Iron deficiency affects plant defence responses and confers resistance to dickeya dadantii and botrytis cinerea

Molecular Plant Pathology

Volumn 13, Issue 8, 2012, Pages 816-827

  Kieu, Nam Phuong ^a,b,d   Aznar, Aude ^b   Segond, Diego ^b,e   Rigault, Martine ^b   Simond Côte, Elizabeth ^b   Kunz, Caroline ^b   Soulie, Marie Christine ^b   Expert, Dominique ^b,c   Dellagi, Alia ^b  

^a UNIVERSITY OF NATURAL SCIENCES   (Viet Nam)

^b SORBONNE UNIVERSITÉ   (France)

^c CNRS   (France)

^d GHENT UNIVERSITY   (Belgium)

^e UMR1319 MICALIS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

IRON; MESSENGER RNA; PECTATE LYASE; POLYSACCHARIDE LYASE; REACTIVE OXYGEN METABOLITE;

ARABIDOPSIS; ARTICLE; BOTRYTIS; ENTEROBACTERIACEAE; GENETICS; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PLANT GENE;

ARABIDOPSIS; BOTRYTIS; ENTEROBACTERIACEAE; GENES, PLANT; IRON; POLYSACCHARIDE-LYASES; REACTIVE OXYGEN SPECIES; RNA, MESSENGER;

ARABIDOPSIS; ARABIDOPSIS THALIANA; BACTERIA (MICROORGANISMS); BOTRYOTINIA FUCKELIANA; DICKEYA DADANTII; FUNGI;

EID: 84865736383     PISSN: 14646722     EISSN: 13643703     Source Type: Journal    
DOI: 10.1111/j.1364-3703.2012.00790.x     Document Type: Article

References (54)

