Perlick AM. 1997. The Vicia faba leghemoglobin gene VfLb29 is induced in root nodules and in roots colonized by the arbuscular mycorrhizal fungus Glomus fasciculatum. Mol. Plant-Microbe Interact. 10:124-31
76. Gallaud I. 1905. Etudes sur les mycorrhizesendotrophes. Rév. Gen. Bot. 17:5-48
77. Galun M, Bubrick P. 1984. Physiological interactions between partners of the lichen symbiosis. In Cellular Interactions. Encyclopedia of Plant Physiology, ed. HF Linskins, J Heslop-Harrison, 17:362-401. Berlin: Springer-Verlag
78. García-Garrido JM, Cabello MN, García-Romera I, Ocampo JA. 1992. Endoglucanase activity in lettuce plants colonized with the vesicular-arbuscular mycorrhizal fungus Glomus fasciculatum. Soil Biol. Biochem. 24:955-59
79. Garcia-Garrido JM, Garcia-Romera I, Ocampo JA. 1992. Cellulase production by the vesicular-arbuscular mycorrhizal fungus Glomus mosseae (Nicol. & Gerd.) Gerd, and Trappe. New Phytol. 121:221-26
80. García-Garrido JM, García-Romera I, Parra-García MD, Ocampo JA. 1996. Purification of an arbuscular mycorrhizal endoglucanase from onion roots colonized by Glomus mosseae. Soil Biol. Biochem. 28:1443-49
81. Garcia-Garrido JM, Toro N, Ocampo JA. 1993. Presence of specific polypeptide in onion roots colonized by Glomus mosseae. Mycorrhiza 2:175-77
82. Garcia-Romera I, Garcia-Garrido JM, Martinez-Molina E, Ocampo JA. 1991. Production of pectolytic enzymes in lettuce root colonized by Glomus mosseae. Soil Biol. Biochem. 23:597-601
83. Genre A, Bonfante P. 1997. A mycorrhizal fungus changes microtubule orientation in tobacco root cells. Protoplasma 199:30-38
84. Gerdemann JW. 1965. Vesicular-arbuscular mycorrhizas formed on maize and tulip tree by Endogene fasciculata. Mycologia 57:562-75
85. Gianinazzi-Pearson V. 1996. Plant cell responses to arbuscular myorrhiza fungi: getting to the roots of the symbiosis. Plant Cell 8:1871-83
86. Gianinazzi-Pearson V, Branzanti B, Gianinazzi S. 1989. In vitro enhancement of spore germination and early hyphal growth of a vesicular-arbuscular mycorrhizal fungus by host root exudates and plant flavonoids. Symbiosis 7:243-55
87. Gianinazzi-Pearson V, Dumas-Gaudot E, Gollotte A, Tahiri-Alaoui A, Gianinazzi S. 1996. Cellular and molecular defence-related root responses to invasion by arbuscular mycorrhizal fungi. New Phytol. 133:45-57
88. Gianinazzi-Pearson V, Gianinazzi S, Guillemin JP, Trouvelot A, Duc G. 1991. Genetic and cellular analysis of resistance to vesicular arbuscular (VA) mycorrhizal fungi in pea mutants. In Advances in Molecular Genetics of Plant-Microbe Interactions, ed. H Hennecke, DPS Verma, 1:336-42. Dordrecht, Netherlands: Kluwer
89. Gianinazzi-Pearson V, Smith SE, Gianinazzi S, Smith FA. 1991. Enzymatic studies on the metabolism of vesicular-arbuscular mycorrhizas. New Phytol. 117:61-74
90. Giovannetti M, Avio L, Sbrana C, Citernesi AS. 1993. Factors affecting appressorium development in the vesicular-arbuscular mycorrhizal fungus Glomus mosseae (Nicol. & Gerd.) Gerd. & Trappe. New Phytol. 123:115-22
91. Giovannetti M, Sbrana C, Avio L, Citernesi AS, Logi C. 1993. Differential hyphal morphogenesis in arbuscular mycorrhizal fungi during pre-infection stages. New Phytol. 125:587-93
