Colonization of barley by the broad-host hemibiotrophic pathogen Phytophthora palmivora uncovers a leaf development-dependent involvement of Mlo

Molecular Plant-Microbe Interactions

Volumn 29, Issue 5, 2016, Pages 385-395

  Le Fevre, Ruth ^a   O'Boyle, Bridget ^a   Moscou, Matthew J ^b   Schornack, Sebastian ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b SAINSBURY LABORATORY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

MLO PROTEIN, HORDEUM VULGARE; VEGETABLE PROTEIN;

CLASSIFICATION; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HORDEUM; METABOLISM; MICROBIOLOGY; MUTATION; PHYSIOLOGY; PHYTOPHTHORA; PLANT DISEASE; PLANT LEAF; PLANT ROOT;

GENE EXPRESSION REGULATION, PLANT; HORDEUM; MUTATION; PHYTOPHTHORA; PLANT DISEASES; PLANT LEAVES; PLANT PROTEINS; PLANT ROOTS;

EID: 84968616020     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-12-15-0276-R     Document Type: Article

References (58)

1. Acevedo-Garcia, J., Kusch, S., and Panstruga, R. 2014. Magical mystery tour: MLO proteins in plant immunity and beyond. New Phytol. 204: 273-281.
2. Ah Fong, A., and Judelson, H. S. 2003. Cell cycle regulator Cdc14 is expressed during sporulation but not hyphal growth in the fungus-like oomycete Phytophthora infestans. Mol. Microbiol. 50:487-494.
3. Büschges, R., Hollricher, K., Panstruga, R., Simons, G., Wolter, M., Frijters, A., van Daelen, R., van der Lee, T., Diergaarde, P., Groenendijk, J., Töpsch, S., Vos, P., Salamini, F., and Schulze-Lefert, P. 1997. The barley Mlo gene: A novel control element of plant pathogen resistance. Cell 88:695-705.
4. Chaparro-Garcia, A., Wilkinson, R. C., Gimenez-Ibanez, S., Findlay, K., Coffey, M. D., Zipfel, C., Rathjen, J. P., Kamoun, S., and Schornack, S. 2011. The receptor-like kinase SERK3/BAK1 is required for basal resistance against the late blight pathogen Phytophthora infestans in Nicotiana benthamiana. PLoS One 6:e16608.
5. Chen, L., Shiotani, K., Togashi, T., Miki, D., Aoyama, M., Wong, H. L., Kawasaki, T., and Shimamoto, K. 2010. Analysis of the Rac/Rop small GTPase family in rice: Expression, subcellular localization and role in disease resistance. Plant Cell Physiol. 51:585-595.
6. De Coninck, B., Timmermans, P., Vos, C., Cammue, B. P., and Kazan, K. 2015. What lies beneath: Belowground defense strategies in plants. Trends Plant Sci. 20:91-101.
7. Drenth, A., and Guest, D. I. 2004. Diversity and management of Phytophthora in Southeast Asia. Australian Centre for International Agricultural Research, Canberra, Australia.
8. Dufresne, M., and Osbourn, A. E. 2001. Definition of tissue-specific and general requirements for plant infection in a phytopathogenic fungus. Mol. Plant-Microbe Interact. 14:300-307.
9. Eichmann, R., Schultheiss, H., Kogel, K.-H., and Hückelhoven, R. 2004. The barley apoptosis suppressor homologue Bax inhibitor-1 compromises nonhost penetration resistance of barley to the inappropriate pathogen Blumeria graminis f. sp. tritici. Mol. Plant Microbe Interact. 17:484-490.
10. Eichmann, R., Bischof, M., Weis, C., Shaw, J., Lacomme, C., Schweizer, P., Duchkov, D., Hensel, G., Kumlehn, J., and Hückelhoven, R. 2010. BAX INHIBITOR-1 is required for full susceptibility of barley to powdery mildew. Mol. Plant Microbe Interact. 23:1217-1227.
