Identification of mycorrhiza-regulated genes with arbuscule development-related expression profile

Plant Molecular Biology

Volumn 55, Issue 4, 2004, Pages 553-566

  Grunwald, Ulf ^a   Nyamsuren, Oyunbileg ^b   Tamasloukht, M'Barek ^c   Lapopin, Laurence ^d   Becker, Anke ^e   Mann, Petra ^a   Gianinazzi Pearson, Vivienne ^f   Krajinski, Franziska ^b   Franken, Philipp ^g  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b LEIBNIZ UNIVERSITY HANNOVER   (Germany)

^c ETH ZURICH   (Switzerland)

^d ROCHE DIAGNOSTICS GMBH   (Germany)

^e BIELEFELD UNIVERSITY   (Germany)

^f UNIVERSITÉ DE BOURGOGNE   (France)

^g LEIBNIZ INSTITUTE OF VEGETABLE AND ORNAMENTAL CROPS   (Germany)

Author keywords

Arbuscular mycorrhiza; Medicago truncatula; Pisum sativum; Suppressive subtractive hybridisation; Trypsin inhibitor

Indexed keywords

CLONING; DNA; FUNGI; GENES; MUTAGENESIS; RNA;

CDNA; GENE EXPRESSION; MACRO-ARRAYS; TRYPSIN INHIBITORS;

PLANTS (BOTANY);

CLONES; FUNGI; GENES; MUTATION; MYCORRHIZA; NUCLEIC ACIDS; PLANTS;

ARBUSCULAR MYCORRHIZAE; FUNGI; GLOMUS MOSSEAE; MEDICAGO; MEDICAGO TRUNCATULA; PISUM SATIVUM; SATIVUM;

PLANT RNA;

ARTICLE; BARREL MEDIC; COMPARATIVE STUDY; EXPRESSED SEQUENCE TAG; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; MYCORRHIZA; PEA; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

EXPRESSED SEQUENCE TAGS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; MEDICAGO TRUNCATULA; MYCORRHIZAE; PEAS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, PLANT;

EID: 16644403234     PISSN: 01674412     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11103-004-1303-y     Document Type: Article

References (86)