92. Giovannetti M, Sbrana C, Citernesi AS, Avio L. 1996. Analysis of factors involved in fungal recognition responses to host-derived signals by arbuscular mycorrhizal fungi. New Phytol. 133:65-71
93. Giovannetti M, Sbrana C, Logi C. 1994. Early processes involved in host recognition by arbuscular mycorrhizal fungi. New Phytol. 127:703-9
94. Gollotte A, Gianinazzi-Pearson V, Gianinazzi S. 1995. Immunodetection of infection thread glycoprotein and ara-binogalactan protein in wild type Pisusativum (L.) or an isogenic mycorrhiza-resistant mutant interacting with Glomus mosseae. Symbiosis 18:69-85
95. Gollotte A, Gianinazzi-Pearson V, Giovannetti M, Sbrana C, Avio L, Gianinazzi S. 1993. Cellular localization and cytochemical probing of resistance reactions to arbuscular mycorrhizal fungi in a 'locus a' myc-mutant of Pisum sativum L. Planta 191:112-22
96. Hahn M, Neef U, Struck C, Göttfert M, Mendgen K. 1997. A putative amino acid transporter is specifically expressed in haustoria of the rust fungus Uromyces fabae. Mol. Plant-Microbe Interact. 10: 438-45
97. Harley JL, Smith SE. 1983. Mycorrhizal Symbiosis. London/New York: Academic
98. Harrison MJ. 1996. A sugar transporter from Medicago truncatula: altered expression pattern in roots during vesicular-arbuscular (VA) mycorrhizal associations. Plant J. 9:491-503
99. Harrison MJ, Dixon RA. 1993. Isoflavonoid accumulation and expression of defense gene transcripts during the establishment of vesicular-arbuscular mycorrhizal associations in roots of Medicago truncatula. Mol. Plant-Microbe Interact. 6:643-54
100. Harrison MJ, Dixon RA. 1994. Spatial patterns of expression of flavonoid/isoflavonoid pathway genes during interactions between roots of Medicago truncatula and the mycorrhizal fungus Glomus versiforme. Plant J. 6:9-20
101. Harrison MJ, van Buuren ML. 1995. A phosphate transporter from the mycorrhizal fungus Glomus versiforme. Nature 378:626-29
102. Hinde R. 1983. Host release factors in symbioses between algae and invertebrates. In Endocytobiology II. Intracellular Space as Oligogenetic System, ed. HEA Schenk, W Schwemmler, pp. 709-26. Berlin/New York: Walter de Gruyter
103. 14C from Festuca plants to their endomycorrhizal fungi. Nature 244:30-31
104. Hosny M, de Barros J-PP, Gianinazzi-Pearson V, Dulieu H. 1997. Base composition of DNA from glomalean fungi: high amounts of methylated cytosine. Fungal Genet. Bol. 22:103-11
105. Hosny M, Gianinazzi-Pearson V, Dulieu H. 1998. Nuclear DNA contents of eleven fungal species in Glomales. Genome 41:422-28
106. Jacobs M, Rubery PH. 1988. Naturally occurring auxin transport regulators. Science 241:346-49
107. Jacquelinet-Jeanmougin S, Gianinazzi-Pearson V. 1983. Endomycorrhizas in the Gentianaceae. I. The fungus associated with Gentiana lutea L. New Phytol. 95:663-66
108. Jolicoeur M, Germette S, Gaudette M, Perrier M, Becard G. 1998. Intracellular pH in arbuscular mycorrhizal fungia symbiotic physiological marker. Plant Physiol. 116:1279-88
109. Kaldorf M, Schmelzer E, Bothe H. 1998. Expression of maize and fungal nitrate reductase genes in arbuscular mycorrhiza. Mol. Plant-Microbe Interact. 11:439-48
110. Kape R, Wex K, Pamiske M, Gorge E, Wetzel A, Werner D. 1992. Legume root metabolites and VA-mycorrhiza development. J. Plant Physiol. 141:54-60