1. Anderson, A.J. and Guerra, D. (1985) Responses of bean to root colonization with Pseudomonas putida in a hydroponic system. Phytopathology, 75, 992-995.
2. Andrews, S.C., Robinson, A.K. and Rodriguez-Quinones, F. (2003) Bacterial iron homeostasis. FEMS Microbiol. Rev. 27, 215-237.
3. Arbelet, D., Malfatti, P., Simond-Cote, E., Fontaine, T., Desquilbet, L., Expert, D., Kunz, C. and Soulie, M.C. (2010) Disruption of the bcchs3a chitin synthase gene in Botrytis cinerea is responsible for altered adhesion and overstimulation of host plant immunity. Mol. Plant-Microbe Interact. 23, 1324-1334.
4. Briat, J.-F., Curie, C. and Gaymard, F. (2007a) Iron utilization and metabolism in plants. Curr. Opin. Plant Biol. 10, 276-282.
5. Briat, J.F., Arnaud, N., Cellier, F., Curie, C., Gaymard, F., Ravel, K., Seguela, M. and Vert, G. (2007b) Iron uptake and storage in plants. Am. J. Hematol. 82, 506-507.
6. Dellagi, A., Rigault, M., Segond, D., Roux, C., Kraepiel, Y., Cellier, F., Briat, J.F., Gaymard, F. and Expert, D. (2005) Siderophore-mediated upregulation of Arabidopsis ferritin expression in response to Erwinia chrysanthemi infection. Plant J. 43, 262-272.
7. Eichhorn, H., Lessing, F., Winterberg, B., Schirawski, J., Kaemper, J., Mueller, P. and Kahmann, R. (2006) A ferroxidation/permeation iron uptake system is required for virulence in Ustilago maydis. Plant Cell, 18, 3332-3345.
8. Eide, D., Broderius, M., Fett, J. and Guerinot, M.L. (1996) A novel iron-regulated metal transporter from plants identified by functional expression in yeast. Proc. Natl. Acad. Sci. USA, 93, 5624-5628.
9. Enard, C., Diolez, A. and Expert, D. (1988) Systemic virulence of Erwinia-chrysanthemi 3937 requires a functional iron assimilation system. J. Bacteriol. 170, 2419-2426.
10. Expert, D. (1999) Withholding and exchanging iron: interactions between Erwinia spp. and their plant hosts. Annu. Rev. Phytopathol. 37, 307-334.
11. Fagard, M., Dellagi, A., Roux, C., Perino, C., Rigault, M., Boucher, V., Shevchik, V.E. and Expert, D. (2007) Arabidopsis thaliana expresses multiple lines of defense to counterattack Erwinia chrysanthemi. Mol. Plant-Microbe Interact. 20, 794-805.
12. Franza, T., Mahe, B. and Expert, D. (2005) Erwinia chrysanthemi requires a second iron transport route dependent on the siderophore achromobactin for extracellular growth and plant infection. Mol. Microbiol. 55, 261-275.
13. Galletti, R., Denoux, C., Gambetta, S., Dewdney, J., Ausubel, F.M., De Lorenzo, G. and Ferrari, S. (2008) The AtrbohD-mediated oxidative burst elicited by oligogalacturonides in Arabidopsis is dispensable for the activation of defense responses effective against Botrytis cinerea. Plant Physiol. 148, 1695-1706.
14. Gaymard, F., Boucherez, J. and Briat, J.F. (1996) Characterization of a ferritin mRNA from Arabidopsis thaliana accumulated in response to iron through an oxidative pathway independent of abscisic acid. Biochem. J. 318, 67-73.
15. Glazebrook, J. (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu. Rev. Phytopathol. 43, 205-227.
16. Greenshields, D.L., Liu, G.S., Feng, J., Selvaraj, G. and Wei, Y.D. (2007) The siderophore biosynthetic gene SID1, but not the ferroxidase gene FET3, is required for full Fusarium graminearum virulence. Mol. Plant Pathol. 8, 411-421.
17. Haas, H., Eisendle, M. and Turgeon, B.G. (2008) Siderophores in fungal physiology and virulence. Annu. Rev. Phytopathol. 46, 149-187.
18. Huber, D.M. and Watson, R.D. (1974) Nitrogen form and plant disease. Annu. Rev. Phytopathol. 12, 139-165.
19. Kim, S.A., Punshon, T., Lanzirotti, A., Li, L., Alonso, J.M., Ecker, J.R., Kaplan, J. and Guerinot, M.L. (2006) Localization of iron in Arabidopsis seed requires the vacuolar membrane transporter VIT1. Science, 314, 1295-1298.
20. Kobayashi, T., Nakanishi, H. and Nishizawa, N.K. (2010) Recent insights into iron homeostasis and their application in graminaceous crops. Proc. Jpn. Acad., Ser. B, Phys. Biol. Sci. 86, 900-913.
21. Konetschny-Rapp, S., Jung, G., Huschka, H.-G. and Winkelmann, G. (1988) Isolation and identification of the principal siderophore of the plant pathogenic fungus Botrytis cinerea. Biol. Metals, 1, 90-98.
22. Kraepiel, Y., Pedron, J., Patrit, O., Simond-Cote, E., Hermand, V. and Van Gijsegem, F. (2011) Analysis of the plant bos1 mutant highlights necrosis as an efficient defence mechanism during D. dadantii/Arabidospis thaliana interaction. PLoS ONE 6, e18991.
23. Lanquar, V., Lelievre, F., Bolte, S., Hames, C., Alcon, C., Neumann, D., Vansuyt, G., Curie, C., Schroder, A., Kramer, U., Barbier-Brygoo, H. and Thomine, S. (2005) Mobilization of vacuolar iron by AtNRAMP3 and AtNRAMP4 is essential for seed germination on low iron. EMBO J. 24, 4041-4051.
24. Lanquar, V., Ramos, M.S., Lelievre, F., Barbier-Brygoo, H., Krieger-Liszkay, A., Kraemer, U. and Thomine, S. (2010) Export of vacuolar manganese by AtNRAMP3 and AtNRAMP4 is required for optimal photosynthesis and growth under manganese deficiency. Plant Physiol. 152, 1986-1999.
25. Lebeau, A., Reverchon, S., Gaubert, S., Kraepiel, Y., Simond-Cote, E., Nasser, W. and Van Gijsegem, F. (2008) The GacA global regulator is required for the appropriate expression of Erwinia chrysanthemi 3937 pathogenicity genes during plant infection. Environ. Microbiol. 10, 545-559.
