Arbuscular mycorrhizal symbiosis is accompanied by local and systemic alterations in gene expression and an increase in disease resistance in the shoots

Plant Journal

Volumn 50, Issue 3, 2007, Pages 529-544

  Liu, Jinyuan ^a,c   Maldonado Mendoza, Ignacio ^b,c   Lopez Meyer, Melina ^b,c   Cheung, Foo ^d   Town, Christopher D ^d   Harrison, Maria J ^c  

^a Department of Obstetrics Gynecology   (United States)

^b INSTITUTO POLITÉCNICO NACIONAL   (Mexico)

^c United States Department of Agriculture Agricultural Research Service and Boyce Thompson Institute for Plant Research   (United States)

^d J CRAIG VENTER INSTITUTE   (United States)

Author keywords

Arbuscular mycorrhizal symbiosis; Defense response; Induced systemic resistance; Medicago truncatula; Microarray; Roots

Indexed keywords

DISEASES; FUNGI; GENE EXPRESSION; MICROARRAYS; NUTRITION; PHOSPHORUS;

ARBUSCULAR MYCORRHIZAL SYMBIOSIS; DEFENSE RESPONSES; INDUCED SYSTEMIC RESISTANCES; MEDICAGO TRUNCATULA;

ECOSYSTEMS;

ARTICLE; BARREL MEDIC; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; IMMUNOLOGY; INNATE IMMUNITY; METABOLISM; MICROBIOLOGY; MYCORRHIZA; PHYSIOLOGY; PLANT; PLANT DISEASE; PLANT ROOT; SYMBIOSIS; XANTHOMONAS CAMPESTRIS;

GENE EXPRESSION REGULATION, PLANT; IMMUNITY, NATURAL; MEDICAGO TRUNCATULA; MYCORRHIZAE; PLANT DISEASES; PLANT ROOTS; PLANT SHOOTS; SYMBIOSIS; TRANSCRIPTION, GENETIC; XANTHOMONAS CAMPESTRIS;

DISEASES; ECOSYSTEMS; FUNGI; NUTRITION; PHOSPHORUS; ROOTS;

ARBUSCULAR; BACTERIA (MICROORGANISMS); FUNGI; MEDICAGO TRUNCATULA; XANTHOMONAS CAMPESTRIS;

EID: 34247357385     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2007.03069.x     Document Type: Article

References (78)