111. Kapulnik Y, Volpin H, Itzhaki H, Ganon D, Galili S, et al. 1996. Suppression of defence responses in mycorrhizal alfalfa and tobacco roots. New Phytol. 133:59-64
112. Koide RT, Schreiner RP. 1992. Regulation of the vesicular-arbuscular mycorrhizal symbiosis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 43:557-81
113. Lagunas R. 1993. Sugartransport in Sacharomyces cerevisiae. FEMS Microbiol. Rev. 104:229-42
114. Lambais MR, Mehdy MC. 1993. Suppression of endochitinase, β-1,3-endoglucanase, and chalcone isomerase expression in bean vesicular-arbuscular mycorrhizal roots under different soil phosphate conditions. Mol. Plant-Microbe Interact. 6:75-83
115. Lambais MR, Mehdy MC. 1996. Soybean roots infected by Glomus intra-radices strains differing in infectivitexhibit differential chitinase and β-1,3-glucanase expression. New Phytol. 134:531-38
116. Lanfranco L, Wyss P, Marzachi C, Bonfante P. 1995. Generation of RAPD-PCR primers for the identification of isolates of Glomus mosseae, an arbuscular mycorrhizal fungus. Mol. Ecol. 4:61-68
117. Leggewie G, Willmitzer L, Riesmeier JW. 1997. Two cDNAs from potato are able to complement a phosphate uptakedeficient yeast mutant: identification of phosphate transporters from higher plants. Plant Cell 9:381-92
118. 32P uptake and plasmalemma ATPase activity in vesicular-arbuscular mycorrhizal fungus, Gigaspora margarita. New Phytol. 118:289-94
119. Liu C, Muchhal US, Uthappa M, Kononowicz AK, Raghomama KG. 1998. Tomato phosphate transporter genes are differentially regulated in plant tissues by phosphorus. Plant Physiol. 116:91-99
120. Liu H, Trieu AT, Blaylock LA, Harrison MJ. 1998. Cloning and characterization of two phosphate transporters from Medicago truncatula roots: regulation in response to phosphate and to colonization by arbuscular mycorrhizal (AM) fungi. Mol. Plant-Microbe Interact. 11:14-22
121. Lloyd-MacGilp SA, Chambers SM, Dodd JC, Fitter AH, Walker C, Yound JPW. 1996. Diversity of the ribosomal internal transcribed spacers within and among isolates of Glomus mosseae and related mycorrhizal fungi. New Phytol. 133:103-11
122. Longato S, Bonfante P. 1997. Molecular identification of mycorrhizal fungi by direct amplification of microsatellite regions. Mycol. Res. 101:425-32
123. Longman D, Callow JA. 1987. Specific saccharide residues are involved in the recognition of plant root surfaces by zoospores of Pythium aphanidermatum. Physiol. Mol. Plant Pathol. 30:139-50
124. Manners JM, Gay JL. 1983. The hostparasite interface and nutrient transfer in biotrophic parasitism. In Biochemical Plant Pathology, ed. JA Callow, pp. 163-68. Chichester, UK: Wiley
125. Marre E. 1979. Fusicoccin: a tool in plant physiology. Annu. Rev. Plant Physiol. 30:273-88
126. Marrs KA, Alfenito MR, Lloyd AM, Walbot V. 1995. A glutathione Stransferase involved in vacuolar transfer encoded by the maize gene Bronze-2. Nature 375:397-400
127. Martin-Laurent F, van Tuinen D, Dumas-Gaudot E, Gianinazzi-Pearson V, Gianinazzi S, Franken P. 1997. Differential display analysis of RNA accumulation in arbuscular mycorrhiza of pea and isolation of a novel symbiosisregulated plant gene. Mol. Gen. Genet. 256:37-44
