Mutations in DMI3 and SUNN modify the appressorium-responsive root proteome in arbuscular mycorrhiza

Molecular Plant-Microbe Interactions

Volumn 19, Issue 9, 2006, Pages 988-997

  Amiour, Nardjis ^a   Recorbet, Ghislaine ^a   Robert, Franck ^a   Gianinazzi, Silvio ^a   Dumas Gaudot, Eliane ^a  

^a UNIVERSITÉ DE BOURGOGNE   (France)

Author keywords

Flavodoxin; GST; MtAnn1; Narbonin; Protease inhibitor

Indexed keywords

PROTEOME; VEGETABLE PROTEIN;

ARTICLE; BARREL MEDIC; GENE; GENETICS; GROWTH, DEVELOPMENT AND AGING; MASS SPECTROMETRY; METABOLISM; METHODOLOGY; MICROBIOLOGY; MUTATION; MYCORRHIZA; PHYSIOLOGY; PLANT ROOT; PROTEOMICS; SYMBIOSIS; TIME; TWO DIMENSIONAL GEL ELECTROPHORESIS;

ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; GENES, PLANT; MASS SPECTROMETRY; MEDICAGO TRUNCATULA; MUTATION; MYCORRHIZAE; PLANT PROTEINS; PLANT ROOTS; PROTEOME; PROTEOMICS; SYMBIOSIS; TIME FACTORS;

ARBUSCULAR; GLOMUS INTRARADICES; MEDICAGO TRUNCATULA;

EID: 33747478283     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-19-0988     Document Type: Article

References (65)