26. Lemanceau, P., Expert, D., Gaymard, F., Bakker, P. and Briat, J.F. (2009) Role of iron in plant-microbe interactions. Adv. Bot. Res. 51, 491-549.
27. Lindsay, W.L. and Schwab, A.P. (1982) The chemistry of iron in soils and its availability to plants. J. Plant Nutr. 5, 821-840.
28. Luna, E., Pastor, V., Robert, J., Flors, V., Mauch-Mani, B. and Ton, J. (2011) Callose deposition: a multifaceted plant defense response. Mol. Plant-Microbe Interact. 24, 183-193.
29. Macur, R.E., Mathre, D.E. and Olsen, R.A. (1991) Interactions between iron nutrition and verticillium wilt resistance in tomato. Plant Soil, 134, 281-286.
30. Marschner, H. (1995) Mineral Nutrition of Higher Plants, New York: Academic Press.
31. Mittler, R., Vanderauwera, S., Suzuki, N., Miller, G., Tognetti, V.B., Vandepoele, K., Gollery, M., Shulaev, V. and Van Breusegem, F. (2011) ROS signaling: the new wave? Trends Plant Sci. 16, 300-309.
32. Morrissey, J. and Guerinot, M.L. (2009) Iron uptake and transport in plants: the good, the bad, and the ionome. Chem. Rev. 109, 4553-4567.
33. Münzinger, M., Budzikiewicz, H., Expert, D., Enard, C. and Meyer, J.M. (2000) Achromobactin, a new citrate siderophore of Erwinia chrysanthemi. Z. Naturforsch. C, 55, 328-332.
34. Murdoch, L., Corbel, J.C., Reis, D., Bertheau, Y. and Vian, B. (1999) Differential cell wall degradation by Erwinia chrysanthemi in petiole of Saintpaulia ionantha. Protoplasma, 210, 59-74.
35. Nurchi, V.M., Pivetta, T., Lachowicz, J.I. and Crisponi, G. (2009) Effect of substituents on complex stability aimed at designing new iron(III) and aluminum(III) chelators. J. Inorg. Biochem. 103, 227-236.
36. Oide, S., Moeder, W., Krasnoff, S., Gibson, D., Haas, H., Yoshioka, K. and Turgeon, B.G. (2006) NPS6, encoding a nonribosomal peptide synthetase involved in siderophore-mediated iron metabolism, is a conserved virulence determinant of plant pathogenic ascomycetes. Plant Cell, 18, 2836-2853.
37. Perombelon, M.C.M. (2002) Potato diseases caused by soft rot erwinias: an overview of pathogenesis. Plant Pathol. 51, 1-12.
38. Persmark, M., Expert, D. and Neilands, J.B. (1989) Isolation, characterization, and synthesis of chrysobactin, a compound with siderophore activity from Erwinia-chrysanthemi. J. Biol. Chem. 264, 3187-3193.
39. Petit, J.M., Briat, J.F. and Lobreaux, S. (2001) Structure and differential expression of the four members of the Arabidopsis thaliana ferritin gene family. Biochem. J. 359, 575-582.
40. Pierre, J.L. and Fontecave, M. (1999) Iron and activated oxygen species in biology: the basic chemistry. Biometals, 12, 195-199.
41. Ravet, K., Touraine, B., Kim, S.A., Cellier, F., Thomine, S., Guerinot, M.L., Briat, J.F. and Gaymard, F. (2009) Post-translational regulation of atfer2 ferritin in response to intracellular iron trafficking during fruit development in Arabidopsis. Mol. Plant, 2, 1095-1106.
42. Reignault, P., Kunz, C., Delage, N., Moreau, E., Vedel, R., Hamada, W., Bompeix, G. and Boccara, M. (2000) Host- and symptom-specific pectinase isozymes produced by Botrytis cinerea. Mycol. Res. 104, 421-428.
43. Robinson, N.J., Procter, C.M., Connolly, E.L. and Guerinot, M.L. (1999) A ferric-chelate reductase for iron uptake from soils. Nature, 397, 694-697.
44. Romheld, V. and Marschner, H. (1986) Evidence for a specific uptake system for iron phytosiderophores in roots of grasses. Plant Physiol. 80, 175-180.
45. Sambrook, J., Fritsch, E.F. and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Press.
46. Samson, R., Legendre, J.B., Christen, R., Fischer-Le Saux, M., Achouak, W. and Gardan, L. (2005) Transfer of Pectobacterium chrysanthemi (Burkholder etal. 1953) Brenner etal. 1973 and Brenneria paradisiaca to the genus Dickeya gen. nov as Dickeya chrysanthemi comb. nov and Dickeya paradisiaca comb. nov and delineation of four novel species, Dickeya dadantii sp nov., Dickeya dianthicola sp nov., Dickeya dieffenbachiae sp nov and Dickeya zeae sp nov. Int. J. Syst. Evol. Microbiol. 55, 1415-1427.
47. Schwyn, B. and Neilands, J.B. (1987) Universal chemical assay for the detection and determination of siderophores. Anal. Biochem. 160, 47-56.
48. Segond, D., Dellagi, A., Lanquar, V., Rigault, M., Patrit, O., Thomine, S. and Expert, D. (2009) NRAMP genes function in Arabidopsis thaliana resistance to Erwinia chrysanthemi infection. Plant J. 58, 195-207.
49. Snoeijers, S.S., Perez-Garcia, A., Joosten, M. and De Wit, P. (2000) The effect of nitrogen on disease development and gene expression in bacterial and fungal plant pathogens. Eur. J. Plant Pathol. 106, 493-506.
50. Toth, I.K., Bell, K.S., Holeva, M.C. and Birch, P.R.J. (2003) Soft rot erwiniae: from genes to genomes. Mol. Plant Pathol. 4, 17-30.
51. Weiss, G. (2002) Iron and immunity: a double-edged sword. Eur. J. Clin. Invest. 32, 70-78.
52. Winkelmann, G. (2007) Ecology of siderophores with special reference to the fungi. Biometals, 20, 379-392.
53. Yang, T.J.W., Lin, W.-D. and Schmidt, W. (2010) Transcriptional profiling of the Arabidopsis iron deficiency response reveals conserved transition metal homeostasis networks. Plant Physiol. 152, 2130-2141.
54. Zhang, C., Gutsche, A.T. and Shapiro, A.D. (2004) Feedback control of the Arabidopsis hypersensitive response. Mol. Plant-Microbe Interact. 17, 357-365.