1. Altschul, S.F., Gish, W., Miller, W., Myers E.W. and Lipman, D.J. 1990. Basic local alignment search tool. J. Mol. Biol. 215: 403-410.
2. Alexander, T., Meier, R., Toth, R. and Weber, H.C. 1988. Dynamics of arbuscule development and degeneration in mycorrhizas of Triticum aestivum L. and Avena sativa L. with reference to Zea mays L. New Phytol. 110: 363-370.
3. Balestrini, R., Jose-Estanyol, M., Puigdomenech, P. and 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.
4. Bauer, D., Müller, H., Reich, J., Riedel, H., Ahrenkiel, V., Warthoe, P. and Strauss, M. 1993. Identification of differentially expressed mRNA species by an improved display technique (DDRT-PCR). Nucl. Acids Res. 21: 4272-4280.
5. Berta, G., Tagliasacchi, A.M., Fusconi, A., Gerlero, D., Trotta, A. and Scannerini, S. 1991. The mitotic-cycle in root apical meristems of Allium-porrum 1 is controlled by the endomycorrhizal fungus Glomus sp strain e3. Protoplasma 161: 12-16.
6. Blee, E. 1998. Biosynthesis of phytooxylipins - the peroxygenase pathway. Lipid 100: 121-127.
7. Blee, K.A. and Andersen, A.J. 1996. Defense-related transcript accumulation in Phaseolus vulgaris L. colonized by the arbuscular mycorrhizal fungus Glomus intraradices Schenck & Smith. Plant Physiol. 110: 675-688.
8. Blee, K.A. and Anderson, A.J. 1998. Regulation of arbuscule formation by carbon in the plant. Plant J. 16: 523-530.
9. Blee, K.A. and Anderson, A.J. 2000. Defense responses in plants to arbuscular mycorrhizal fungi. In: G. Podila (Ed.), Current Advances in Mycorrhizal Research, American Phytopathology Society, St. Paul, pp. 27-44.
10. Blee, K.A. and Anderson, A.J. 2002. Transcripts for genes encoding soluble acid invertase and sucrose synthase accumulate in root tip and cortical cells containing mycorrhizal arbuscules. Plant Mol. Biol. 50: 197-211.
11. Boisson-Dernier, A., Chabaud, M., Garcia, F., Becard, G., Rosenberg, C. and Barker, D.G. 2001. Agrobacterium rhizogenes-transformed roots of Medicago truncatula for the study of nitrogen-fixing and endomycorrhizal symbiotic associations. Mol. Plant-Microbe. Interact. 14: 695-700.
12. Bonanomi, A., Wiemken, A., Boller, T. and Salzer P. 2001. Local induction of a mycorrhiza-specific class III chitinase gene in cortical root cells of Medicago truncatula containing developing or mature arbuscules. Plant Biol. 3: 194-199.
13. Bonfante, P., Bergero, R., Uribe, X., Romera, C., Rigau, J. and Puigdomenech, P. 1996. Transcriptional activation of a maize α-tubulin gene in mycorrhizal maize and transgenic tobacco plants. Plant J. 9: 737-743.
14. Bonfante, P. and Perotto, S. 1995. Transley review No. 82: strategies of arbuscular mycorrhizal fungi when infecting host plants. New Phytol. 130: 3-21.
15. Bonfante-Fasolo, P., Tamagnone, L., Perotto, R., Esquerré- Tugayé, M.T., Mazau, D., Mosiniak, M. and Vian, B. 1991. Immunocytochemical location of hydroxyproline-rich glycoproteins at the interface between a mycorrhizal fungus and its host plant. Protoplasma 165: 127-138.
16. Brechenmacher, L., Weidmann, S., van Tuinen, D., Chatagnier, O., Gianinazzi, S., Franken, P. and Gianinazzi-Pearson, V. 2004. Expression profiling of up-regulated plant and fungal genes in early and late stages of Medicago truncatula-Glomus mosseae interactions. Mycorrhiza: in press.
17. Butt, A., Mousley, C., Morris, K., Beynon, J., Can, C., Holub, E., Greenberg, J.T. and Buchanan-Wollaston, V. 1998. Differential expression of a senescence-enhanced metallothionein gene in Arabidopsis in response to isolates of Peronospora parasitica and Pseudomonas syringae. Plant J. 16: 209-221.