1. Akiyama, K., Matsuzaki, K., and Hayashi, H. 2005. Plant sesquiterpenes induce hypha1 branching in arbuscular mycorrhizal fungi. Nature 435:824-827.
2. Bestel-Corre, G., Dumas-Gaudot, E., Poinsot, V., Dieu, M., Dierick, J. F., van Tuinen, D., Remacle, J., Gianinazzi-Pearson, V., and Gianinazzi, S. 2002. Proteome analysis and identification of symbiosis-related proteins from Medicago truncatula Gaertn. by two-dimensional electrophoresis and mass spectrometry. Electrophoresis 23:122-137.
3. Blilou, I., Bueno, P., Ocampo, J. A., and GarciaGarrido, J. 2000. Induction of catalase and ascorbate peroxidase activities in tobacco roots inoculated with the arbuscular mycorrhizal Glomus mosseae. Mycol. Res. 104:722-725.
4. Blokhina, O., Virolainen, E., and Fagerstedt, K. V. 2003. Antioxidants, oxidative damage and oxygen deprivation stress: A review. Ann. Bot. 91:179-194.
5. Bonanomi, A., Oetiker, J. H., Guggenheim, R., Boller, T., Wiemken, A., and VogeliLange, R. 2001. Arbuscular mycorrhiza in mini-mycorrhizotrons: First contact of Medicago truncatula roots with Glomus intraradices induces chalcone synthase. New Phytol. 150:573-582.
6. 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 14:253-262.
7. Breuninger, M., and Requena, N. 2004. Recognition events in AM symbiosis: Analysis of fungal gene expression at the early appressorium stage. Fungal Genet. Biol. 41:794-804.
8. Calantzis, C., Morandi, D., Arnould, C., and Gianinazzi-Pearson, V. 2001. Cellular interactions between G. mosseae and a Myc(-) dmi2 mutant in Medicago truncatula. Symbiosis 30:97-108.
9. Carvalho-Niebel, F., Lescure, N., Cullimore, J. V., and Gamas, P. 1998. The Medicago truncatula MtAnnI gene encoding an annexin is induced by Nod factors and during the symbiotic interaction with Rhizobium meliloti. Mol. Plant-Microbe Interact. 11:504-513.
10. Carvalho-Niebel, F., Timmers, A. C. J., Chabaud, M., Defaux-Petras, A. and Barker, D. G., 2002. The Nod factor-elicited annexin MtAnn1 is preferentially localised at the nuclear periphery in symbiotically activated root tissues of Medicago truncatula. Plant J. 32:343-352.
11. Catford, J. G., Staehelin, C., Lerat, S., Piche, Y., and Vierheilig, H. 2003. Suppression of arbuscular mycorrhizal colonization and nodulation in split-root systems of alfalfa after pre-inoculation and treatment with Nod factors. J. Exp. Bot. 54:1481-1487.
12. Catoira, R., Galera, C., de Billy, F., Penmetsa, R. V., Journet, E. P., Maillet, F., Rosenberg, C., Cook, D., Gough, C., and Denarie, J. 2000. Four genes of Medicago truncatula controlling components of a nod factor transduction pathway. Plant Cell 12:1647-1665.
13. Ceccarelli, E. A., Arakaki, A. K., Cortez, N., and Carrillo, N. 2004. Functional plasticity and catalytic efficiency in plant and bacterial ferredoxin-NADP(H) reductases. Biochim. Biophys. Acta 1698:155-165.
14. Chou, I. T., and Gasser, C. S. 1997. Characterization of the cyclophilin gene family of Arabidopsis thaliana and phylogenetic analysis of known cyclophilin proteins. Plant Mol. Biol. 35:873-892.
15. Dixon, D. P., Davis, B. G., and Edwards, R. 2002. Functional divergence in the glutathione transferase superfamily in plants. Identification of two classes with putative functions in redox homeostasis in Arabidopsis thaliana. J. Biol. Chem. 277:30859-30869.
16. Dumas-Gaudot, E., Guillaume, P., Tahiri-Alaoui, A., Gianinazzi-Pearson, V., and Gianinazzi, S. 1994. Changes in polypeptide patterns in tobacco roots colonized by two Glomus species. Mycorrhiza 4:215-221.
17. Dumas-Gaudot, E., Valot, B., Bestel-Corre, G., Recorbet, G., St-Arnaud, M., Fontaine, B., Dieu, M., Raes, M., Saravanan, R. S., and Gianinazzi, S. 2004. Proteomics as a way to identify extra-radicular fungal proteins from Glomus intraradices-RiT-DNA carrot root mycorrhizas. FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Ecol. 48:401-411.
18. El Yahyaoui, F., Kuster, H., Ben Amor, B., Hohnjec, N., Puhler, A., Becker, A., Gouzy, J., Vernie, T., Gough, C., Niebel, A., Godiard, L., and Gamas, P. 2004. Expression profiling in Medicago truncatula identifies more than 750 genes differentially expressed during nodulation, including many potential regulators of the symbiotic program. Plant Physiol. 136:3159-3176.
