Two RxLR avirulence genes in Phytophthora sojae determine soybean Rps1k-mediated disease resistance

Molecular Plant-Microbe Interactions

Volumn 26, Issue 7, 2013, Pages 711-720

  Song, Tianqiao ^a   Kale, Shiv D ^b   Arredondo, Felipe D ^b,c   Shen, Danyu ^a,c   Su, Liming ^a   Liu, Li ^a   Wu, Yuren ^a   Wang, Yuanchao ^a   Dou, Daolong ^a,b   Tyler, Brett M ^b,c  

^a NANJING AGRICULTURAL UNIVERSITY   (China)

^b VIRGINIA BIOINFORMATICS INSTITUTE   (United States)

^c OREGON STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

VIRULENCE FACTOR;

ALLELE; AMINO ACID SEQUENCE; ARTICLE; CELL DEATH; DISEASE RESISTANCE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE LOCUS; GENE SILENCING; GENETIC LINKAGE; GENETIC POLYMORPHISM; GENETICS; GENOTYPE; IMMUNOLOGY; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PARASITOLOGY; PATHOGENICITY; PHENOTYPE; PHYSIOLOGY; PHYTOPHTHORA; PLANT DISEASE; PLANT GENE; PLANT GROWTH; PLANT LEAF; PLANT ROOT; PLANT STEM; SEEDLING; SOYBEAN; VIRULENCE;

ALLELES; AMINO ACID SEQUENCE; CELL DEATH; DISEASE RESISTANCE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE SILENCING; GENES, PLANT; GENETIC LINKAGE; GENETIC LOCI; GENOTYPE; HYPOCOTYL; MOLECULAR SEQUENCE DATA; PHENOTYPE; PHYTOPHTHORA; PLANT DISEASES; PLANT LEAVES; PLANT ROOTS; PLANT STEMS; POLYMORPHISM, GENETIC; SEEDLING; SOYBEANS; VIRULENCE; VIRULENCE FACTORS;

GLYCINE MAX; OOMYCETES; PHYTOPHTHORA; PHYTOPHTHORA SOJAE;

EID: 84878640592     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-12-12-0289-R     Document Type: Article

References (62)