1. Akkopru, A. Demir, S. (2005) Biological control of Fusarium wilt in tomato caused by Fusarium oxysporum f. sp. lycopersici by AMF Glomus intraradices and some rhizobacteria. J. Phytopathol. 153, 544 550.
2. Alexander, T., Meier, R., Toth, R. 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. Ames, B.N. (1966) Assay of inorganic phosphate, total phosphate and phosphatases. Methods Enzymol. 8, 115 118.
4. Ane, J.-M., Kiss, G.B., Riely, B.K. et al. (2004) Medicago truncatula DMI1 required for bacterial and fungal symbioses in legumes. Science, 303, 1364 1367.
5. Bécard, G. Fortin, J.A. (1988) Early events of vesicular-arbuscular mycorrhiza formation on Ri T-DNA transformed roots. New Phytol. 108, 211 218.
6. Berta, G., Sampo, S., Gamalero, E., Massa, N. Lemanceau, P. (2005) Suppression of Rhizoctonia root-rot of tomato by Glomus mossae BEG12 and Pseudomonas fluorescens A6RI is associated with their effect on the pathogen growth and on the root morphogenesis. Eur. J. Plant Pathol. 111, 279 288.
7. Bonfante-Fasolo, P. (1984) Anatomy and morphology of VA mycorrhizae. In VA Mycorrhizae (Powell, C.L. Bagyaraj, D.J., eds). Boca Raton, FL : CRC Press, pp. 5 33.
8. Bostock, R.M. (2005) Signal crosstalk and induced resistance: straddling the line between cost and benefit. Annu. Rev. Phytopathol. 43, 545 580.
9. Braunberger, P.G., Miller, M.H. Peterson, R.L. (1991) Effect of phosphorus nutrition on morphological characteristics of vesicular-arbuscular mycorrhizal colonization of maize. New Phytol. 119, 107 113.
10. Brechenmacher, L., Weidmann, S., van Tuinen, D., Chatagnier, O., Gianinazzi, S., Franken, P. 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.
11. Burleigh, S.H. Harrison, M.J. (1998) Mt4, a phosphorus starvation-inducible cDNA from Medicago truncatula, which is down-regulated both by phosphorus fertilization and arbuscular-mycorrhizal colonization. In Phosphorous in Plant Biology: Regulatory Roles in Molecular Cellular, Organismic, and Ecosystem Processes (Lynch, J.P. Deikman, J., eds). Rockville, MD : American Society of Plant Physiologists, pp. 359 360.
12. Cartieaux, F., Thibaud, M.C., Zimmerli, L., Lessard, P., Sarrobert, C., David, P., Gerbaud, A., Robaglia, C., Somerville, S. Nussaume, L. (2003) Transcriptome analysis of Arabidopsis colonized by a plant-growth promoting rhizobacterium reveals a general effect on disease resistance. Plant J. 36, 177 188.
13. Cordier, C., Pozo, M.J., Barea, J.M., Gianinazzi, S. Gianinazzi-Pearson, V. (1998) Cell defense responses associated with localized and systemic resistance to Phytophthora parasitica induced in tomato by an arbuscular mycorrhizal fungus. Mol. Plant Microbe Interact. 11, 1017 1028.
14. Corradi, N., Hijri, M., Fumagalli, L. Sanders, I.R. (2004) Arbuscular mycorrhizal fungi (Glomeromycota) harbour ancient fungal tubulin genes that resemble those of the chytrids (Chytridiomycota). Fung. Genet. Biol. 41, 1037 1045.
15. Durrant, W.E. Dong, X. (2004) Systemic acquired resistance. Annu. Rev. Phytopathol. 42, 185 209.
16. Durrant, W.E., Rowland, O., Piedras, P., Hammond-Kosack, K.E. Jones, J.D.G. (2000) cDNA-AFLP reveals a striking overlap in race-specific resistance and wound response gene expression profiles. Plant Cell, 12, 963 977.
17. Endre, G., Kereszt, A., Kevel, Z., Mihacea, S., Kaló, P. Kiss, G. (2002) A receptor kinase gene regulating symbiotic nodule development. Nature, 417, 962 966.
18. Frenzel, A., Manthey, K., Perlick, A.M., Meyer, F., Puhler, A., Kuster, H. Krajinski, F. (2005) Combined transcriptome profiling reveals a novel family of arbuscular mycorrhizal-specific Medicago truncatula lectin genes. Mol. Plant Microbe Interact. 18, 771 782.
19. Gamas, P., de Billy, F. Truchet, G. (1998) Symbiosis-specific expression of two Medicago truncatula nodulin genes, MtN1 and MtN13, encoding products homologous to plant defense proteins. Mol. Plant Microbe Interact. 11, 393 403.