19. Foyer, C. H., Theodoulou, F. L., and Delrot, S. 2001. The functions of inter- and intracellular glutathione transport systems in plants. Trends Plant Sci. 6:486-492.
20. Frosch, S. C., Becker, J. D., Schultze, M., Schlesier, B., Kahmann, U., Puhler, A., and Perlick, A. M. 2002. Characterization of NVO2: A narbonin-like nodulin of high abundance in Vicia faba L. Plant Sci. 162:401-411.
21. Frova, C. 2003. The plant glutathione transferase gene family: Genomic structure, functions, expression and evolution. Physiol. Plant 119:469-479.
22. Garcia-Garrido, J. M., and Ocampo, J. A. 2002. Regulation of the plant defence response in arbuscular mycorrhizal symbiosis. J. Exp. Bot. 53:1377-1386.
23. Genre, A., Chabaud, M., Timmers, T., Bonfante, P., and Barker, D.G. 2005. Arbuscular mycorrhizal fungi elicit a novel intacellular apparatus in Medicago root epidermal cells before infection. Plant Cell 17:3489-3799.
24. Gianinazzi-Pearson, V. 1996. Plant cell responses to arbuscular mycorrhizal fungi: Getting to the roots of the symbiosis. Plant Cell 8:1871-1883.
25. Giovannetti, M., Sbrana, C., Citernesi, A. S., and Avio, L. 1996. Analysis of factors involved in fungal recognition responses to host-derived signals by arbuscular mycorrhizal fungi. New Phytol. 133:65-71.
26. Godoy, A. V., Lazzaro, A. S., Casalongue, C. A., and San Segundo, B. 2000. Expression of a Solanum tuberosum cyclophilin gene is regulated by fungal infection and abiotic stress conditions. Plant Sci. 152:123-134.
27. Görg, A., Postel, W., Weser, J., Günther, S., Strahler, J. R., Hanash, S. M., and Somerlot, L. 1987. Elimination of point streaking on silver stained two-dimensional gels by addition of iodoacetamide to the equilibration buffer. Electrophoresis 8:122-124.
28. Grunwald, U., Nyamsuren, O., Tarnasloukht, M., Lapopin, L., Becker, A., Mann, P., Gianinazzi-Pearson, V., Krajinski, F., and Franken, P. 2004. Identification of mycorrhiza-regulated genes with arbuscule development-related expression profile. Plant Mol. Biol. 55:553-566.
29. Harborne, J. B. 1988. Flavonoids in the environment: Structure-activity relationships. Prog. Clin. Biol. Res. 280:17-27.
30. Harrison, M. J. 1999. Molecular and cellular aspects of the arbuscular mycorrhizal symbiosis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50:361-389.
31. Harrison, M. J., and Dixon, R. A. 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. 6:643-654.
32. Hennig, M., Pfeffer-Hennig, S., Dauter, Z., Wilson, K. S., Schlesier, B., and Nong, V. H. 1995. Crystal structure of narbonin at 1.8 A resolution. Acta Crystallogr. D Biol. Crystallogr. 51:177-89.
33. Journet, E. P., van Tuinen, D., Gouzy, J., Crespeau, H., Carreau, V., Farmer, M. J., Niebel, A., Chiex, T., Saillon, 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 trunctula using EST analysis. Nucleic Acids Res. 15:5579-5592.
34. Kong, H., Lee, S., and Hwang, B. 2001. Expression of pepper cyclophilin gene is differentially regulated during the pathogen infection and abiotic stress conditions. Physiol. Mol. Plant Pathol. 59:189-199.
35. Laskowski, M. J., Dreher, K. A., Gehring, M. A., Abel, S., Gensler, A. L., and Sussex, I. M. 2002. FQR1, a novel primary auxin-response gene, encodes a flavin mononucleotide-binding quinone reductase. Plant Physiol. 128:578-590.
36. 2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science 303:1361-1364.
37. Maciver, S., K., and Hussey, P. J. 2002. The ADF/cofilin family. Actin-remodeling proteins. Genome Biol. 3:1-12.
38. Marivet, J., Margis-Pinheiro, M., Frendo, P., and Burkard, G. 1994. Bean cyclophilin gene expression during plant development and stress conditions. Plant Mol. Biol. 26:1181-1189.
39. Marrs, K. A. 1996. The functions and regulation of glutathione 5-transferases in plants. Annu. Rev. Plant Physiol. Plant. Mol. Biol. 47:127-158.
40. Marsh, J. F., and Schultze, M. 2001. Analysis of arbuscular mycorrhizas using symbiosis-defective plant mutants. New Phytol. 150:525-532.
41. Mathesius, U., Keijzers, G., Natera, S. H., Weinman, J. J., Djordjevic, M. A., and Rolfe, B. G. 2001. Establishment of a root proteome reference map for the model legume Medicago truncatula using the expressed sequence tag database for peptide mass fingerprinting. Proteomics 11:1424-1440.
42. 2+/calmodulin-dependent protein kinase required for symbiotic nodule development: Gene identification by transcript-based cloning. Proc. Natl. Acad. Sci. USA 101:4701-4705.