18. + and cloning of differentially expressed cDNA of a mutant in Arabidopsis thaliana. P. Natl. Acad. Sci. USA. 13: 271-275.
19. Chiang, C.C. and Hadwiger, L.A. 1991. The Fusarium solani-induced expression of a pea gene family encoding high cysteine content proteins. Mol. Plant-Microbe. Interact. 4: 324-331.
20. Danneberg, G., Latus, C., Zimmer, W., Hundeshagen, B., Schneider-Poetsch H.J. and Bothe, H. 1993. Influence of vesicular-arbuscular mycorrhiza on phytohormone balances in maize (Zea mays L.). J. Plant. Physiol. 141: 33-39.
21. Dellaporta, S.L., Wood, J. and Hicks, J.B. 1983. Maize DNA minipreps. Maize Genet. Coop. News Let. 57: 26.
22. Delp, G., Smith, S.E. and Barker, S.J. 2000. Isolation by differential display of three partial cDNAs potentially coding for proteins from the VA mycorrhizal fungus Glomus intraradices. Mycol. Res. 104: 293-300.
23. De Vries, S.C., Springer, J. and Wessels, J.G.H. 1982. Diversity of abundant mRNA sequences and patterns of protein synthesis in etiolated and greened pea seedlings. Planta 156: 129-135.
24. Dickson. S. and Smith S.E. 2001. Cross walls in arbuscular trunk hyphae form after loss of metabolic activity. New Phytol. 151: 735-742.
25. Doll J., Hause B., Demchenko K., Pawlowski, K. and Krajinski, F. 2003. A member of the germin-like protein family is a highly conserved mycorrhiza-specific induced gene. Plant Cell Physiol. 44: 1208-1214.
26. Dumas-Gaudot, E., Asselin, A., Gianinazzi-Pearson, V., Gollotte, A. and Gianinazzi, S. 1994. Chitinase isoforms in roots of various pea genotypes infected with arbuscular mycorrhizal fungi. Plant Sci. 99: 27-37.
27. Engvild, K.C. 1987. Nodulation and nitrogen fixation mutants of pea, Pisum sativum L. Theoret. Appl. Genet. 74: 711-713.
28. Evans, K.M., Gatehouse, J.A., Lindsay, W.P., Shi, J., Tommey, A.M. and Robinson, N.J. 1992. Expression of the pea metallothionein-like gene Psmta in Escherichia coli and Arabidopsis thaliana and analysis of trace metal ion accumulation: implications for PsMTA function. Plant Mol. Biol. 20: 1019-28.
29. +-ATPase gene expression in tomato plants. J Exp Bot 53: 1683-1687.
30. Fester, T., Strack, D. and Hause, B. 2001. Reorganization of tobacco root plastids during arbuscule development. Planta 213: 864-868.
31. Franken, P., Requena, N., Bütehorn, B., Krajinski, F., Kuhn, G., Lapopin, L., Mann, P., Rhody, D., and Stommel, M. 2000. Molecular analysis of the arbuscular mycorrhiza symbiosis. Arch. Agron. Soil. Sci. 45: 271-286.
32. Genre, A. and Bonfante, P. 1997. A mycorrhizal fungus changes microtubule orientation in tobacco root cells. Protoplasma 199: 30-38.
33. Genre, A. and Bonfante, P. 1998. Actin versus tubulin configuration in arbuscule-containing cells from mycorrhizal tobacco roots. New Phytol. 140: 745-752.
34. Genre, A. and Bonfante, P. 2002. Epidermal cells of a symbiosis-defective mutant of Lotus japonicus show altered cytoskeleton organisation in the presence of a mycorrhizal fungus. Protoplasma 219: 43-50.
35. Gianinazzi-Pearson, V. 1996. Plant cell response to arbuscular mycorrhizal fungi: getting to the roots of the symbiosis. Plant Cell 8: 1871-1883.
36. +-ATPase genes by an arbuscular mycorrhizal fungus in root cells of transgenic tobacco. Planta 211: 609-613.
37. Gianinazzi-Pearson, V., Brechenmacher, L., Weidmann, S., Sanchez, L., Gianinazzi, S. and van Tuinen, D. 2004. Molecular dialogue in arbuscular mycorrhiza: getting to the symbiotic cell programme. Mol. Plant-Microbe Interact. in press.
