Deregulation of plant cell death through disruption of chloroplast functionality affects asexual sporulation of Zymoseptoria tritici on wheat

Molecular Plant-Microbe Interactions

Volumn 28, Issue 5, 2015, Pages 590-604

  Lee, Wing Sham ^a   Devonshire, B Jean ^a   Hammond Kosack, Kim E ^a   Rudd, Jason J ^a   Kanyuka, Kostya ^a  

^a ROTHAMSTED RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGI; TRITICUM AESTIVUM;

CHLOROPHYLL; CYCLOPENTANE DERIVATIVE; HYDROGEN PEROXIDE; JASMONIC ACID; OXYLIPIN; SALICYLIC ACID; VEGETABLE PROTEIN;

ASCOMYCETES; CELL DEATH; CHLOROPLAST; GENE EXPRESSION REGULATION; GENETICS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; PLANT DISEASE; PLANT LEAF; REPORTER GENE; ULTRASTRUCTURE; WHEAT;

ASCOMYCOTA; CELL DEATH; CHLOROPHYLL; CHLOROPLASTS; CYCLOPENTANES; GENE EXPRESSION REGULATION, PLANT; GENES, REPORTER; HOST-PATHOGEN INTERACTIONS; HYDROGEN PEROXIDE; OXYLIPINS; PLANT DISEASES; PLANT LEAVES; PLANT PROTEINS; SALICYLIC ACID; TRITICUM;

EID: 84930371892     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-10-14-0346-R     Document Type: Article

References (62)