11. Elliott, C., Zhou, F., Spielmeyer, W., Panstruga, R., and Schulze-Lefert, P. 2002. Functional conservation of wheat and rice Mlo orthologs in defense modulation to the powdery mildew fungus. Mol. Plant Microbe Interact. 15:1069-1077.
12. Ellis, J. G., Rafiqi, M., Gan, P., Chakrabarti, A., and Dodds, P. N. 2009. Recent progress in discovery and functional analysis of effector proteins of fungal and oomycete plant pathogens. Curr. Opin. Plant Biol. 12: 399-405.
13. Erwin, D. C., and Ribeiro, O. 1996. Phytophthora Diseases Worldwide. American Phytopathological Society, St Paul, MN, U.S.A.
14. Fisher, M. C., Henk, D. A., Briggs, C. J., Brownstein, J. S., Madoff, L. C., McCraw, S. L., and Gurr, S. J. 2012. Emerging fungal threats to animal, plant and ecosystem health. Nature 484:186-194.
15. Forsberg, L. 1985. Foliar diseases of nursery-grown ornamental palms in Queensland. Australas. Plant Pathol. 14:67-71.
16. Harris, D., Cardon, J. A., Justin, S., and Passey, A. 1984. Phytophthora palmivora on cultured roots of coconut. Trans. Br. Mycol. Soc. 82:249-255.
17. Harrison, M. J. 1999. Biotrophic interfaces and nutrient transport in plant fungal symbioses. J. Exp. Bot. 50:1013-1022.
18. Hayden, M. J., Kuchel, H., and Chalmers, K. J. 2004. Sequence tagged microsatellites for the Xgwm533 locus provide new diagnostic markers to select for the presence of stem rust resistance gene Sr2 in bread wheat (Triticum aestivum L.). Theor. Appl. Genet. 109:1641-1647.
19. Hok, S., Attard, A., and Keller, H. 2010. Getting the most from the host: How pathogens force plants to cooperate in disease. Mol. Plant-Microbe Interact. 23:1253-1259.
20. Hugot, K., Aime, S., Conrod, S., Poupet, A., and Galiana, E. 1999. Developmental regulated mechanisms affect the ability of a fungal pathogen to infect and colonize tobacco leaves. Plant J. 20:163-170.
21. Huitema, E., Smoker, M., and Kamoun, S. 2011. A straightforward protocol for electro-transformation of Phytophthora capsici zoospores. Methods Mol. Biol. 712:129-135.
22. Jarosch, B., Kogel, K. H., and Schaffrath, U. 1999. The ambivalence of the barley Mlo locus: Mutations conferring resistance against powdery mildew (Blumeria graminis f. sp. hordei) enhance susceptibility to the rice blast fungus Magnaporthe grisea. Mol. Plant Microbe Interact. 12: 508-514.
23. Jørgensen, J. H. 1992. Discovery, characterization and exploitation of Mlo powdery mildew resistance in barley. Euphytica 63:141-152.
24. Kamoun, S., van West, P., de Jong, A. J., de Groot, K. E., Vleeshouwers, V. G., and Govers, F. 1997. A gene encoding a protein elicitor of Phytophthora infestans is down-regulated during infection of potato. Mol. Plant Microbe Interact. 10:13-20.
25. Kemen, E., Kemen, A. C., Rafiqi, M., Hempel, U., Mendgen, K., Hahn, M., and Voegele, R. T. 2005. Identification of a protein from rust fungi transferred from haustoria into infected plant cells. Mol. Plant-Microbe Interact. 18:1130-1139.
26. Kessler, S. A., Shimosato-Asano, H., Keinath, N. F., Wuest, S. E., Ingram, G., Panstruga, R., and Grossniklaus, U. 2010. Conserved molecular components for pollen tube reception and fungal invasion. Science 330:968-971.
27. Kim, Y. J., Hwang, B. K., and Park, K. W. 1989. Expression of age-related resistance in pepper plants infected with Phytophthora capsici. Plant Dis. 73:745-474.