38. +-ATPase a component of ATP-hydrolysing enzyme activities in plant-fungus interfaces? New Phytol. 117: 61-74.
39. Gianinazzi-Pearson, V., Tahiri-Alaoui, A., Antoniw, J.F., Gianinazzi, S. and Dumas-Gaudot, E. 1992. Weak expression of the pathogenesis related PR-b1 gene and localization of related proteins during symbiotic endomycorrhizal interaction in tobacco roots. Endocytosis Cell Res. 8: 177-185.
40. Giovannetti, M., Sbrana, C. and Logi, C. 1994. Early processes involved in host recognition by arbuscular mycorrhizal fungi. New Phytol. 127:703-709.
41. Giritch, A., Herbik, A., Balzer, H.J., Ganal, M., Stephan, U.W. and Baumlein, H. 1997. A root-specific iron-regulated gene of tomato encodes a lysyl-tRNA-synthetase-like protein. Eur. J. Biochem. 244: 310-317.
42. Gish, W. and States, D.J. 1993. Identification of protein coding regions by database similarity search. Nature Genet. 3: 266-272.
43. Giudici, A. M., Regente, M. C. and de la Canal, L. 2000. A potent antifungal protein from Helianthus annuus flowers is a trypsin inhibitor. Plant Physiol. Biochem. 38: 881-888.
44. Gollotte, A., Gianinazzi-Pearson, V. and Gianinazzi, S. 1995. Immunodetection of infection thread glycoprotein and arabinogalactan protein in wild type Pisum sativum (L.) or an isogenic mycorrhiza-resistant mutant interacting with Glomus mosseae. Symbiosis 18: 69-85.
45. Harrison, M.J. and Dixon, R.A. 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.
46. Harrison, M.J., Dewbre, G.R. and Liu, J.Y. 2002. A phosphate transporter from Medicago truncatula involved in the acquisiton of phosphate released by arbuscular mycorrhizal fungi. Plant Cell 14: 2413-2429.
47. Hause, B. Maier, W. Miersch, O. Kramell, R. and Strack, D. 2002. Induction of jasmonate biosynthesis in arbuscular mycorrhizal barley roots. Plant Physiol. 130: 1213-1220.
48. Jacquelinet-Jeanmougin, J., Gianinazzi-Pearson , V. and Gianinazzi, S. 1987. Endomycorrhizas in the Gentianaceae II. Ultrastructural aspects of symbiont relationships in Gentiana lutea L. Symbiosis 3: 269-286.
49. Jonak, C., Pay, A., Bogre, L., Hirt, H. and Heberle-Bors, E. 1993. The plant homologue of MAP kinase is expressed in a cell cycle-dependent and organ-specific manner. Plant J 3: 611-617.
50. Journet, E.P., van Tuinen, D., Gouzy, J., Crespeau, H., Carreau, V., Farmer, M.J., Niebel, A., Schiex, T., Jaillon, O., Chatagnier, O., Godiard, L., Micheli, F., Kahn, D., Gianinazzi-Pearson, V. and Gamas, P. 2002. Exploring root symbiotic programs in the model legume Medicago truncatula using EST analysis. Nucleic Acids Res. 30: 5579-5592.
51. Journet, E.P., El-Gachtouli, N., Vernoud, V., de Billy, F., Pichon, M., Dedieu, A., Arnould, C., Morandi, D., Barker, D.G. and Gianinazzi-Pearson, V. 2001. Medicago truncatula ENOD11: A novel RPRP-encoding early nodulin gene expressed during mycorrhization in arbuscule-containing cells. Mol. Plant-Microbe. Interact. 14: 737-748.
52. Koka, C.V., Cerny, R.E., Gardner, R.G., Noguchi, T., Fujioka, S., Takatsuto, S., Yoshida. S. and Clouse, S.D. 2000. A putative role for the tomato genes DUMPY and CURL-3 in brassinosteroid biosynthesis and response. Plant Physiol. 122: 85-98.
53. Krajinski, F., Biela, A., Schubert, D., Gianinazzi-Pearson, V., Kaldenhoff, R. and Franken, P. 2000. Arbuscular mycorrhiza development regulates the mRNA abundance of Mtaqp1 encoding a mercury-insensitive aquaporin of Medicago truncatula. Planta 211: 85-90.
54. +-ATPase gene from Medicago truncatula, shows arbuscule-specific induced expression in mycorrhizal tissue. Plant Biol. 4: 754-761 NOV 2002