1. Ah-Fong, A. M., Bormann-Chung, C. A., and Judelson, H. S. 2008. Optimization of transgene-mediated silencing in Phytophthora infestans and its association with small-interfering RNAs. Fungal Genet. Biol. 45:1197-1205.
2. Armstrong, M. R., Whisson, S. C., Pritchard, L., Bos, J. I., Venter, E., Avrova, A. O., Rehmany, A. P., Bohme, U., Brooks, K., Cherevach, I., Hamlin, N., White, B., Fraser, A., Lord, A., Quail, M. A., Churcher, C., Hall, N., Berriman, M., Huang, S., Kamoun, S., Beynon, J. L., and Birch, P. R. 2005. An ancestral oomycete locus contains late blight avirulence gene Avr3a, encoding a protein that is recognized in the host cytoplasm. Proc. Natl. Acad. Sci. U.S.A. 102:7766-7771. (Pubitemid 40741044)
3. Bhattacharyya, M. K., Narayanan, N. N., Gao, H., Santra, D. K., Salimath, S. S., Kasuga, T., Liu, Y., Espinosa, B., Ellison, L., Marek, L., Shoemaker, R., Gijzen, M., and Buzzell, R. I. 2005. Identification of a large cluster of coiled coil-nucleotide binding site-leucine rich repeat-type genes from the Rps1 region containing Phytophthora resistance genes in soybean. Theor. Appl. Genet. 111:75-86. (Pubitemid 40912330)
4. Bisgrove, S. R., Simonich, M. T., Smith, N. M., Sattler, A., and Innes, R. W. 1994. A disease resistance gene in Arabidopsis with specificity for two different pathogen avirulence genes. Plant Cell 6:927-933.
5. Bos, J. I., Armstrong, M. R., Gilroy, E. M., Boevink, P. C., Hein, I., Taylor, R. M., Zhendong, T., Engelhardt, S., Vetukuri, R. R., Harrower, B., Dixelius, C., Bryan, G., Sadanandom, A., Whisson, S. C., Kamoun, S., and Birch, P. R. 2010. Phytophthora infestans effector AVR3a is essential for virulence and manipulates plant immunity by stabilizing host E3 ligase CMPG1. Proc. Natl. Acad. Sci. U.S.A. 107:9909-9914.
6. Boutemy, L. S., King, S. R., Win, J., Hughes, R. K., Clarke, T. A., Blumenschein, T. M., Kamoun, S., and Banfield, M. J. 2011. Structures of Phytophthora RXLR effector proteins: A conserved but adaptable fold underpins functional diversity. J. Biol. Chem. 286:35834-35842.
7. Catanzariti, A. M., Dodds, P. N., Lawrence, G. J., Ayliffe, M. A., and Ellis, J. G. 2006. Haustorially expressed secreted proteins from flax rust are highly enriched for avirulence elicitors. Plant Cell 18:243-256. (Pubitemid 43951327)
8. Chen, X., Shen, G., Wang, Y., and Zheng, X. 2007. Identification of Phytophthora sojae genes upregulated during the early stage of soybean infection. FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Lett. 269:280-288. (Pubitemid 46449734)
9. Cheng, B., Yu, X., Ma, Z., Dong, S., Dou, D., Wang Y., and Zheng, X., 2012. Phytophthora sojae effector Avh331 suppresses the plant defence response by disturbing the MAPK signalling pathway. Physiol. Mol. Plant Pathol. 77:1-9.
10. Cui, L., Yin, W., Tang, Q., Dong, S., Zheng, X., Zhang, Z., and Wang, Y. 2010. Distribution, pathotypes, and metalaxyl sensitivity of Phytophthora sojae from Heilongjiang and Fujian provinces in China. Plant Dis. 94:881-884.
11. Cui, L., Yin, W., Dong, S., and Wang, Y. 2012. Analysis of polymorphism and transcription of the effector gene Avr1b in Phytophthora sojae isolates from China virulent to Rps1b. Mol. Plant. Pathol. 13:114-122.
12. Dehal, P. S., and Boore, J. L. 2006. A phylogenomic gene cluster resource: The Phylogenetically Inferred Groups (PHIGs) database. BMC Bioinf. 7:201.
13. Dodds, P. N., Lawrence, G. J., Catanzariti, A. M., Teh, T., Wang, C. I., Ayliffe, M. A., Kobe, B., and Ellis, J. G. 2006. Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes. Proc. Natl. Acad. Sci. U.S.A. 103:8888-8893. (Pubitemid 43878113)
14. Dong, S., Qutob, D., Tedman-Jones, J., Kuflu, K., Wang, Y., Tyler, B. M., and Gijzen, M. 2009. The Phytophthora sojae avirulence locus Avr3c encodes a multi-copy RXLR effector with sequence polymorphisms among pathogen strains. PLoS ONE 4:e5556. Published online.