128. Martin-Laurent FA, Franken P, van Tuinen D, Dumas-Gaudot E, Schlichter U, et al. 1996. Differential display reverse transcription polymerase chain reaction: a new approach to detect symbiosisrelated genes involved in arbuscular mycorrhiza. See Ref. 9a, pp. 195-98
129. Mendgen K, Deising H. 1993. Tansley Review No. 48. Infection structures of fungal plant pathogens - a cytological and physiological evaluation. New Phytol. 124:193-213
130. Mendgen K, Hahn M, Deising H. 1996. Morphogenesis and mechanisms of penetration by plant pathogenic fungi. Annu. Rev. Phytopathol. 34:367-86
131. Morton JB, Benny GL. 1990. Revised classification of arbusular mycorrhizal fungi (zygomycetes): a new order, glomales, two new suborders, glomineae and gigasporineae, and two new families, acaulosporaceae and gigasporaceae, with an amendation of glomaceae. Mycotaxon 37:471-91
132. Mosse B, Hepper CM. 1975. Vesicular-arbuscular mycorrhizal infections in root organ cultures. Physiol. Plant Pathol. 5:215-23
133. Muchhal US, Pardo JM, Raghathama KG. 1996. Phosphate transporters from the higher plant Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 93:101519-23
134. Mugnier J, Mosse B. 1987. Vesicular-arbuscular mycorrhizal infection in transformed root-inducing T-DNA roots grown axenically. Phytopathology 77: 1045-50
135. Murphy PJ, Langridge P, Smith SE. 1997. Cloning plant genes differentially expressed during colonization of roots of Hordeum vulgare by the vesicular-arbuscular mycorrhizal fungus Glomus intraradices. New Phytol. 135:291-301
136. Nagahashi G, Douds DD Jr. 1997. Appressorium formation by AM fungi on isolated cell walls of carrot roots. New Phytol. 136:299-304
137. Nair MG, Safir GR, Siqueira JO. 1991. Isolation and identification of vesicular-arbuscular mycorrhiza stimulatory compounds from clover (Trifolium repens) roots. Appl. Environ. Microbiol. 57:434-39
138. Nehls U, Wiese J, Guttenberger M, Hampp R. 1998. Carbon allocation in ectomycorrhizas: identification and expression analysis of an Amanita muscaria monosaccharide transporter. Mol. Plant-Microbe Interact. 11:167-76
139. Olsson PA, Baath E, Jakobsen I. 1997. Phosphorus effects on the mycelium and storage structures of an arbuscular mycorrhizal fungus as studied in the soil and roots by analysis of fatty acid signatures. Appl. Environ. Microbiol. 63:3531-38
140. Patrick JW. 1989. Solute efflux from the host at plant-microorganism interfaces. Aust. J. Plant Physiol. 16:53-67
141. 33P. New Phytol. 124: 489-94
142. Peretto R, Bettini V, Favaron F, Alghisi P, Bonfante P. 1995. Polygalacturonase activity and location in arbuscular mycorrhizal roots of Allium porrum L. Mycorrhiza 3:157-63
143. Perfect SE, O'Connell RJ, Green EF, Doering-Saad C, Green JR. 1998. Expression cloning of a fungal proline-rich glycoprotein specific to the biotrophic interface formed in the Colletotrichumbean interaction. Plant J. 15:273-79
144. Perotto S, Brewin N, Bonfante P. 1994. Colonization of pea roots by the mycorrhizal fungus Glomus versiforme and by Rhizobium bacteria: immunological comparison using monoclonal antibodies as probes for plant cell surface components. Mol. Plant-Microbe Interact. 7:91-98