43. Nagahashi, G., and Douds, D. D. 1997. Appressorium formation by AM fungi on isolated cell walls of carrot roots. New Phytol. 136:299-304.
44. Nuc, K., Nuc, P., and Slomski, R. 2001. Yellow lupine cyclophilin transcripts are highly accumulated in the nodule meristem zone. Mol. Plant-Microbe Interact. 14:1384-1394.
45. Oh, K., Ivanchenko, M. G., White, T. J., and Lomax, T. L. 2006. The diageotropica gene of tomato encodes a cyclophilin: A novel player in auxin signaling. Planta 4:1-12.
46. Perlick, A. M., Fruhling, M., Schroder, G., Frosch, S. C., and Puhler, A. 1996. The broad bean gene VfNOD32 encodes a nodulin with sequence similarities to chitinases that is homologous to (alpha/beta)(8)-barrel-type seed proteins. Plant Physiol. 110:147-154.
47. Phillips, J. M., and Hayman, D. S. 1970. Improved procedures for clearing and staining parasite and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans. Br. Mycol. Soc. 55:158-161.
48. Polya, G. 2001. Protease inhibitory plant defensive proteins. Curr. Topics Peptide Protein Res. 4:37-54.
49. Ramagli, L. S., and Rodriguez, L. W. 1985. Quantification of microgram amounts of protein in two-dimensional polyacrylamide gel electrophoresis sample buffer. Electrophoresis 6:559-563.
50. +-ATPase genes from the mycorrhizal fungus Glomus mosseae. Plant Physiol. 132:1540-1549.
51. Romano, P., Gray, J., Horton, P., and Luan, S. 2005. Plant immunophilins: Functional versatility beyond protein maturation. New Phytol. 166:752-769.
52. 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.
53. Sagan, M., Morandi, D., Tarenghi, E., and Due, G. 1995. Selection of nodulation and mycorrhizal mutants in the model plant Medicago truncatula (Gaertn.) after γ-ray mutagenesis. Plant Sci. 111:63-71.
54. Sanchez, L., Weidmann, S., Arnould, C., Bernard, A. R., Gianinazzi, S., and Gianinazzi-Pearson, V. 2005. Pseudomonas fluorescens and Glomus mosseae trigger DMI3-dependent activation of genes related to a signal transduction pathway in roots of Medicago truncatula. Plant Physiol. 139:1065-1077.
55. Schnabel, E., Journet, E.-P., de Carvalho-Niebel, F., Due, G., and Frugoli, J. 2005. The Medicago truncatula SUNN gene encodes a CLV1-like leucine-rich repeat receptor kinase that regulates nodule number and root length. Plant Mol. Biol. 58:809-822.
56. Smith, C. E., Ruttledge, T., Zeng, Z., O'Malley, R. C., and Lynn, D. G. 1996. A mechanism for inducing plant development: The genesis of a specific inhibitor. Proc. Natl. Acad. Sci. USA 93:6986-6991.
57. Smith, S. E., and Read, D. J. 1997. Genetic, cellular and molecular interactions in the establishment of VA mycorrhizas. Pages 81-104 in: Mycorrhizal Symbiosis. S. E. Smith and D. J. Read, eds. Academic Press, London.
58. Tucker, S. L., and Talbot, N. J. 2001. Surface attachment and pre-penetration stage development by plant pathogenic fungi. Annu. Rev. Phytopathol. 39:385-417.
59. Valot, V., Dumas-Gaudot, E., and Gianinazzi, S. 2004. Sub-cellular proteomic analysis of a Medicago truncatula root fraction. Phytochemistry 65:1721-1732.
60. Valueva, T. A., and Mosolov, V. V. 2004. Role of inhibitors of proteolytic enzymes in plant defense against phytopathogenic microorganisms. Biochemistry 69:1305-1309.
61. van Brussel, A. A., Tak, T., Boot, K. J., and Kijne, J. W. 2002. Autoregulation of root nodule formation: Signals of both symbiotic partners studied in a split-root system of Vicia sativa subsp. nigra. Mol. Plant-Microbe Interact. 15:341-349.
62. van Noorden, G. E., Ross, J. J., Reid, J. B., Rolfe, B. G., and Mathesius, U. 2006. Defective long distance signal auxin transport regulation in the Medicago truncatula sunn mutant. 2006. Plant Physiol. 140:1494-1506.
63. Vantard, M., and Blanchoin, L. 2002. Actin polymerization processes in plant cells. Curr. Opin. Plant Biol. 5:502-506.
64. Vierheilig, H. 2004. Regulatory mechanisms during the plant-arbuscular mycorrhizal fungus interaction. Can. J. Bot. 82:1166-1176.
65. Weidmann, S., Sanchez, L., Descombin, J., Chatagnier, O., Gianinazzi, S., and Gianinazzi-Pearson, V. 2004. Fungal elicitation of signal transduction-related plant genes precedes mycorrhiza establishment and requires the dmi3 gene in Medicago truncatula. Mol. Plant-Microbe Interact. 17:1385-1393.