The rpg4-mediated resistance to wheat stem rust (Puccinia graminis) in barley (Hordeum vulgare) requires Rpg5, a second NBS-LRR gene, and an actin depolymerization factor

Molecular Plant-Microbe Interactions

Volumn 26, Issue 4, 2013, Pages 407-418

  Wang, X ^a   Richards, J ^a   Gross, T ^a   Druka, A ^b   Kleinhofs, A ^c   Steffenson, B ^d   Acevedo, M ^a   Brueggeman, R ^a  

^a NORTH DAKOTA STATE UNIVERSITY   (United States)

^b SCOTTISH CROP RESEARCH INSTITUTE   (United Kingdom)

^c WASHINGTON STATE UNIVERSITY   (United States)

^d UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN DEPOLYMERIZING FACTOR; VEGETABLE PROTEIN;

ARTICLE; BASIDIOMYCETES; DISEASE RESISTANCE; GENE SILENCING; GENETICS; GENOTYPE; HORDEUM; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PHYSIOLOGY; PLANT DISEASE;

BASIDIOMYCOTA; DESTRIN; DISEASE RESISTANCE; GENE SILENCING; GENOTYPE; HORDEUM; PLANT DISEASES; PLANT PROTEINS;

EID: 84874608061     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-06-12-0146-R     Document Type: Article

References (68)