1. Allen, A. M., Barker, G. L. A., Wilkinson, P., Burridge, A., Winfield, M., Coghill, J., Uauy, C., Griffiths, S., Jack, P., Berry, S., Werner, P., Melichar, J. P., McDougall, J., Gwilliam, R., Robinson, P., and Edwards, K. J. 2013. Discovery and development of exome-based, co-dominant single nucleotide polymorphism markers in hexaploid wheat (Triticum aestivum L.). Plant Biotechnol. J. 11:279-295.
2. Asada, K. 1999. The water-water cycle in chloroplasts: Scavenging of active oxygens and dissipation of excess photos. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50:601-639.
3. Asselbergh, B., Curvers, K., Franca, S. C., Audenaert, K., Vuylsteke, M., Van Breusegem, F., and Höfte, M. 2007. Resistance to Botrytis cinerea in sitiens, an abscisic acid-deficient tomato mutant, involves timely production of hydrogen peroxide and cell wall modifications in the epidermis. Plant Physiol. 144:1863-1877.
4. Brading, P. A., Verstappen, E. C. P., Kema, G. H. J., and Brown, J. K. M. 2002. A gene-for-gene relationship between wheat and Mycosphaerella graminicola, the Septoria tritici blotch pathogen. Phytopathology 92: 439-445.
5. Bryan, G. T., Wu, K. S., Farrall, L., Jia, Y., Hershey, H. P., McAdams, S. A., Faulk, K. N., Donaldson, G. K., Tarchini, R., and Valent, B. 2000. A single amino acid difference distinguishes resistant and susceptible alleles of the rice blast resistance gene Pi-ta. Plant Cell 12:2033-2046.
6. Chartrain, L., Brading, P. A., and Brown, J. K. M. 2005. Presence of the Stb6 gene for resistance to septoria tritici blotch (Mycosphaerella graminicola) in cultivars used in wheat-breeding programmes worldwide. Plant Pathol. 54:134-143.
7. Coego, A., Ramirez, V., Gil, M. J., Flors, V., Mauch-Mani, B., and Vera, P. 2005. An Arabidopsis homeodomain transcription factor, OVEREXPRESSOR OF CATIONIC PEROXIDASE 3, mediates resistance to infection by necrotrophic pathogens. Plant Cell 17:2123-2137.
8. Consolo, V. F., Albani, C. M., Berón, C. M., Salerno, G. L., and Cordo, C. A. 2009. A conventional PCR technique to detect Septoria tritici in wheat seeds. Australas. Plant Pathol. 38:222-227.
9. Creelman, R. A., and Mullet, J. E. 1997. Biosynthesis and action of jasmonates in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48:355-381.
10. Dean, R., Van Kan, J. A. L., Pretorius, Z. A., Hammond-Kosack, K. E., Di Pietro, A., Spanu, P. D., Rudd, J. J., Dickman, M., Kahmann, R., Ellis, J., and Foster, G. D. 2012. The top 10 fungal pathogens in molecular plant pathology. Mol. Plant Pathol. 13:414-430.
11. Dickman, M. B., and de Figueiredo, P. 2013. Death be not proud - cell death control in plant fungal interactions. PLoS Pathog. 9:e1003542 Published online.
12. Ding, S., Lu, Q., Zhang, Y., Yang, Z., Wen, X., Zhang, L., and Lu, C. 2009. Enhanced sensitivity to oxidative stress in transgenic tobacco plants with decreased glutathione reductase activity leads to a decrease in ascorbate pool and ascorbate redox state. Plant Mol. Biol. 69:577-592.
13. Du Fall, L. A. D., and Solomon, P. S. 2013. The necrotrophic effector SnToxA induces the synthesis of a novel phytoalexin in wheat. New Phytol. 200:185-200.
14. Eyal, Z. 1999. The Septoria tritici and Stagonospora nodorum blotch diseases of wheat. Eur. J. Plant Pathol. 105:629-641.
15. Faris, J. D., Zhang, Z., Lu, H., Lu, S., Reddy, L., Cloutier, S., Fellers, J. P., Meinhardt, S. W., Rasmussen, J. B., Xu, S. S., Oliver, R. P., Simons, K. J., and Friesen, T. L. 2010. A unique wheat disease resistance-like gene governs effector-triggered susceptibility to necrotrophic pathogens. Proc. Natl. Acad. Sci. USA 107:13544-13549.
16. Galvez-Valdivieso, G., and Mullineaux, P. M. 2010. The role of reactive oxygen species in signalling from chloroplasts to the nucleus. Physiol. Plant. 138:430-439.