145. Perotto S, Vandenbosch KA, Brewin NJ, Faccio A, Knox JP, Bonfante-Fasolo P. 1990. Modifications of the host cell wall during root colonization by Rhizobium and VAM fungi. In Endocytobiology IV, ed. P Nardon, V Gianinazzi-Pearson, AM Grenier, M Margulis, DC Smith, pp. 114-17. Paris: INRA Press
146. Peterson RL, Bradbury SM. 1995. Use of plant mutants, intraspecific variants, and non-hosts in studying mycorrhiza formation and function. In Mycorrhiza: Structure, Function, Molecular Biology and Biotechnology, ed. A Varma, B Hock, pp. 157-80. Berlin: Springer-Verlag
147. Pirozynski KA, Malloch DW. 1975. The origin of land plants: a matter of mycotrophism. Biosystems 6:153-64
148. 2 enrichment. J. Chem. Ecol. 19:2317-27
149. Poulin M-J, Simard J, Catford J-G, Labrie F, Piché Y. 1997. Response of symbiotic endomycorrhizal fungi to estrogens and antiestrogens. Mol. PlantMicrobe Interact. 10:481-87
150. Pozo MJ, Dumas-Gaudot E, Slezack S, Cordier C, Asselin A, et al. 1996. Induction of new chitinase isoforms in tomato roots during interactions with Glomus mosseae and/or Phytopthora nicotianae va. parasitica. Agronomie 16:689-97
151. Rasmussen U, Johansson C, Renglin A, Peterson C, Bergman B. 1996. A moleular characterization of the GunneraNostoc symbiosis: comparison with Rhizobium- and Agrobacterium-plant interactions. New Phytol. 133:391-98
152. Deleted in proof
153. Redecker D, Thierfelder H, Walker C, Werner D. 1997. Restriction analysis of PCR-amplified internal transcribed spacers of ribosomal DNA as a tool for species identification in different genera of the order Glomales. Appl. Environ. Microbiol. 63:1756-61
154. Rejon-PalomaresA,Garcia-GarridoJM, Ocampo JA, Garcia-Romera I. 1996. Presence of xyloglucan-hydrolyzing glucanases (xylogucanases) in arbuscular mycorrhizal symbiosis. Symbiosis 21:249-61
155. Remy W, Taylor TN, Hass H, Kerp H. 1994. Four hundred-million-year-old vesicular arbuscular mycorrhizae. Proc. Natl. Acad. Sci. USA 91:11841-43
156. Rhlid RB, Chabot S, Piché Y, Chenevert R. 1993. Isolation and identification of flavonoids from Ri T-DNA-transformed roots (Daucus carota) and their significance in vesicular-arbuscular mycorrhiza. Phytochemistry 33:1369-71
157. Rosendahl S, Taylor JW. 1997. Development of multiple genetic markers for studies of genetic variation in arbuscular mycorrhizal fungi using AFLP. Mol. Ecol. 6:821-29
158. Roussel H, Brans S, Gianinazzi-Pearson V, Hahlbrock K, Franken P. 1997. Induction of a membrane intrinsic protein-encoding mRNA in arbuscular mycorrhiza and elicitor-stimulated cell suspension cultures of parsley. Plant Sci. 126:203-10
159. Sagan M, Morandi D, Tarenghi E, Duc G. 1995. Selection of nodulation and mycorrhizal mutants in the model plant Medicago truncatula (Gaertn.) after γ-ray mutagenesis. Plant Sci. 111:63-71
160. Salzer P, Hager A. 1991. Sucrose utilisation of the ectomycorrhizal fungi Amanita muscaria and Hebeloma crustuliniforme depends on the cell wall-bound invertase activity of their host Picea abies. Bot. Acta 104:439-45
161. Salzer P, Hübner B, Sirrenberg A, Hager A. 1997. Differential effect of purified spruce chitinases and β-1,3-glucanases on the activity of elicitors from ectomycorrhizal fungi. Plant Physiol. 114:957-68