15. Dong, S., Yin, W., Kong, G., Yang, X., Qutob, D., Chen, Q., Kale, S. D., Sui, Y., Zhang, Z., Dou, D., Zheng, X., Gijzen, M., Tyler, B. M., and Wang, Y. 2011a. Phytophthora sojae avirulence effector Avr3b is a secreted NADH and ADP-ribose pyrophosphorylase that modulates plant immunity. PLoS Pathog. 7:e1002353. Published online.
16. Dong, S., Yu, D., Cui, L., Qutob, D., Tedman-Jones, J., Kale, S. D., Tyler, B. M., Wang, Y., and Gijzen, M. 2011b. Sequence variants of the Phytophthora sojae RXLR effector Avr3a/5 are differentially recognized by Rps3a and Rps5 in soybean. PLoS ONE 6:e20172. Published online.
17. Dou, D., Kale, S. D., Wang, X., Chen, Y., Wang, Q., Jiang, R. H., Arredondo, F. D., Anderson, R. G., Thakur, P. B., McDowell, J. M., Wang, Y., and Tyler, B. M. 2008a. Conserved C-terminal motifs required for avirulence and suppression of cell death by Phytophthora sojae effector Avr1b. Plant Cell 20:1118-1133. (Pubitemid 352843983)
18. Dou, D., Kale, S. D., Wang, X., Jiang, R. H. Y., Bruce, N. A., Arredondo, F. D., Zhang, X., and Tyler, B. M. 2008b. RXLR-mediated entry of Phytophthora sojae effector Avr1b into soybean cells does not require pathogen-encoded machinery. Plant Cell 20:1930-1947. (Pubitemid 352844542)
19. Dou, D., Kale, S. D., Liu, T., Tang, Q., Wang, X., Arredondo, F. D., Basnayake, S., Whisson, S., Drenth, A., Maclean, D., and Tyler, B. M. 2010. Different domains of Phytophthora sojae effector Avr4/6 are recognized by soybean resistance genes Rps4 and Rps6. Mol. Plant-Microbe Interact. 23:425-435.
20. Erwin, D., and Ribiero. O., 1996. Phytophthora Diseases Worldwide. American Phytopathological Society Press, St. Paul, MN, U.S.A.
21. Forster, H., Tyler, B. M., and Coffey, M. D. 1994. Phytophthora sojae races have arisen by clonal evolution and by rare outcrosses. Mol. Plant-Microbe Interact. 7:780-791.
22. Gao, H., and Bhattacharyya, M. K. 2008. The soybean-Phytophthora resistance locus Rps1-k encompasses coiled coil-nucleotide binding-leucine rich repeat-like genes and repetitive sequences. BMC Plant Biol. 8:29.
23. Gao, H., Narayanan, N. N., Ellison, L., and Bhattacharyya, M. K. 2005. Two classes of highly similar coiled coil-nucleotide binding-leucine rich repeat genes isolated from the Rps1-k locus encode Phytophthora resistance in soybean. Mol. Plant-Microbe Interact. 18:1035-1045. (Pubitemid 41356407)
24. Gijzen, M., Förster, H., Coffey, M. D., and Tyler, B. 1996. Cosegregation of Avr4 and Avr6 in Phytophthora sojae. Can. J. Bot. 74:800-802. (Pubitemid 126511114)
25. Gordon, S. G., St. Martin, S. K., and Dorrance, A. E. 2006. Rps8 maps to a resistance gene rich region on soybean molecular linkage group F. Crop Sci. 46:168-173. (Pubitemid 43219999)
26. Gu, B., Kale, S. D., Wang, Q., Wang, D., Pan, Q., Cao, H., Meng, Y., Kang, Z., Tyler, B. M., and Shan, W. 2011. Rust secreted protein Ps87 is conserved in diverse fungal pathogens and contains a RXLR-like motif sufficient for translocation into plant cells. PLoS ONE 6:e27217. Published online.
27. Jiang, R. H., Tripathy, S., Govers, F., and Tyler, B. M. 2008. RXLR effector reservoir in two Phytophthora species is dominated by a single rapidly evolving superfamily with more than 700 members. Proc. Natl. Acad. Sci. U.S.A. 105:4874-4879. (Pubitemid 351753839)
28. Judelson, H., Tyler, B. M., and Michelmore, R. W. 1991. Transformation of the oomycete pathogen, Phytophthora infestans. Mol. Plant-Microbe Interact. 4:602-607.
29. Jurka, J., Kapitonov, V. V., Pavlicek, A., Klonowski, P., Kohany, O., and Walichiewicz, J. 2005. Repbase update, a database of eukaryotic repetitive elements. Cytogenet. Genome Res. 110:462-467. (Pubitemid 41159923)
30. Kale, S. D., Gu, B., Capelluto, D. G. S., Dou, D., Feldman, E., Rumore, A., Arredondo, F. D., Hanlon, R., Fudal, I., Rouxel, T., Lawrence, C. B., Shan, W., and Tyler, B. M. 2010. External lipid PI3P mediates entry of eukaryotic pathogen effectors into plant and animal host cells. Cell 142:284-295.