28. Kølster, P., Munk, L., Stølen, O., and Løhde, J. 1986. Near-isogenic barley lines with genes for resistance to powdery mildew. Crop Sci. 26:903-907.
29. Kumar, J., Hückelhoven, R., Beckhove, U., Nagarajan, S., and Kogel, K.-H. 2001. A compromised Mlo pathway affects the response of barley to the necrotrophic fungus Bipolaris sorokiniana (Teleomorph: Cochliobolus sativus) and its toxins. Phytopathology 91:127-133.
30. Lagudah, E. S., McFadden, H., Singh, R. P., Huerta-Espino, J., Bariana, H. S., and Spielmeyer, W. 2006. Molecular genetic characterization of the Lr34/Yr18 slow rusting resistance gene region in wheat. Theor. Appl. Genet. 114:21-30.
31. Lazarovits, G., Stössel, R., and Ward, E. W. B. 1981. Age-related changes in specificity and glyceollin production in the hypocotyl reaction of soybeans to Phytophthora megasperma var. sojae. Phytopathology 71: 94-97.
32. Li, B., and Xu, X. 2002. Infection and development of apple Scab (Venturia inaequalis) on old leaves. J. Phytopathol. 150:687-691.
33. -ΔΔCt method. Methods 25:402-408.
34. Marcel, S., Sawers, R., Oakeley, E., Angliker, H., and Paszkowski, U. 2010. Tissue-adapted invasion Strategies of the rice blast fungus Magnaporthe oryzae. Plant Cell 22:3177-3187.
35. Mazaheri-Naeini, M., Sabbagh, S. K., Martinez, Y., Sejalon-Delmas, N., and Roux, C. 2015. Assessment of Ustilago maydis as a fungal model for root infection studies. Fungal Biol-Uk 119:145-153.
36. McDonald, B. A., and Linde, C. 2002. Pathogen population genetics, evolutionary potential, and durable resistance. Annu. Rev. Phytopathol. 40:349-379.
37. McGrann, G. R. D., Townsend, B. J., Antoniw, J. F., Asher, M. J. C., and Mutasa-Goettgens, E. S. 2009. Barley elicits a similar early basal defence response during host and non-host interactions with Polymyxa root parasites. Eur. J. Plant Pathol. 123:5-15.
38. McGrann, G. R. D., Stavrinides, A., Russell, J., Corbitt, M. M., Booth, A., Chartrain, L., Thomas, W. T. B., and Brown, J. K. M. 2014. A trade off between mlo resistance to powdery mildew and increased susceptibility of barley to a newly important disease, Ramularia leaf spot. J. Exp. Bot. 65:1025-1037.
39. Peterhansel, C., Freialdenhoven, A., Kurth, J., Kolsch, R., and Schulze-Lefert, P. 1997. Interaction analyses of genes required for resistance responses to powdery mildew in barley reveal distinct pathways leading to leaf cell death. Plant Cell 9:1397-1409.
40. Piffanelli, P., Zhou, F. S., Casais, C., Orme, J., Jarosch, B., Schaffrath, U., Collins, N. C., Panstruga, R., and Schulze-Lefert, P. 2002. The barley MLO modulator of defense and cell death is responsive to biotic and abiotic stress stimuli. Plant Physiol. 129:1076-1085.
41. Pretorius, Z. A., Singh, R. P., Wagoire, W. W., and Payne, T. S. 2000. Detection of virulence to wheat stem rust resistance gene Sr31 in Puccinia graminis f. sp. tritici in Uganda. Plant Dis. 84:203.
42. Rafiqi, M., Gan, P. H., Ravensdale, M., Lawrence, G. J., Ellis, J. G., Jones, D. A., Hardham, A. R., and Dodds, P. N. 2010. Internalization of flax rust avirulence proteins into flax and tobacco cells can occur in the absence of the pathogen. Plant Cell 22:2017-2032.
43. Rey, T., Chatterjee, A., Buttay, M., Toulotte, J., and Schornack, S. 2015. Medicago truncatula symbiosis mutants affected in the interaction with a biotrophic root pathogen. New Phytol. 206:497-500.