20. Gianinazzi-Pearson, V. (1996) Plant cell responses to arbuscular myorrhiza fungi: getting to the roots of the symbiosis. Plant Cell, 8, 1871 1883.
21. Gianinazzi-Pearson, V., Arnould, C., Oufattole, M., Arango, M. Gianinazzi, S. (2000) Differential activation of H+-ATPase genes by an arbuscular mycorrhizal fungus in root cells of transgenic tobacco. Planta, 211, 609 613.
22. Glazebrook, J. (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu. Rev. Phytopathol. 43, 205 227.
23. Graham, J.H., Leonard, R.T. Menge, J.A. (1982) Interaction of light intensity and soil temperature with phosphorus inhibition of vesicular-arbuscular mycorrhiza formation. New Phytol. 91, 683 690.
24. Guimil, S., Chang, H.-S., Zhu, T. et al. (2005) Comparative transcriptomics of rice reveals an ancient pattern of response to microbial colonization. Proc. Natl Acad. Sci. USA, 102, 8066 8070.
25. Hagihara, T., Hashi, M., Takeuchi, Y. Yamaoka, N. (2004) Cloning of soybean genes induced during hypersensitive cell death caused by syringolide elicitor. Planta, 218, 606 614.
26. Hanks, J.N., Synder, A.K., Graham, M.A., Shah, R.K., Blaylock, L.A., Harrison, M.J. Shah, D.M. (2005) Defensin gene family in Medicago truncatula: structure, expression and induction by signal molecules. Plant Mol. Biol. 58, 385 399.
27. Harrison, M.J. (2005) Signaling in the arbuscular mycorrhizal symbiosis. Annu. Rev. Microbiol. 59, 19 42.
28. Harrison, M.J. 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.
29. Harrison, M.J. 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.
30. Harrison, M.J., Dewbre, G.R. Liu, J. (2002) A phosphate transporter from Medicago truncatula involved in the acquisition of phosphate released by arbuscular mycorrhizal fungi. Plant Cell, 14, 2413 2429.
31. Hohnjec, N., Vieweg, M.F., Puhler, A., Becker, A. Kuster, H. (2005) Overlaps in the transcriptional profiles of Medicago truncatula roots inoculated with two different Glomus fungi provide insights into the genetic program activated during arbuscular mycorrhiza. Plant Physiol. 137, 1283 1301.
32. Hohnjec, N., Henckel, K., Bekel, T., Gouzy, J., Dondrup, M., Goesmann, A. Kuster, H. (2006) Transcriptional snapshots provide insights into the molecular basis of arbuscular mycorrhiza in the model legume Medicago truncatula. Funct. Plant Biol. 33, 737 748.
33. Imaizumi-Anraku, H., Takeda, N., Charpentier, M. et al. (2005) Plastid proteins crucial for symbiotic fungal and bacterial entry into plant roots. Nature, 433, 527 531.
34. Ivashuta, S., Liu, J., Liu, J., Lohar, D.P., Haridas, S., Bucciarelli, B., VandenBosch, K.A., Vance, C.P., Harrison, M.J. Gantt, J.S. (2005) RNA interference identifies a calcium-dependent protein kinase involved in Medicago truncatula root development. Plant Cell, 17, 2911 2921.
35. Journet, E.P., van Tuinen, D., Gouzy, J. et al. (2002) Exploring root symbiotic programs in the model legume Medicago truncatula using EST analysis. Nucleic Acids Res. 30, 5579 5592.
36. Kanamori, N., Madsen, L.H., Radutoiu, S. et al. (2006) From The Cover: A nucleoporin is required fo induction of Ca2+ spiking in legume nodule development and essential for rhizobial and fungal symbiosis. PNAS, 103, 359 364.
37. Kuster, H., Hohnjec, N., Krajinski, F. et al. (2004) Construction and validation of cDNA-based Mt6k-RIT macro- and microarrays to explore root endosymbioses in the model legume Medicago truncatula. J. Biotechnol. 108, 95 113.
38. Levy, J., Bres, C., Geurts, R. et al. (2004) A putative Ca2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science, 303, 1361 1364.
39. Li, H.-Y., Yang, G.-D., Shu, H.-R., Yang, Y.-T., Ye, B.-X., Nishida, I. Zheng, C.-C. (2006) Colonization by the arbuscular mycorrhizal fungus Glomus versiforme induces a defense response against the root-knot nematode Meloidogyne incognita in the grapevine (Vitis amurensis Rupr.), which includes transcriptional activation of the class III chitinase gene VCH3. Plant Cell Physiol. 47, 154 163.