55. Lapopin, L., Gianinazzi-Pearson, V. and Franken, P. 1999. Comparative differential display analysis of arbuscular mycorrhiza in Pisum sativum and a mutant defective in late stage development. Plant Mol. Biol. 41: 669-677.
56. Lebrun-Garcia, A., Quaked, F., Chilitz, A. and Pugin, A. 1998. Activation of MAPK homologues by elicitors in tobacco cells. Plant J. 15: 773-781
57. Ligterink, W., Kroj, T., zur Nieden, U., Hirt, H. and Scheel, D. 1997. Receptor-mediated activation of a MAP kinase in pathogen defense of plants. Science 276: 2054-2057.
58. Liu, J.Y., Blaylock, L.A., Endre, G., Cho, J., Town, C.D., VandenBosch, K.A. and Harrison, M.J. 2003. Transcript profiling coupled with spatial expression analyses reveals genes involved in distinct developmental stages of an arbuscular mycorrhizal symbiosis. Plant Cell 15: 2106-2123.
59. Newman, E.I. and Reddell, P. 1987. The distribution of mycorrhizas among families of vascular plants. New Phytol. 106: 745-751.
60. Paszkowski, U., Kroken, S., Roux, C. and Briggs, S.P. 2002. Rice phosphate transporters include an evolutionarily divergent gene specifically activated in arbuscular mycorrhizal symbiosis. P Natl. Acad. Sci. USA. 99 : 13324-13329.
61. Quandt, H.J., Puhler, A. and Broer, I. 1993. Transgenic root-nodules of Vicia hirsuta - a fast and efficient system for the study of gene-expression in indeterminate-type nodules. Mol. Plant-Microbe Interact. 6: 699-706.
62. Rathbun, E.A., Naldrett, M.J. and Brewin, N.J. 2002. Identification of a family of extensin-like glycoproteins in the lumen of Rhizobium-induced infection threads in pea root nodules. Mol. Plant-Microbe Interact. 15: 350-359.
63. Rausch, C., Daram, P., Brunner, S., Jansa, J., Laloi, M., Leggewie, G., Amrhein, N. and Bucher, M. 2001. A phosphate transporter expressed in arbuscule-containing cells in potato. Nature 414: 462-466.
64. Read, D.J., Lewis, D.H., Fitter, A.H. and Alexander, I.J. 1992. Mycorrhizas in Ecosystems. CAB International, Oxford.
65. Requena, N., Fueller, P. and Franken, P. 1999. Molecular characterisation of GmFOX2, an evolutionary highly conserved gene from the mycorrhizal fungus Glomus mosseae, down-regulated during interaction with rhizobacteria. Mol. Plant-Microbe Interact. 12: 934-942.
66. Requena, N., Mann, P., Hampp, R. and Franken, P. 2002. Early developmentally 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.
67. Rosewarne, G.M., Barker, S.J., Smith, S.E., Smith, F.A. and Schachtman, D.P. 1999. A Lycopersicon esculentum phosphate transporter (LePT1) involved in phosphorus uptake from a vesicular-arbuscular mycorrhizal fungus. New Phytol. 144 (3): 507-516.
68. Ruiz-Lozano, J.M., Roussel, H., Gianinazzi, S. and Gianinazzi-Pearson, V. 1999. Defense genes are differentially induced by a mycorrhizal fungus and Rhizobium sp in wild-type and symbiosis-defective pea genotypes. Mol Plant-Microbe Interact 12: 976-984.
69. Salzer, P., Corbiere, H. and Boller, T. 1999. Hydrogen peroxide accumulation in Medicago truncatula roots colonized by the arbuscular mycorrhiza-forming fungus Glomus intraradices. Planta 208: 319-325.
70. Salzer, P., Bonanomi, A., Beyer, K., Vögeli-Lange, R., Aeschbacher, R.A., Lange, J., Wiemken, A., Kim, D., Cook, D.R. and Boller, T. 2000. Differential expression of eight chitinase genes in Medicago truncatula roots during mycorrhiza formation, nodulation, and pathogen infection. Mol. Plant-Microbe Interact. 13: 763-777.
71. Sambrook, J., Fritsch, E.F. and Maniatis, T. 1989. Molecular Cloning. A Laboratory Manual. Cold Spring Harbor Press, Cold Spring Harbor.