1. Ashikawa, I., Hayashi, N., Yamane, H., Kanamori, H., Wu, J., Matsumoto, T., Ono, K., and Yano, M. 2008. Two adjacent nucleotide-binding site- leucine-rich repeat class genes are required to confer Pikm-specific rice blast resistance. Genetics 180:2267-2276.
2. Birker, D., Heidrich, K., Takahara, H., Narusaka, M., Deslandes, L., Narusaka, Y., Reymond, M., Parker, J. E., and O'Connell, R. 2009. A locus conferring resistance to Colletotrichum higginsianum is shared by four geographically distinct Arabidopsis accessions. Plant J. 60:602-613.
3. Block, A., and Alfano, J. R. 2011. Plant targets for Pseudomonas syringae type III effectors: Virulence targets or guarded decoys? Curr. Opin. Microbiol. 14:39-46.
4. Borovkova, I. G., Steffenson, B. J., Jin, Y., Rasmussen, J. B., Kilian, A., Kleinhofs, A., Rossnagel, B. G., and Kao, K. N. 1995. Identification of molecular markers linked to the stem rust resistance gene rpg4 in barley. Phytopathology 85:181-185.
5. Brueggeman, R., Rostoks, N., Kudrna, D., Kilian, A., Han, F., Chen, J., Druka, A., Steffenson, B., and Kleinhofs, A. 2002. The barley stem rustresistance gene Rpg1 is a novel disease-resistance gene with homology to receptor kinases. Proc. Natl. Acad. Sci. U.S.A. 99:9328-9333. (Pubitemid 34764613)
6. Brueggeman, R., Druka, A., Nirmala, J., Cavileer, T., Drader, T., Rostoks, N., Mirlohi, A., Bennypaul, H., Gill, U., Kudrna, D., Whitelaw, C., Kilian, A., Han, F., Sun, Y., Gill, K., Steffenson, B., and Kleinhofs, A. 2008. The stem rust resistance gene Rpg5 encodes a novel protein with nucleotide binding site, leucine-rich and protein kinase domains. Proc. Natl. Acad. Sci. U.S.A. 105:14970-14975.
7. Brueggeman, R., Steffenson, B. J., and Kleinhofs, A. 2009. The rpg4/Rpg5 stem rust resistance locus in barley; resistance genes and cytoskeleton dynamics. Cell Cycle 8:977-981.
8. Caplan, J., Padmanabhan, M., and Dinesh-Kumar, S. P. 2008 Plant NBLRR immune receptors: From recognition to transcriptional reprogramming. Cell Host Microbe 3:126-135. (Pubitemid 351325765)
9. Chai, Y. 2011. Investigations on stem rust resistance genes in barley. M.S. thesis, University of Minnesota, St. Paul.
10. Chen, Y., Cheung, A. Y., and Wu, H. M. 2003. Actin-depolymerizing factor mediates Rac/Rop GTPase-regulated pollen tube growth. Plant Cell 15:237-249. (Pubitemid 36137673)
11. Deslandes, L., Olivier, J., Peeters, N., Feng, D. X., Khounlotham, M., Boucher, C, Somssich, I., Genin, S., and Marco, Y. 2003. Physical interaction between RRS1-R, a protein conferring resistance to bacterial wilt, and PopP2, a type III effector targeted to the plant nucleus. Proc. Natl. Acad. Sci. U.S.A. 100:8024-8029. (Pubitemid 36760088)
12. Dodds, P. N., Lawrence, G. J., Catanzariti, A.-M., The, T., Wang, C.-I. A., Ayliffe, M., Kobe, B., and Ellis, J. G. 2006. Direct protein interaction underlies gene-for-gene specificity and co-evolution of the flax resistance genes and flax rust avirulence genes. Proc. Natl. Acad. Sci. U.S.A. 103:8888-8893. (Pubitemid 43878113)
13. Druka, A., Kudrna, D., Han, F., Kilian, A., Steffenson, B., Frisch, D., Tomkins, J., Wing, R., and Kleinhofs, A. 2000. Physical mapping of barley stem rust resistance gene rpg4. Mol. Gen. Genet. 264:283-290.
14. Eitas, T. K., and Dangl, J. L. 2010. NB-LRR proteins: Pairs, pieces, perception, partners, and pathways. Curr. Opin. Plant Biol. 13:472-477.
15. Faris, J. D., Zhang, Z., Lu, H., Lu, S., Reedy, 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. U.S.A. 107:13544-13549.
16. Feng, Y., Liu, Q., and Xue, Q. 2006. Comparative study of rice and Arabidopsis actin-depolymerizing factors gene families. J. Plant Physiol. 163:69-79. (Pubitemid 41797561)