31. Kamoun, S. 2003. Molecular genetics of pathogenic oomycetes. Eukaryot. Cell 2:191-199. (Pubitemid 36562358)
32. Kaufmann, M. J., and Gerdemann, J. W. 1958. Root and stem rot of soybean caused by Phytophthora sojae. Phytopathology 48:201-208.
33. Kohany, O., Gentles, A. J., Hankus, L., and Jurka, J. 2006. Annotation, submission and screening of repetitive elements in Repbase: Repbase-Submitter and Censor. BMC Bioinf. 7:474.
34. Kroon, L., Henk, B., Decock, A., and Govers, F. 2012. The Phytophthora Genus Anno 2012. Phytopathology 102:348-364.
35. Liu, T., Ye, W., Ru, Y., Yang, X., Gu, B., Tao, K., Lu, S., Dong, S., Zheng, X., Shan, W., Wang, Y., and Dou, D. 2011. Two host cytoplasmic effectors are required for pathogenesis of Phytophthora sojae by suppression of host defenses. Plant Physiol. 155:490-501.
36. Lohnes, D. G., and Schmitthenner, A. F. 1997. Position of the Phytophthora resistance gene Rps7 on the soybean molecular map. Crop Sci. 37:555-556. (Pubitemid 27185781)
37. Lozano-Torres, J. L., Wilbers, R. H., Gawronski, P., Boshoven, J. C., Finkers-Tomczak, A., Cordewener, J. H., America, A. H., Overmars, H. A., Van 't Klooster, J. W., Baranowski, L., Sobczak, M., Ilyas, M., van der Hoorn, R. A., Schots, A., de Wit, P. J., Bakker, J., Goverse, A., and Smant, G. 2012. Dual disease resistance mediated by the immune receptor Cf-2 in tomato requires a common virulence target of a fungus and a nematode. Proc. Natl. Acad. Sci. U.S.A. 109:10119-10124.
38. Mackey, D., Holt, B. F., 3rd, Wiig, A., and Dangl, J. L. 2002. RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell 108:743-754. (Pubitemid 34327527)
39. May, K. J., Whisson, S. C., Zwart, R. S., Searle, I. R., Irwin, J. A. G., Maclean, D. J., Carroll, B. J., and Drenth, A. 2002. Inheritance and mapping of 11 avirulence genes in Phytophthora sojae. Fungal Genet. Biol. 37:1-12.
40. McLeod, A., Fry, B. A., Zuluaga, A. P., Myers, K. L., and Fry, W. E. 2008. Toward improvements of oomycete transformation protocols. J. Eukaryot. Microbiol. 55:103-109. (Pubitemid 351342109)
41. Polzin, K. M., Lohnes, D. G., Nickell, C. D., and Shoemaker, R. C. 1994. Integration of Rps2, Rmd, and Rj2 into linkage group J of the soybean molecular map. J. Hered. 85:300-303. (Pubitemid 24278091)
42. Qutob, D., Tedman-Jones, J., Dong, S., Kuflu, K., Pham, H., Wang, Y., Dou, D., Kale, S. D., Arredondo, F. D., Tyler, B. M., and Gijzen, M. 2009. Copy number variation and transcriptional polymorphisms of Phytophthora sojae RXLR effector genes Avr1a and Avr3a. PLoS ONE 4:e5066. Published online.
43. Qutob, D., Chapman, B. P., and Gijzen, M. 2013. Transgenerational gene silencing causes gain of virulence in a plant pathogen. Nat. Commun. 4:1349.
44. Sandhu, D., Schallock, K. G., Rivera-Velez, N., Lundeen, P., Cianzio, S., and Bhattacharyya, M. K. 2005. Soybean Phytophthora resistance gene Rps8 maps closely to the Rps3 region. J. Hered. 96:536-541. (Pubitemid 41442782)
45. Schuhmacher, T., Lemuth, K., Hardiman, T., Vacun, G., Reuss, M., and Siemann-Herzberg, M. 2010. Quantifying cytosolic messenger RNA concentrations in Escherichia coli using real-time polymerase chain reaction for a systems biology approach. Anal. Biochem. 398:212-217.
46. Shan, W., Cao, M., Leung, D., and Tyler, B. M. 2004. The Avr1b locus of Phytophthora sojae encodes an elicitor and a regulator required for avirulence on soybean plants carrying resistance gene Rps1b. Mol. Plant-Microbe Interact. 17:394-403. (Pubitemid 38398428)
47. Sun, F., Kale, S. D., Azurmendi, H. F., Li, D., Tyler, B. M., and Capelluto, D. G. S. 2013. Structural basis for interactions of the Phytophthora sojae RXLR effector Avh5 with phosphatidylinositol 3-phosphate and for host cell entry. Mol. Plant-Microbe Interact. 26:330-344.
48. Tyler, B. M. 2007. Phytophthora sojae: Root rot pathogen of soybean and model oomycete. Mol. Plant Pathol. 8:1-8. (Pubitemid 46066633)