72. Schoenbeck, M.A., Samac, D.A., Fedorova, M., Gregerson, R.G., Gantt, J.S. and Vance, C.P. 1999. The alfalfa (Medicago sativa) TDY1 gene encodes a mitogen-activated protein kinase homolog. Mol. Plant-Microbe Interact. 12: 882-893.
73. Slezack, S., Dumas-Gaudot, E., Rosendahl, S., Kjoller, R., Paynot, M., Negrel, J. and Gianinazzi, S. 1999. Endoproteolytic activities in pea roots inoculated with the arbuscular mycorrhizal fungus Glomus mosseae and/or Aphanomyces euteiches in relation to bioprotection. New Phytol. 142: 517-529.
74. Slezack, S., Dumas-Gaudot, E., Paynot, M. and Gianinazzi, S. 2000. Is a fully established arbuscular mycorrhizal symbiosis required for bioprotection of Pisum sativum roots against Aphanomyces euteiches? Mol. Plant-Microbe Interact. 13: 238-241.
75. Smith, S.E., Gianinazzi-Pearson, V., Koide, R. and Cairney, J.W.G. 1993. Nutrient transport in mycorrhizas: structure, physiology and consequences for efficiency of the symbiosis. Plant Soil 159: 103-113.
76. Smith, F.A. and Smith, S.E. 1997. Tansley review no. 96: Structural diversity in (vesicular)-arbuscular mycorrhizal symbioses. New Phytol. 137: 373-388.
77. Stafstrom, J.P., Altschuler, M. and Anderson, D.H. 1993. Molecular cloning and expression of a MAP kinase homologue from pea. Plant Mol. Biol. 22: 83-90.
78. Staehelin, C., Charon, C., Boller, T., Crespi, M. and Kondorosi, A. 2001. Medicago truncatula plants overexpressing the early nodulin gene enod40 exhibit accelerated mycorrhizal colonization and enhanced formation of arbuscules. P Natl. Acad. Sci. USA. 98: 15366-15371.
79. Strittmatter, G., Gheysen, G., Gianinazzi-Pearson, V., Hahn, K., Niebel, A., Rohde, W. and Tacke, E. 1996. Infections with various types of organisms stimulate transcription from a short promoter fragment of the potato Gst1 gene. Mol. Plant-Microbe Interact. 9: 68-73.
80. Szabados, L., Charrier, B., Kondorosi, A., Debruijn, F.J. and Ratet, P. 1995. New plant promoter and enhancer testing vectors. Mol. Breed. 1: 419-423.
81. Tamasloukht, M., Sejalon-Delmas, N., Kluever, A., Jauneau, A., Roux, C., Bécard, G. and Franken, P. 2003. Root factors induce mitochondrial- related gene expression and fungal respiration during the developmental switch from asymbiosis to presymbiosis in the arbuscular mycorrhizal fungus Gigaspora rosea. Plant Physiol. 131: 1468-1478.
82. Timonen, S. and Peterson, R.L. 2002. Cytoskeleton in mycorrhizal symbiosis. Plant Soil 244: 199-210.
83. Toth, E.C., Vissi, E., Kovacs, I., Szoke, A., Arino, J., Gergely, P., Dudits, D. and Dombradi, V. 2000. Protein phosphatase 2A holoenzyme and its subunits from Medicago sativa. Plant Mol. Biol. 43: 527-536.
84. Trouvelot, A., Kough, J.L. and Gianinazzi-Pearson, V. 1986. Mesure du taux de mycorhization VA d'un système radiculaire. Recherche des méthodes d'estimation ayant une signification fonctionnelle. In: V. Gianinazzi-Pearson and S. Gianinazzi (Eds.), The Mycorrhizae : Physiology and Genetic, INRA Presse, Paris, pp. 217-221.
85. Van Buuren, M.L., Maldonado-Mendoza, I.E., Trieu, A.T., Blaylock, L.A. and Harrison, M.J. 1999. Novel genes induced during an arbuscular mycorrhizal (AM) symbiosis formed between Medicago truncatula and Glomus versiforme. Mol. Plant-Microbe Interact. 12: 171-181.
86. Wulf, A., Manthey, K., Doll, J., Perlick, A., Franken, P., Linke, B., Meyer, F., Küster, H. and Krajinski, F. 2003. Detection of highly specific transcriptional changes of the model plant Medicago truncatula in response to arbuscular mycorrhiza development. Mol. Plant-Microbe Interact. 16: 306-314.