17. Flor, H. H. 1971. Current status of the gene-for-gene concept. Annu. Rev. Phytopathol. 9:275-296.
18. Fu, D., Uauy, C., Distelfeld, A., Blechl, A., Epstein, L., Chen, X., Sela, H., Fahima, T., and Dubcovsky, J. 2009. A kinase-START gene confers temperature-dependent resistance to wheat stripe rust. Science 323:1357-1360.
19. Hanks, S., Quinn, A., and Hunter, T. 1988. The protein kinase family: Conserved features and deduced phylogeny of the catalytic domains. Science 241:42-52.
20. Hein, I., Barciszewska-Pacak, M., Hrubikova, K., Williamson, S., Dinesen, M., Soenderby, I., 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. (Pubitemid 43733558)
21. Holzberg, S. S., Brosio, P., Gross, C., and Pogue, G. P. 2002. Barley Stripe Mosaic Virus-induced gene silencing in monocot plant. Plant J. 30:315-327. (Pubitemid 34544033)
22. Hulbert, S. H., Webb, C. A., Smith, S. M., and Sun, Q. 2001. Resistance gene complexes: Evolution and utilization. Annu. Rev. Phytopathol. 39:285-312. (Pubitemid 32965187)
23. Jia, J., 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 (Eur. Mol. Biol. Organ.) J. 19:4004- 4014. (Pubitemid 30608539)
24. Jin, Y., Steffenson, B. J., and Fetch, T. G. J. 1994a. Sources of resistance to pathotype QCC of Puccinia graminis f. sp. tritici in barley. Crop Sci. 34:285-288. (Pubitemid 2044367)
25. Jin, Y., Steffenson, B. J., and Miller, J. D. 1994b. Inheritance of resistance to pathotypes QCC and MCC of Puccinia graminis f. sp. tritici in barley line Q21861 and temperature effects on the expression of resistance. Phytopathology 84:452-455.
26. Kleinhofs, A., Brueggeman, R., Nirmala, J., Zhang, L., Mirlohi, A., Druka, A., Rostoks, N., and Steffenson, B. J. 2009 Barley stem rust resistance genes: Structure and function. Plant Genome 2:109-120.
27. Kwon, C., Bednarek, P., and Schulze-Lefert, P. 2008. Secretory pathways in plant immune responses. Plant Physiol. 147:1575-1583. (Pubitemid 352844204)
28. Lee, S.-K., Song, M.-Y., Seo, Y.-S., Kim, H.-K., Ko, S., Cao, P.-J., Suh, J.- P., Yi, G., Roh, J.-H., Lee, S., An, G., Hahn, T.-R., Wang, G.-L., Ronald, P., and Jeon, J.-S. 2009. Rice Pi5-mediated resistance to Magnaporthe oryzae requires the presence of two coiled-coil-nucleotide-bindingleucine- rich repeat genes. Genetics 181:1627-1638.
29. Leister, D. 2004. Tandem and segmental gene duplication and recombination in the evolution of plant disease resistance genes. Trends Gene 20:116-122. (Pubitemid 38230024)
30. Loutre, C., Wicker, T., Travella, S., Galli, P., Scofield, S., Fahima, T., Feuillet, C., and Keller, B. 2009. Two different CC-NBS-LRR genes are required for Lr10-mediated leaf rust resistance in tetraploid and hexaploid wheat. Plant J. 60:1043-1054.
31. Martin, G. B., Brommonschenkel, S. H., Chunwongse, J., Frary, A., Ganal, M. W., Spivey, R., Wu, T., Earle, E. D., and Tanksley, S. D. 1993. Mapbased cloning of a protein kinase gene conferring disease resistance in tomato. Science 262:1432-1436. (Pubitemid 24035063)
32. Martin, G. B, Bogdanove, A. J., and Sessa, G. 2003. Understanding the function of plant disease resistance proteins. Annu. Rev. Plant Biol. 54:23-61. (Pubitemid 37399986)
33. Meyers, B. C., Kozik, A., Griego, A., Kuang, H. H., and Michelmore, R. W. 2003 Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell 15:809-834. (Pubitemid 36453281)
34. Miklis, M., Consonni, C., Bhat, R. A., Lipka, V., Schulze-Lefert, P., and Panstruga, R. 2007. Barley MLO modulates actin-dependent and actinindependent antifungal defense pathways at the cell periphery. Plant Physiol. 144:1132-1143. (Pubitemid 46944774)