49. Tyler, B. M. 2008. Genomics of fungal- and oomycete-soybean interactions. Pages 243-267 in: Soybean Genomics. G. Stacey, ed. Springer, New York.
50. Tyler, B. M. 2009. Entering and breaking: Virulence effector proteins of oomycete plant pathogens. Cell. Microbiol. 11:13-20.
51. Tyler, B.M. 2009. Effectors. Pages 361-385 in: Oomycete Genetics and Genomics: Diversity, Interactions and Research Tools, Chapter 18. K. Lamour and S. Kamoun, eds. Wiley-Blackwell, Hoboken, NJ, U.S.A.
52. Tyler, B. M., Forster, H., and Coffey, M. D. 1995. Inheritance of avirulence factors and restriction-fragment-length-polymorphism markers in outcrosses of the oomycete Phytophthora sojae. Mol. Plant-Microbe Interact. 8:515-523.
53. Tyler, B. M., Tripathy, S., Zhang, X., Dehal, P., Jiang, R. H., Aerts, A., Arredondo, F. D., Baxter, L., Bensasson, D., Beynon, J. L., Chapman, J., Damasceno, C. M., Dorrance, A. E., Dou, D., Dickerman, A.W., Dubchak, I. L., Garbelotto, M., Gijzen, M., Gordon, S. G., Govers, F., Grunwald, N.J., Huang, W., Ivors, K. L., Jones, R. W., Kamoun, S., Krampis, K., Lamour, K. H., Lee, M. K., McDonald, W. H., Medina, M., Meijer, H. J., Nordberg, E. K., Maclean, D. J., Ospina-Giraldo, M. D., Morris, P. F., Phuntumart, V., Putnam, N. H., Rash, S., Rose, J. K., Sakihama, Y., Salamov, A. A., Savidor, A., Scheuring, C. F., Smith, B. M., Sobral, B. W., Terry, A., Torto-Alalibo, T. A., Win, J., Xu, Z., Zhang, H., Grigoriev, I. V., Rokhsar, D. S., and Boore, J. L. 2006. Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Science 313:1261-1266. (Pubitemid 44330944)
54. van West, P., Kamoun, S., van 't Klooster, J. W., and Govers, F. 1999. Internuclear gene silencing in Phytophthora infestans. Mol. Cell 3:339-348. (Pubitemid 29290674)
55. Wang, Q., Han, C., Ferreira, A. O., Yu, X., Ye, W., Tripathy, S., Kale, S. D., Gu, B., Sheng, Y., Sui, Y., Wang, X., Zhang, Z., Cheng, B., Dong, S., Shan, W., Zheng, X., Dou, D., Tyler, B. M., and Wang, Y. 2011. Transcriptional programming and functional interactions within the Phytophthora sojae RXLR effector repertoire. Plant Cell 23:2064-2086.
56. Whisson, S. C., Drenth, A., Maclean, D. J., and Irwin, J. A. 1994. Evidence for outcrossing in Phytophthora sojae and linkage of a DNA marker to two avirulence genes. Curr. Genet. 27:77-82. (Pubitemid 24368408)
57. Whisson, S. C., Drenth, A., Maclean, D. J., and Irwin, J. A. 1995. Phytophthora sojae avirulence genes, RAPD, and RFLP markers used to construct a detailed genetic linkage map. Mol. Plant-Microbe Interact. 8:988-995. (Pubitemid 3023327)
58. Whisson, S. C., Basnayake, S., Maclean, D. J., Irwin, J. A. G., and Drenth, A. 2004. Phytophthora sojae avirulence genes Avr4 and Avr6 are located in a 24kb, recombination-rich region of genomic DNA. Fungal Genet. Biol. 41:62-74. (Pubitemid 37485670)
59. Wrather, J. A., and Koenning, S. R. 2010. Soybean Disease Loss Estimates for the United States, 1996-2010. University of Missouri Agricultural Experiment Station, Portageville, MI, U.S.A. Published online. http://aes.missouri.edu/ delta/research/soyloss.stm
60. Wu, X.-L., Zhang, B.-Q., Sun, S., Zhao, J.-M., Yang, F., Guo, N., Gai, J.-Y., and Xing, H. 2011. Identification, genetic analysis and mapping of resistance to Phytophthora sojae of Pm28 in soybean. Agric. Sci. China 10:1506-1511.
61. Yu, X., Tang, J., Wang, Q., Ye, W., Tao, K., Duan, S., Lu, C., Yang, X., Dong, S., Zheng, X., and Wang, Y. 2012. The RxLR effector Avh241 from Phytophthora sojae requires plasma membrane localization to induce plant cell death. New Phytol. 196:247-260.
62. Zhou, L., Mideros, S. X., Bao, L., Hanlon, R., Arredondo, F. D., Tripathy, S., Krampis, K., Jerauld, A., Evans, C., St Martin, S. K., Maroof, M. A., Hoeschele, I., Dorrance, A. E., and Tyler, B. M. 2009. Infection and genotype remodel the entire soybean transcriptome. BMC Genomics 10:49.