44. Ruiz-Lozano, J. M., Gianinazzi, S., and Gianinazzi-Pearson, V. 1999. Genes involved in resistance to powdery mildew in barley differentially modulate root colonization by the mycorrhizal fungus Glomus mosseae. Mycorrhiza 9:237-240.
45. Salzman, R. A., Tikhonova, I., Bordelon, B. P., Hasegawa, P. M., and Bressan, R. A. 1998. Coordinate accumulation of antifungal proteins and hexoses constitutes a developmentally controlled defense response during fruit ripening in grape. Plant Physiol. 117:465-472.
46. Schilling, L., Matei, A., Redkar, A., Walbot, V., and Doehlemann, G. 2014. Virulence of the maize smut Ustilago maydis is shaped by organ-specific effectors. Mol. Plant Pathol. 15:780-789.
47. Schreiber, C., Slusarenko, A. J., and Schaffrath, U. 2011. Organ identity and environmental conditions determine the effectiveness of nonhost resistance in the interaction between Arabidopsis thaliana and Magnaporthe oryzae. Mol. Plant Pathol. 12:397-402.
48. Schultheiss, H., Dechert, C., Kogel, K.-H., and Hückelhoven, R. 2002. A small GTP-binding host protein is required for entry of powdery mildew fungus into epidermal cells of barley. Plant Physiol. 128:1447-1454.
49. Segovia, V., Hubbard, A., Craze, M., Bowden, S., Wallington, E., Bryant, R., Greenland, A., Bayles, R., and Uauy, C. 2014. Yr36 confers partial resistance at temperatures below 18°C to UK isolates of Puccinia striiformis. Phytopathology 104:871-878.
50. Sesma, A., and Osbourn, A. E. 2004. The rice leaf blast pathogen undergoes developmental processes typical of root-infecting fungi. Nature 431: 582-586.
51. Shibata, Y., Kawakita, K., and Takemoto, D. 2010. Age-related resistance of Nicotiana benthamiana against hemibiotrophic pathogen Phytophthora infestans requires both ethylene- and salicylic acid-mediated signaling pathways. Mol. Plant-Microbe Interact. 23:1130-1142.
52. Skibbe, D. S., Doehlemann, G., Fernandes, J., and Walbot, V. 2010. Maize tumors caused by Ustilago maydis require organ-specific genes in host and pathogen. Science 328:89-92.
53. Sukno, S. A., Garcia, V. M., Shaw, B. D., and Thon, M.R. 2008. Root infection and systemic colonization of maize by Colletotrichum graminicola. Appl. Environ. Microbiol. 74:823-832.
54. Torres, G., Sarria, G., Varon, F., Coffey, M., Elliott, M., and Martinez, G. 2010. First report of bud rot caused by Phytophthora palmivora on African oil palm in Colombia. Plant Dis. 94:1163-1163.
55. van Schie, C. C., and Takken, F. L. 2014. Susceptibility genes 101: How to be a good host. Annu. Rev. Phytopathol. 52:551-581.
56. Wang, E., Schornack, S., Marsh, J. F., Gobbato, E., Schwessinger, B., Eastmond, P., Schultze, M., Kamoun, S., and Oldroyd, G. E. 2012. A common signaling process that promotes mycorrhizal and oomycete colonization of plants. Curr. Biol. 22:2242-2246.
57. Wang, Y., Cheng, X., Shan, Q., Zhang, Y., Liu, J., Gao, C., and Qiu, J.-L. 2014. Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nat. Biotechnol. 32:947-951.
58. Wolter, M., Hollricher, K., Salamini, F., and Schulze-Lefert, P. 1993. The mlo resistance alleles to powdery mildew infection in barley trigger a developmentally controlled defence mimic phenotype. Mol. Gen. Genet. 239:122-128.