35. Moscou, M. J., Lauter, N., Steffenson, B., and Wise, R. P. 2011 Quantitative and qualitative stem rust resistance factors in barley are associated with transcriptional suppression of defense regulons. PLoS Genet. 7:e1002208.
36. Narusaka, M., Shirasu, K., Noutoshi, Y., Kubo, Y., Shiraishi, T., Iwabuchi, M., and Narusaka, Y. 2009 RRS1 and RPS4 provide a dual resistancegene system against fungal and bacterial pathogens. Plant J. 60:218-226.
37. Nirmala, J., Drader, T., Chen, X., Steffenson, B., and Kleinhofs, A. 2010 Stem rust spores elicit rapid RPG1 phosphorylation. Mol. Plant- Microbe Interact. 23:1635-1642.
38. Okuyama, Y., Kanzaki, H., Abe, A., Yoshida, K., Tamiru, M., Saitoh, H., Fujibe, T., Matsumura, H., Shenton, M., Galam, D. C. Undan, J., Ito, A., Sone, T., and Terauchi, R. 2011. A multi-faceted genomics approach allows the isolation of rice Pia-blast resistance gene consisting of two adjacent NBS-LRR protein genes. Plant J. 66:467-479.
39. Ouellet, F., Carpentier, E., Cope, J., Monroy, A.F., and Sarhan, F. 2001. Regulation of a wheat actin-depolymerizing factor during cold acclimation. Plant Physiol. 125:360-368. (Pubitemid 32116773)
40. Park, C.-J., Peng, Y., Chen, X., Dardick, C., Ruan, D., Bart, R., Canlas, P. E., and Ronald, P. E. 2008. Rice XB15, a protein phospahatase 2C, negatively regulates cell death and XA21-mediated innate immunity. PLoS Biol. 6:e231.
41. Peart, J. R., Mestre, P., Lu, R., Malcuit, I., and Baulcombe, D. C. 2005. NRG1, a CC-NB-LRR protein, together with N, a TIR-NB-LRR protein, mediates resistance against tobacco mosaic virus. Curr. Biol. 15:968-973. (Pubitemid 40772068)
42. 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.
43. Roelfs, A. P., Casper, D. H., Long, D. L., and Roberts, J. J. 1991. Races of Puccinia graminis in the United States in 1989. Plant Dis 75:1127-1130.
44. Rostoks, N., Schmierer, D., Kudrna, D., and Kleinhofs, A. 2003. Barley putative hypersensitive induced reaction genes: Genetic mapping, sequence analyses and differential expression in disease lesion mimic mutants. Theor. Appl. Genet. 107:1094-1101. (Pubitemid 37261739)
45. 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 LR21-mediated leaf rust resistance pathway. Plant Physiol. 138:2165-2173. (Pubitemid 43733559)
46. Shao, F., Golstein, C., Ade, J., Stoutemyer, M., Dixon, J. E., and Innes, R. W. 2003. Cleavage of Arabidopsis PBS1 by a bacterial type III effector. Science 301:1230-1233. (Pubitemid 37052210)
47. Sinapidou, E., Williams, K., Nott, L., Bahky, S., Tor, M., Bittner-Eddy, P., and Beynon, J. 2004. Two TIR:NB:LRR genes are required to specify resistance to Peronospora parasitica isolate Cala2 in Arabidopsis. Plant J. 38:898-909. (Pubitemid 38783966)
48. Singh, R. P., Hodson, D. P., Huerta-Espino, J., Jin, Y., Njau, P., Wanyera, R., Herrera-Foessel, S. A., and Ward, R. W. 2008. Will stem rust destroy the world's wheat crop? Adv. Agron. 98:271-309.
49. Song, W.-Y., Wang, G.-L., Chen, L., Kim, H.-S., Pi, L.-Y., Gardner, J., Wang, B., Holsten, T., Zhai, W.-X., Zhu, L.-H., Fauquet, C., and Ronald, P. C. 1995. A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science 270:1804-1806. (Pubitemid 26007223)
50. Stakman, E. C., Stewart, D. M., and Loegering, W. Q. 1962. Identification of physiological races of Puccinia graminis f. sp. tritici. U.S. Dep. Agric. Agric. Res. Serv. Publ. No. E617.
51. Steffenson, B. J. 1992. Analysis of durable resistance to stem rust in barley. Euphytica 63:153-167.
52. Steffenson, B. J., and Jin, Y. 2006. Resistance to race TTKS of Puccinia graminis f. sp. tritici in barley. (Abstr.) Phytopathology 96:S110.