40. Liu, J., Blaylock, L., Endre, G., Cho, J., Town, C.D., VandenBosch, K. Harrison, M.J. (2003) Transcript profiling coupled with spatial expression analyses reveals genes involved in distinct developmental stages of the arbuscular mycorrhizal symbiosis. Plant Cell, 15, 2106 2123.
41. Liu, J., Blaylock, L. Harrison, M.J. (2004) cDNA arrays as tools to identify mycorrhiza-regulated genes: identification of mycorrhiza-induced genes that encode or generate signaling molecules implicated in the control of root growth. Can. J. Bot. 82, 1177 1185.
42. Maldonado-Mendoza, I.E., Dewbre, G.R., Blaylock, L. Harrison, M.J. (2005) Expression of a xyloglucan endotransglucosylase/hydrolase gene, Mt-XTH1, from Medicago truncatula is induced systemically in mycorrhizal roots. Gene, 345, 191 197.
43. Manthey, K., Krajinski, F., Hohnjec, N., Firnhaber, C., Puhler, A., Perlick, A.M. Kuster, H. (2004) Transcriptome profiling in root nodules and arbuscular mycorrhiza identifies a collection of novel genes induced during Medicago truncatula root endosymbioses. Mol. Plant Microbe Interact. 17, 1063 1077.
44. McGonigle, T.P., Miller, M.H., Evans, D.G., Fairchild, G.L. Swan, J.A. (1990) A new method that gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytol. 115, 495 501.
45. Menge, J.A., Steirle, D., Bagyaraj, D.J., Johnson, E.L.V. Leonard, R.T. (1978) Phosphorus concentrations in plants responsible for inhibition of mycorrhizal infection. New Phytol. 80, 575 578.
46. Mirouze, M., Sels, J., Richard, O. et al. (2006) A putative novel role for plant defensins: a defensin from the zinc hyper-accumulating plant, Arabidopsis halleri, confers zinc tolerance. Plant J. 47, 329 342.
47. Mitra, R.M., Gleason, C.A., Edwards, A., Hadfield, J., Downie, J.A., Oldroyd, G.E.D. Long, S.R. (2004) A Ca2+/calmodulin-dependent protein kinase required for symbiotic nodule development: gene identification by transcript-based cloning. Proc. Natl Acad. Sci. USA, 101, 4701 4705.
48. Parniske, M. (2004) Molecular genetics of the arbuscular mycorrhizal symbiosis. Curr. Opin. Plant Biol. 7, 414 421.
49. Paszkowski, U. (2006) Mutualism and parasitism: the yin and yang of plant symbioses. Curr. Opin. Plant Biol. 9, 364 370.
50. Pfaffl, M.W. (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29 (9), e45.
51. Pieterse, C., van Wees, S., Hoffland, E., van Pelt, J.A. van Loon, L.C. (1996) Systemic resistance in Arabidopsis induced by biocontrol bacteria is independent of salicylic acid accumulation and pathogenesis-related gene expression. Plant Cell, 8, 1225 1237.
52. Pozo, M.J., Cordier, C., Dumas-Gaudot, E., Gianinazzi, S., Barea, J.M. Azcon-Aguilar, C. (2002) Localized versus systemic effect of arbuscular mycorrhizal fungi on defence responses to Phytophthora infection in tomato plants. J. Exp. Bot. 53, 525 534.
53. Sanchez, L., Weidmann, S., Arnould, C., Bernard, A.R., Gianinazzi, S. 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.
54. Sanders, F.E. (1974) The effect of foliar-applied phosphate on the mycorrhizal infections of onion roots. In Endomycorrhizas (Sanders, F.E., Mosse, B. Tinker, P.B., eds). University of Leeds : Academic Press, London, pp. 261 277.
55. Schnabel, E., Journet, E.P., de Carvalho-Niebel, F., Duc, G. 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. Schwab, S.M., Menge, J.A. Leonard, R.T. (1983) Comparison of stages of vesicular-arbuscular mycorrhiza formation in sudangrass grown at two levels of phosphorus nutrition. Am. J. Bot. 70, 1225 1232.
57. Schwab, S.M., Menge, J.A. Tinker, P.B. (1991) Regulation of nutrient transfer between host and fungus in vesicular-arbuscular mycorrhizas. New Phytol. 117, 387 398.
58. Schwarzott, D., Walker, C. Schüßler, A. (2001) Glomus, the largest genus of the arbuscular mycorrhizal fungi (Glomales), is nonmonophyletic. Mol. Phylogenet. Evol. 21, 190 197.