162. Samra A, Dumas-Gaudot E, Gianinazzi-Pearson V, Gianinazzi S. 1997. Changes in polypeptide profiles of two pea genotypes inoculated with the arbuscular mycorrhizal fungus Glomus mosseae. See Ref. 9a, pp. 263-66
163. Sanders IR, Alt M, Grappe K, Boller T, Wiemken A. 1995. Identification of ribosomal DNA polymorphisms in spores of the Glomales: application to studies on the genetic diversity of arbuscular mycorrhizal fungal communities. New Phytol. 130:419-27
164. Sanders IR, Clapp JP, Wiemken A. 1996. The genetic diversity of arbuscular mycorrhizal fungi in natural ecosystems - a key to understanding the ecology and functioning of the mycorrhizal symbiosis. New Phytol. 133:123-34
165. Sauer N, Baier K, Gahrtz M, Stadler R, Stolz J,Truernit E. 1994. Sugar transport across the plasma membranes of higher plants. Plant Mol. Biol. 26:1671-79
166. Schellenbaum L, Gianniazzi S, Giannazzi-Pearson V. 1992. Comparison of acid soluble protein synthesis in roots of endomycorrhizal wild-type Pisum sativum and corresponding isogenic mutants. J. Plant Physiol. 141:2-6
167. Scheres B, van Engelen F, van der Knaap E, van de Wiel C, van Kammen A, Bisseling T. 1990. Sequential induction of nodulin gene expression in the developing pea nodule. Plant Cell 2:687-700
168. Schreiner RP, Koide RT. 1992. Antifungal compounds from the roots of mycotrophic and non-mycotrophic plant species. New Phytol. 123:99-105
169. Schreiner RP, Koide RT. 1993. Mustards, mustard oils and mycorrhizas. New Phytol. 123:107-13
170. Schwab SM, Menge JA, Tinker PB. 1991. Regulation of nutrient transfer between host and fungus in vesicular-arbuscular mycorrhizas. New Phytol. 117:387-98
171. Shachar-Hill Y, Pfeffer PE, Douds D, Osman SF, Doner LW, Ratcliffe RG. 1995. Partitioning of intermediary carbon metabolism in vesicular-arbuscular mycorrhizal leek. Plant Physiol. 108:2979-95
172. - Plant Sci. 118:209-20
173. Simon L. 1996. Phytogeny of the Glomales: deciphering the past to understand the present. New Phytol. 133:95-101
174. Simon L, Bousquet J, Lévesque RC, Lalonde M. 1993. Origin and diversification of endomycorrhizal fungi and cincidence with vascular land plants. Nature 363:67-69
175. Simon L, Lalonde M, Bruns TD. 1992. Specific amplification of 18S fungal ribosomal genes from vesicular-arbuscular endomycorrhizal fungi colonizing roots. Appl. Environ. Microbiol. 58:291-95
176. Siqueira JO, Safir GR, Nair MG. 1991. Stimulation of vesicular-arbuscular mycorrhiza formation and growth of white clover by flavonoid compounds. New Phytol. 118:87-93
177. Smith FA, Smith SE. 1989. Membrane transport at the biotrophic interface: an overview. Aust. J. Plant Physiol. 16:33-43
178. Smith FA, Smith SE. 1997. Structural diversity in (vesicular)-arbuscular mycorrhizal symbioses. New Phytol. 137:373-88
179. Smith FW, Ealing PM, Dong B, Delhaize E. 1997. The cloning of two Arabidopsis genes belonging to a phosphate transporter family. Plant J. 11:83-92
180. Smith SE. 1993. Transport at the mycorrhizal interface. Mycorrhiza News 5:1-3
181. Smith SE, Dickson S, Morris C, Smith FA. 1994. Transfer of phosphate from fungus to plant in VA mycorrhizas: calculation of the area of symbiotic interface and of fluxes of P from two different fungi to Allium porrum L. New Phytol. 127:93-99