53. Steffenson, B. J., Jin, Y., Brueggeman, R. S., Kleinhofs, A., and Sun, Y. 2009. Resistance to stem rust race TTKSK maps to the rpg4/Rpg5 complex of chromosome 5H of barley. Phytopathology 99:1135-1141.
54. Steffenson, B. J., Zhou, H., Chai, Y., and Grando, S. 2012. Vulnerability of cultivated and wild barley to African stem rust race TTKSK. Pages 149- 155 in: Advances in Barley Science: Proc. 11th Int. Barley Genet. Symp. C. Li, G. Zhang, and X. Liu, eds. Zhejiang University Press, Hangzhou, China.
55. Sun, X., Cao, Y., Yang, Z., Xu, C., Li, X., Wang, S., and Zhang, Q. 2004. Xa26, a gene conferring resistance to Xanthomonas oryzae pv. oryzae in rice, encodes an LRR receptor kinase-like protein. Plant J. 37:517- 527. (Pubitemid 38258773)
56. Sun, Y., and Steffenson, B. J. 2005. Reaction of barley seedlings with different stem rust resistance genes to Puccinia graminis f. sp. tritici and Puccinia graminis f. sp. secalis. Can. J. Plant Pathol. 27:80-89. (Pubitemid 40912624)
57. Sun, Y., Steffenson, B. J., and Jin, Y. 1996. Genetics of resistance to Puccinia graminis f. sp. secalis in barley line Q21861. Phytopathology 86:1299-1302. (Pubitemid 27030650)
58. Swiderski, M. R., and Innes, R. W. 2001. The Arabidopsis PBS1 resistance gene encodes a member of a novel protein kinase subfamily. Plant J. 26:101-112. (Pubitemid 32494759)
59. Tang, X., Frederick, R. D., Zhou, J., Halterman, D. A., and Yia, Y. 1996. Initiation of plant disease resistance by physical interaction of AvrPto and Pto kinase. Science 274:2060-2063. (Pubitemid 27020696)
60. Thomas, P., and Schiefelbein, J. 2002. Cloning and characterization of an actin depolymerizing factor gene from grape (Vitis vinifera L.) expressed during rooting in stem cuttings. Plant Sci. 162:283-288. (Pubitemid 34111752)
61. Tian, M., Chaudhry, F., Ruzicka, D. R., Meagher, R. B., Staiger, C. J., and Day, B. 2009. Arabidopsis actin-depolymerizing factor AtADF4 mediates defense signal transduction triggered by the Pseudomonas syringae effector AvrPphB. Plant Physiol. 150:815-824.
62. Tufan, H. A., Stefanato, F. L., McGrann, G. R. D., MacCormack, R., and Boyd, L. A. 2011. The Barley Stripe Mosaic Virus system used for virus-induced gene silencing in cereals differentially affects susceptibility to fungal pathogens in wheat. J. Plant Physiol. 168:990-994.
63. Ueda, H., Yamaguchi, Y., and Sano, H. 2006. Direct interaction between the tobacco mosaic virus helicase domain and the ATP-bound resistance protein, N factor during the hypersensitive response in tobacco plants. Plant Mol. Biol. 61:31-45.
64. Van Der Biezen, E. A., and Jones, J. D. G. 1998. Plant disease-resistance proteins and the gene-for-gene concept. Trends Biochem. Sci. 23):454- 456. (Pubitemid 29002901)
65. Van Der Hoom, R. A. L., and Kamoun, S. 2008. From Guard to Decoy: A New Model for perception of plant pathogen effectors. Plant Cell 20:2009-2017. (Pubitemid 352844506)
66. Yu, Y., Tomkins, J., Waugh, R., Frisch, D., Kudrna, D., Kleinhofs, A., Brueggeman, R., Muehlbauer, G., Wise, R., and Wing, R. 2000. A bacterial artificial chromosome library for barley (Hordeum vulgare L.) and the identification of clones containing putative resistance genes. Theor. Appl. Genet. 101:1093-1099.
67. Yuan, B., Zhai, C., Wang, W., Zeng, X., Xu, X., Hu, H., Lin, F., Wang, L., and Pan, Q. 2011. The Pik-p resistance to Magnaporthe oryzae in rice is mediated by a pair of closely linked CC-NBS-LRR genes. Theor. Appl. Genet. 122:1017-1028.
68. Zhou, T., Wang, Y., Chen, J. Q., Araki, H., Jing, Z., Jiang, K., Shen, J., and Tian, D. 2004. Genome-wide identification of NBS genes in japonica rice reveals significant expansion of divergent non-TIR NBS-LRR genes. Mol. Genet. Genomics 271:402-415. (Pubitemid 38824034)