17. Goodwin, S. B. 2012. Resistance in wheat to septoria diseases caused by Mycosphaerella graminicola (Septoria tritici) and Phaeosphaeria (Stagonospora) nodorum. Pages 151-159 in Disease Resistance in Wheat, 2012, I. Sharma, ed. CABI, Wallingford, U.K.
18. Goodwin, S. B., M'barek, S. B., Dhillon, B., Wittenberg, A. H. J., Crane, C. F., Hane, J. K., Foster, A. J., Van der Lee, T. A., Grimwood, J., Aerts, A., Antoniw, J., Bailey, A., Bluhm, B., Bowler, J., Bristow, J., van der Burgt, A., Canto-Canché, B., Churchill, A. C., Conde-Ferràez, L., Cools, H. J., Coutinho, P. M., Csukai, M., Dehal, P., De Wit, P., Donzelli, B., van de Geest, H. C., van Ham, R. C., Hammond-Kosack, K. E., Henrissat, B., Kilian, A., Kobayashi, A. K., Koopmann, E., Kourmpetis, Y., Kuzniar, A., Lindquist, E., Lombard, V., Maliepaard, C., Martins, N., Mehrabi, R., Nap, J. P., Ponomarenko, A., Rudd, J. J., Salamov, A., Schmutz, J., Schouten, H. J., Shapiro, H., Stergiopoulos, I., Torriani, S. F., Tu, H., de Vries, R. P., Waalwijk, C., Ware, S. B., Wiebenga, A., Zwiers, L. H., Oliver, R. P., Grigoriev, I. V., and Kema, G. H. 2011. Finished genome of the fungal wheat pathogen Mycosphaerella graminicola reveals dispensome structure, chromosome plasticity, and stealth pathogenesis. PLoS Genet. 7:e1002070 Published online.
19. Govrin, E. M., and Levine, A. 2000. The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Curr. Biol. 10:751-757.
20. Hein, I., Barciszewska-Pacak, M., Hrubikova, K., Williamson, S., Dinesen, M., Soenderby, I. E., Sundar, S., Jarmolowski, A., Shirasu, K., and Lacomme, C. 2005. Virus-induced gene silencing-based functional characterization of genes associated with powdery mildew resistance in barley. Plant Physiol. 138:2155-2164.
21. Hiriart, J.-B., Lehto, K., Tyystjärvi, E., Junttila, T., and Aro, E.-M. 2002. Suppression of a key gene involved in chlorophyll biosynthesis by means of virus-inducing gene silencing. Plant Mol. Biol. 50:213-224.
22. Horbach, R., Navarro-Quesada, A. R., Knogge, W., and Deising, H. B. 2011. When and how to kill a plant cell: Infection strategies of plant pathogenic fungi. J. Plant Physiol. 168:51-62.
23. Ishiguro, S., Kawai-Oda, A., Ueda, J., Nishida, I., and Okada, K. 2001. The DEFECTIVE IN ANTHER DEHISCIENCE gene encodes a novel phospholipase A1 catalyzing the initial step of jasmonic acid biosynthesis, which synchronizes pollen maturation, anther dehiscence, and flower opening in Arabidopsis. Plant Cell 13:2191-2209.
24. Jasid, S., Simontacchi, M., Bartoli, C. G., and Puntarulo, S. 2006. Chloroplasts as a nitric oxide cellular source. Effect of reactive nitrogen species on chloroplastic lipids and proteins. Plant Physiol. 142: 1246-1255.
25. Jia, Y., McAdams, S. A., Bryan, G. T., Hershey, H. P., and Valent, B. 2000. Direct interaction of resistance gene and avirulence gene products confers rice blast resistance. EMBO J. 19:4004-4014.
26. Jing, H. C., Lovell, D., Gutteridge, R., Jenk, D., Kornyukhin, D., Mitrofanova, O. P., Kema, G. H., and Hammond-Kosack, K. E. 2008. Phenotypic and genetic analysis of the Triticum monococcum-Mycosphaerella graminicola interaction. New Phytol. 179:1121-1132.
27. Kangasjärvi, S., Neukermans, J., Li, S., Aro, E.-M., and Noctor, G. 2012. Photosynthesis, photorespiration, and light signalling in defence responses. J. Exp. Bot. 63:1619-1636.
28. Kema, G. H. J., Yu, D. Z., Rijkenberg, F. H. J., Shaw, M. W., and Baayen, R. P. 1996. Histology of the pathogenesis of Mycosphaerella graminicola in wheat. Phytopathology 86:777-786.
29. Keogh, R. C., Deverall, B. J. and McLeod, S. 1980. Comparison of histological and physiological responses to Phakopsora pachyrhizi in resistant and susceptible soybean. Trans. Brit. Mycol. Soc. 74:329-333.