182. Smith SE, Gianinazzi-Pearson V. 1988. Physiological interactions between symbionts in vesicular-arbuscular mycorrhizal plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 39:221-44
183. Smith SE, Gianinazzi-Pearson V, Koide R, Cairney JWG. 1994. Nutrient transport in mycorrhizas: structure, physiology and consequences for efficiency of the symbiosis. Plant Soil 159:103-13
184. Smith SE, Read DJ, eds. 1997. Mycorrhizal Symbiosis. San Diego, CA: Academic
185. Smith SE, Smith FA. 1990. Structure and function of the interfaces in biotrophic symbioses as they relate to nutrient transport. New Phytol. 114:1-38
186. Solaiman MDZ, Saito M. 1997. Use of sugars by intraradical hyphae of arbuscular mycorrhizal fungi revealed by radiorespirometry. New Phytol. 136:533-38
187. Spanu P, Boller T, Ludwig A, Wiemken A, Faccio A, Bonfante-Fasolo P. 1989. Chitinase in roots of mycorrhizal Allium porrum: regulation and localization. Planta 177:477-55
188. Spanu P, Bonfante-Fasolo P. 1988. Cell-wall-bound peroxidase activity in roots of mycorrhizal Allium porrum. New Phytol. 109:119-24
189. St-Arnaud M, Hamel C, Vimard B, Caron M, Fortin JA. 1996. Enhanced hyphal growth and spore production of the arbuscular mycorrhizal fungus Glomus intraradices in an in vitro system in the absence of host roots. Mycol. Res. 100:328-32
190. Strittmatter G, Gheysen G, Gianinazzi-Pearson V, Hahn K, Niebel A, et al. 1996. Infections with various types of organisms stimulate transcription from a short promoter fragment of the potato gstl gene. Mol. Plant-Microbe Interact. 9:68-73
191. Tahiri-Aloui A, Antoniw JF. 1996. Cloning of genes associated with the colonization of tomato roots by the arbuscular mycorrhizal fungus Glomus mosseae. Agronomie 16:699-707
192. Tester M, Smith SE, Smith FA. 1987. The phenomenon of "nonmycorrhizal" plants. Can. J. Bot. 65:419-31
193. Thomson BD, Clarkson DT, Brain P. 1990. Kinetics of phosphorus uptake by the germ-tubes of the vesicular-arbuscular mycorrhizal fungus, Gigaspora margarita. New Phytol. 116:647-53
194. Trappe JM. 1987. In Ecophysiology of VA Mycorrhizal Plants, ed. GR Safir, pp. 5-25. Boca Raton, FL: CRC Press
195. Tsai SM, Phillips DA. 1991. Flavonoids released naturally from alfalfa promote development of symbiotic Glomus spores in vitro. Appl. Environ. Microbiol. 57:1485-88
196. van Buuren ML, Lanfranco L, Longato S, Minerdi D, Harrison MJ, Bonfante P. 1998. Construction and characterisation of genomic libraries of two endomycorrhizal fungi: Glomus versiforme and Gigaspora margarita. Fungal Genet. Biol. In press
197. van Buuren ML, Maldonado-Mendoza IE, Trieu AT, Blaylock LA, Harrison MJ. 1998. Novel genes induced during an arbuscular mycorrhizal (AM) symbiosis between M. truncatula and G. versiforme. Mol. Plant Microbe Interact. In press
198. van Rhijn P, Fang Y, Galili S, Shaul O, Atzmon N, et al. 1997. Expression of early nodulin genes in alfalfa mycorrhizae indicates that signal transduction pathways used in forming arbuscular mycorrhizae and Rhizobium-induced nodules may be conserved. Proc. Natl. Acad. Sci. USA 94:5467-72
199. van Tuinen D, Jaquot E, Zhao B, Gollotte A, Gianinazzi-Pearson V. 1998. Characterization of root colonization profiles by a microcosm community of arbuscular mycorrhizal fungi using 25S rDNA-targeted nested PCR. Mol. Ecol. 7:879-87