59. Searle, I.R., Men, A.E., Laniya, T.S., Buzas, D.M., Iturbe-Ormaetxe, I., Carroll, B.J. Gresshoff, P.M. (2002) Long-distance signaling in nodulation directed by a CLAVATA1-like receptor kinase. Science 299, 1 10.
60. Shaul, O., Galili, S., Volpin, H., Ginzberg, I., Elad, Y., Chet, I. Kapulnik, Y. (1999) Mycorrhiza-induced changes in disease severity and PR protein expression in tobacco leaves. Mol. Plant Microbe Interact. 12, 1000 1007.
61. Smith, S.E. Read, D.J. (1997) Mycorrhizal Symbiosis. San Diego, CA : Academic Press, Inc.
62. Smith, F.A. Smith, S.E. (1989) Membrane transport at the biotrophic interface: an overview. Aust. J. Plant Physiol. 16, 33 43.
63. Smith, S.E., Smith, F.A. Jakobsen, I. (2004) Functional diversity in arbuscular mycorrhizal (AM) symbioses: the contribution of the mycorrhizal P uptake pathway is not correlated with mycorrhizal responses in growth or total P uptake. New Phytol. 162, 511 524.
64. Spelbrink, R.G., Dilmac, N., Allen, A., Smith, T.J., Shah, D.M. Hockerman, G.H. (2004) Differential antifungal and calcium channel-blocking activity among structurally related plant defensins. Plant Physiol. 135, 2055 2067.
65. St-Arnaud, M., Hamel, C., Vimard, B., Caron, M. Fortin, J.A. (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, 328 332.
66. Stracke, S., Kistner, C., Yoshida, S. et al. (2002) A plant receptor-like kinase required for both bacterial and fungal symbiosis. Nature, 417, 959 962.
67. Terras, F.R.G., Eggermont, K., Kovaleva, V. et al. (1995) Small cysteine-rich antifungal proteins from radish - their role in host-defense. Plant Cell, 7, 573 588.
68. Thomson, B.D., Robson, A.D. Abbott, L.K. (1991) Soil mediated effects of phosphorus supply on the formation of mycorrhizas by Scutellispora calospora (Nicol. & Gerd.) Walker & Sanders on subterranean clover. New Phytol. 118, 463 469.
69. Timmusk, S. Wagner, E.G.H. (1999) The plant-growth-promoting rhizobacterium Paenibacillus polymyxa induces changes in Arabidopsis thaliana gene expression: a possible connection between biotic and abiotic stress responses. Mol. Plant Microbe Interact. 12, 951 959.
70. Vierheilig, H. (2004) Further root colonization by arbuscular mycorrhizal fungi in already mycorrhizal plants is suppressed after a critical level of root colonization. J. Plant Physiol. 161, 339 341.
71. Vierheilig, H., Garcia-Garrido, J.M., Wyss, U. Piche, Y. (2000) Systemic suppression of mycorrhizal colonization of barley roots already colonized by AM fungi. Soil Biol. Biochem. 32, 589 595.
72. Walker, C. Schussler, A. (2004) Nomenclatural clarification and new taxa in the Glomeromycota. Mycol. Res. 108, 981 982.
73. Walker, C., Blaszowski, L., Schwarzott, D. Schussler, A. (2004) Germannia gen. nov., a genus Glomeromycota. Mycol. Res. 108, 707 718.
74. Weidmann, S., Sanchez-Calderon, L., Descombin, J., Chatagnier, O., Gianinazzi, S. Gianinazzi-Pearson, V. (2004) Fungal elicitation of signal transduction related plant genes precedes mycorrhiza establishment and requires the DMI 3 gene in Medicago truncatula. Mol. Plant Microbe Interact. 17, 1385 1393.
75. Wulf, A., Manthey, K., Doll, J., Perlick, A.M., Linke, B., Bekel, T., Meyer, F., Franken, P., Kuster, H. Krajinski, F. (2003) Transcriptional changes in response to arbuscular mycorrhiza development in the model plant Medicago truncatula. Mol. Plant Microbe Interact. 16, 306 314.
76. Yang, Y.H., Dudoit, S., Luu, P., Lin, D.M., Peng, V., Ngai, J. Speed, T.P. (2002) Normalization for cDNA microarray data: a robust composite method addressing single and multiple slide systematic variation. Nucleic Acids Res. 30, e15.
77. Yang, S.H., Berberich, T., Miyazaki, A., Sano, H. Kusano, T. (2003) Ntdin, a tobacco senescence-associated gene, is involved in molybdenum cofactor biosynthesis. Plant Cell Physiol. 44, 1037 1044.
78. Zeng, L.R., Vega-Sanchez, M.E., Zhu, T. Wang, G.L. (2006) Ubiquitination-mediated protein degradation and modification: an emerging theme in plant-microbe interactions. Cell Res. 16, 413 426.