30. Keon, J., Antoniw, J., Carzaniga, R., Deller, S., Ward, J. L., Baker, J. M., Beale, M. H., Hammond-Kosack, K., and Rudd, J. J. 2007. Transcriptional adaptation of Mycosphaerella graminicola to programmed cell death (PCD) of its susceptible wheat host. Mol. Plant Microbe Interact. 20:178-193.
31. Kumagai, M. H., Donson, J., della-Cioppa, G., Harvey, D., Hanley, K., and Grill, L. K. 1995. Cytoplasmic inhibition of carotenoid biosynthesis with virus-derived RNA. Proc. Natl. Acad. Sci. USA 92:1679-1683.
32. Lam, E., Kato, N., and Lawton, M. 2001. Programmed cell death, mitochondria and the plant hypersensitive response. Nature 411:848-853.
33. Lee, W. S., Hammond-Kosack, K. E., and Kanyuka, K. 2012. Barley stripe mosaic virus-mediated tools for investigating gene function in cereal plants and their pathogens: Virus-induced gene silencing, host-mediated gene silencing, and virus-mediated overexpression of heterologous protein. Plant Physiol. 160:582-590.
34. Lee, W.-S., Rudd, J. J., Hammond-Kosack, K. E., and Kanyuka, K. 2014. Mycosphaerella graminicola LysM effector-mediated stealth pathogenesis subverts recognition through both CERK1 and CEBiP homologues in wheat. Mol. Plant Microbe Interact. 27:236-243.
35. Liu, Z., Zhang, Z., Faris, J. D., Oliver, R. P., Syme, R., McDonald, M. C., McDonald, B. A., Solomon, P. S., Lu, S., Shelver, W. L., Xu, S., and Friesen, T. L. 2012. The cysteine rich necrotrophic effector SnTox1 produced by Stagonospora nodorum triggers susceptibility of wheat lines harboring Snn1. PLoS Pathog. 8:e1002467 Published online.
36. Lorang, J. M., Sweat, T. A., and Wolpert, T. J. 2007. Plant disease susceptibility conferred by a "resistance" gene. Proc. Natl. Acad. Sci. USA 104:14861-14866.
37. Lorang, J., Kidarsa, T., Bradford, C. S., Gilbert, B., Curtis, M., Tzeng, S. C., Maier, C. S., and Wolpert, T. J. 2012. Tricking the guard: Exploiting plant defense for disease susceptibility. Science 338:659-662.
38. Lorrain, S., Vailleau, F., Balagué, C., and Roby, D. 2003. Lesion mimic mutants: Keys for deciphering cell death and defense pathways in plants? Trends Plant Sci. 8:263-271.
39. Luo, T., Luo, S., Araújo, W. L., Schlicke, H., Rothbart, M., Yu, J., Fan, T., Fernie, A. R., Grimm, B., and Luo, M. 2013. Virus-induced gene silencing of pea CHLI and CHLD affects tetrapyrrole biosynthesis, chloroplast development and the primary metabolic network. Plant Physiol. Biochem. 65:17-26.
40. Lyngs Jørgensen, H. J. L., Deneergaard, E., and Smedegaard-Petersen, V. 1993. Histological examination of the interaction between Rhynchosporium secalis and susceptible and resistant cultivars of barley. Physiol. Mol. Plant Pathol. 42:345-358.
41. Masuda, T. 2008. Recent overview of the Mg branch of the tetrapyrrole biosynthesis leading to chlorophylls. Photosynth. Res. 96:121-143.
42. Mengiste, T. 2012. Plant immunity to necrotrophs. Annu. Rev. Phytopathol. 50:267-294.
43. Oliver, R. P., and Solomon, P. S. 2010. New developments in pathogenicity and virulence of necrotrophs. Curr. Opin. Plant Biol. 13:415-419.
44. Palmer, C.-L., and Skinner, W. 2002. Mycosphaerella graminicola: Latent infection, crop devastation and genomics. Mol. Plant Pathol. 3:63-70.
45. Papenbrock, J., Pfündel, E., Mock, H.-P., and Grimm, B. 2000. Decreased and increased expression of the subunit CHL I diminishes Mg chelatase activity and reduces chlorophyll synthesis in transgenic tobacco plants. Plant J. 22:155-164.
46. Qin, G., Gu, H., Ma, L., Peng, Y., Deng, X. W., Chen, Z., and Qu, L.-J. 2007. Disruption of phytoene desaturase gene results in albino and dwarf phenotypes in Arabidopsis by impairing chlorophyll, carotenoid, and gibberellin biosynthesis. Cell Res. 17:471-482.