200. Vierheilig H, Alt M, Lange J, Gut-Rella M, Wiemken A, Boller T. 1995. Colonization of transgenic tobacco constitutively expressing pathogenesis-related proteins by the vesicular-arbuscular mycorrhizal fungus Glomus mosseae. Appl. Environ. Microbiol. 61:3031-34
201. Vierheilig H, Alt M, Mohr U, Boller T, Wiemken A. 1994. Ethylene biosynthesis and activities of chitinase and β-1,3-glucanase in the roots of host and non-host plants of vesicular-arbuscular mycorrhizal fungi after inoculation with Glomus mosseae. J. Plant Pkysiol. 143: 337-43
202. Vierheilig H, Alt M, Neuhaus JM, Boller T, Wiemken A. 1993. Colonization of transgenic Nicotiana silvestris plants, expressing different forms of Nicotiana tabacum chitinase, by the root pathogen Rhizoctonia solani and by the mycorrhizal symbiont Glomus mosseae. Mol. Plant-Microbe Interact. 6:261-64
203. Vierheilig H, Iseli B, Alt M, Raikhel N, Wiemken A, Boller T. 1996. Resistance of Urtica dioica to mycorrhizal colonization: a possible involvement of Urtica dioica agglutinin. Plant Soil 183:131-36
204. -) show the same colonization characteris-tics as ungrafted plants. J. Plant Physiol. 147:762-64
205. Volpin H, Elkind Y, Okon Y, Kapulnik Y. 1994. A vesicular arbuscular mycorrhizal fungus Glomus intraradix induces a defence response in alfalfa roots. Plant Physiol. 104:683-89
206. Volpin H, Phillips DA, Okon Y, Kapulnik Y. 1995. Suppression of an isoflavonoid phytoalexin defense response in mycorrhizal alfalfa roots. Plant Physiol. 108:1449-54
207. Wegel E, Schauser L, Sandal N, Stougaard J, Parniske M. 1998. Mycorrhiza mutants of Lotus japonicus define genetically independent steps during symbiotic infection. Mol. Plant-Microbe Interact. 11:933-36
208. Wright SF, Franke-Snyder M, Morton JB, Upadhyaya A. 1996. Time-course study and partial characterization of a protein on hyphae of arbuscular mycorrhizal fungi during active colonization of roots. Plant Soil 181:193-203
209. Wright SF, Upadhyaya A. 1996. Extraction of an abundant and unusual protein from soil and comparison with hyphal protein of arbuscular mycorrhizal fungi. Soil Sci. 161:575-86
210. Wyss P, Bonfante P. 1993. Amplification of genomic DNA of arbuscularmycorrhizal (AM) fungi by PCR using short arbitrary primers. Mycol. Res. 97:1351-57
211. Xie Z-P, Staehelin C, Vierheilig H, Wiemken A, Jabbouri S, et al. 1995.Rhizobial nodulation factors stimulate mycorrhizal colonization of nodulating and nonnodulating soybeans. Plant Physiol. 108:1519-25
212. Zézé A, Dulieu H, Gianinazzi-Pearson V. 1994. DNA cloning and screening of a partial genomic library from an arbuscular mycorrhizal fungus. Mycorrhiza 4:251-54
213. Zézé A, Hosny M, Gianinazzi-Pearson V, Dulieu H. 1996. Characterization of a highly repeated DNA sequence (SC1) from the arbuscular mycorrhizal fungus Scutellospora castanea and its detection in planta. Appl. Environ. Microbiol. 62:2443-48
214. Zézé A, Sulistyowati E, Ophel-Keller K, Barker S, Smith S. 1997. Intersporal genetic variation of Gigaspora margarita, a vesicular arbuscular mycorrhizal fungus, revealed by M13 minisatelliteprimed PCR. Appl. Environ. Microbiol. 63:676-78