47. Qutob, D., Kemmerling, B., Brunner, F., Küfner, I., Engelhardt, S., Gust, A. A., Luberacki, B., Seitz, H. U., Stahl, D., Rauhut, T., Glawischnig, E., Schween, G., Lacombe, B., Watanabe, N., Lam, E., Schlichting, R., Scheel, D., Nau, K., Dodt, G., Hubert, D., Gijzen, M., and Nürnberger, T. 2006. Phytotoxicity and innate immune responses induced by Nep1-like proteins. Plant Cell 18:3721-3744.
48. Repka, V. 2002. Hydrogen peroxide generated via the octadecanoid pathway is neither necessary nor sufficient for methyl jasmonate-induced hypersensitive cell death in woody plants. Biol. Plantarum 45:105-115.
49. Rudd, J. J., Keon, J., and Hammond-Kosack, K. E. 2008. The wheat mitogen-activated protein kinases TaMPK3 and TaMPK6 are differentially regulated at multiple levels during compatible disease interactions with Mycosphaerella graminicola. Plant Physiol. 147:802-815.
50. Scofield, S. R., Huang, L., Brandt, A. S., and Gill, B. S. 2005. Development of a virus-induced gene-silencing system for hexaploid wheat and its use in functional analysis of the Lr21-mediated leaf rust resistance pathway. Plant Physiol. 138:2165-2173.
51. Shen, Y.-Y., Wang, X.-F., Wu, F.-Q., Du, S.-Y., Cao, Z., Shang, Y., Wang, X.-L., Peng, C.-C., Yu, X.-C., Zhu, S.-Y., Fan, R.-C., Xu, Y.-H., and Zhang, D.-P. 2006. The Mg-chelatase H subunit is an abscisic acid receptor. Nature 443:823-826.
52. Shetty, N. P., Kristensen, B. K., Newman, M. A., Moller, K., Gregersen, P. L., and Jorgensen, H. J. L. 2003. Association of hydrogen peroxide with restriction of Septoria tritici in resistant wheat. Physiol. Mol. Plant Pathol. 62:333-346.
53. Sierla, M., Rahikainen, M., Salojärvi, J., Kangasjärvi, J., and Kangasjärvi, S. 2013. Apoplastic and chloroplastic redox signaling networks in plant stress responses. Antioxid. Redox Signal. 18:2220-2239.
54. Staal, J., Kaliff, M., Dewaele, E., Persson, M., and Dixelius, C. 2008. RLM3, a TIR domain encoding gene involved in broad-range immunity of Arabidopsis to necrotrophic fungal pathogens. Plant J. 55:188-200.
55. Strawn, M.A., Marr, S.K., Inoue, K., Inada, N., Zubieta, C., and Wildermuth, M. C. 2007. Arabidopsis isochorismate synthase functional in pathogen-induced salicylate biosynthesis exhibits properties consistent with a role in diverse stress responses. J. Biol. Chem. 282:5919-5933.
56. 2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J. 11:1187-1194.
57. Triantaphylidès, C., Krischke, M., Hoeberichts, F. A., Ksas, B., Gresser, G., Havaux, M., Van Breusegem, F., and Mueller, M. J. 2008. Singlet oxygen is the major reactive oxygen species involved in photooxidative damage to plants. Plant Physiol. 148:960-968.
58. Vleeshouwers, V. G., van Dooijeweert, W., Govers, F., Kamoun, S., and Colon, L. T. 2000. The hypersensitive response is associated with host and nonhost resistance to Phytophthora infestans. Planta 210:853-864.
59. Wang, M., Wang, G., Ji, J., and Wang, J. 2009. The effect of pds gene silencing on chloroplast pigment composition, thylakoid membrane structure and photosynthesis efficiency in tobacco plants. Plant Sci. 177: 222-226.
60. Williams, B., Kabbage, M., Kim, H. J., Britt, R., and Dickman, M. B. 2011. Tipping the balance: Sclerotinia sclerotiorum secreted oxalic acid suppresses host defenses by manipulating the host redox environment. PLoS Pathog. 7:e1002107 Published online.
61. Wolpert, T. J., Dunkle, L. D., and Ciuffetti, L. M. 2002. Host-selective toxins and avirulence determinants: What's in a name? Annu. Rev. Phytopathol. 40:251-285.
62. Yuan, C., Li, C., Yan, L., Jackson, A. O., Liu, Z., Han, C., Yu, J., and Li, D. 2011. A high throughput Barley stripe mosaic virus vector for virus induced gene silencing in monocots and dicots. PLoS ONE 6:e26468 Published online.