Phytophthora suppressor of RNA silencing 2 is a conserved RxLR effector that promotes infection in soybean and Arabidopsis thaliana

Molecular Plant-Microbe Interactions

Volumn 27, Issue 12, 2014, Pages 1379-1389

  Xiong, Qin ^a,b   Ye, Wenwu ^a   Choi, Duseok ^b   Wong, James ^b   Qiao, Yongli ^b,c   Tao, Kai ^a   Wang, Yuanchao ^a   Ma, Wenbo ^b,c  

^a NANJING AGRICULTURAL UNIVERSITY   (China)

^b Department of Plant Pathology and Microbiology ^*  (China)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS THALIANA; GLYCINE MAX; PHYTOPHTHORA;

HYBRID PROTEIN; SALICYLIC ACID; VIRULENCE FACTOR;

ARABIDOPSIS; COTYLEDON; CYTOLOGY; DISEASE PREDISPOSITION; DNA SEQUENCE; GENE EXPRESSION; GENETICS; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PHYLOGENY; PHYTOPHTHORA; PLANT DISEASE; PLANT LEAF; PLANT ROOT; PLANT STEM; REPORTER GENE; RNA INTERFERENCE; SOYBEAN;

ARABIDOPSIS; COTYLEDON; DISEASE SUSCEPTIBILITY; GENE EXPRESSION; GENES, REPORTER; PHYLOGENY; PHYTOPHTHORA; PLANT DISEASES; PLANT LEAVES; PLANT ROOTS; PLANT STEMS; RECOMBINANT FUSION PROTEINS; RNA INTERFERENCE; SALICYLIC ACID; SEQUENCE ANALYSIS, DNA; SOYBEANS; VIRULENCE FACTORS;

EID: 84910598873     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-06-14-0190-R     Document Type: Article

References (75)

1. Anderson, R. G., Casady, M. S., Fee, R. A., Vaughan, M. M., Deb, D., Fedkenheuer, K., Huffaker, A., Schmelz, E. A., Tyler, B. M., and McDowell, J. M. 2012. Homologous RXLR effectors from Hyaloperonospora arabidopsidis and Phytophthora sojae suppress immunity in distantly related plants. Plant J. 72:882-893.
2. Baxter, L., Tripathy, S., Ishaque, N., Boot, N., Cabral, A., Kemen, E., Thines, M., Ah-Fong, A., Anderson, R., Badejoko, W., Bittner-Eddy, P., Boore, J. L., Chibucos, M. C., Coates, M., Dehal, P., Delehaunty, K., Dong, S., Downton, P., Dumas, B., Fabro, G., Fronick, C., Fuerstenberg, S. I., Fulton, L., Gaulin, E., Govers, F., Hughes, L., Humphray, S., Jiang, R. H., Judelson, H., Kamoun, S., Kyung, K., Meijer, H., Minx, P., Morris, P., Nelson, J., Phuntumart, V., Qutob, D., Rehmany, A., Rougon-Cardoso, A., Ryden, P., Torto-Alalibo, T., Studholme, D., Wang, Y., Win, J., Wood, J., Clifton, S. W., Rogers, J., Van den Ackerveken, G., Jones, J. D., McDowell, J. M., Beynon, J., and Tyler, B. M. 2010. Signatures of adaptation to obligate biotrophy in the Hyaloperonospora arabidopsidis genome. Science 330:1549-1551.
3. Bhattacharjee, S., Hiller, N. L., Liolios, K., Win, J., Kanneganti, T. D., Young, C., Kamoun, S., and Haldar, K. 2006. The malarial host-targeting signal is conserved in the Irish potato famine pathogen. PLoS Pathog. 2:e50.
4. Birch, P. R., Rehmany, A. P., Pritchard, L., Kamoun, S., and Beynon, J. L. 2006. Trafficking arms: Oomycete effectors enter host plant cells. Trends Microbiol. 14:8-11.
5. Birch, P. R., Boevink, P. C., Gilroy, E. M., Hein, I., Pritchard, L., and Whisson, S. C. 2008. Oomycete RXLR effectors: Delivery, functional redundancy and durable disease resistance. Curr. Opin. Plant Biol. 11:373-379.
6. Boccara, M., Sarazin, A., Thiebeauld, O., Jay, F., Voinnet, O., Navarro, L., and Colot, V. 2014. The Arabidopsis miR472-RDR6 silencing pathway modulates PAMP- and effector-triggered immunity through the posttranscriptional control of disease resistance genes. PLoS Pathog. 10:e1003883.
7. Boller, T., and Felix, G. 2009. A renaissance of elicitors: Perception of microbe-associated molecular patterns and danger signals by patternrecognition receptors. Annu. Rev. Plant Biol. 60:379-406.
8. Boller, T., and He, S. Y. 2009. Innate immunity in plants: An arms race between pattern recognition receptors in plants and effectors in microbial pathogens. Science 324:742-744.
9. Bonas, U. 1994. hrp genes of phytopathogenic bacteria. Curr. Top. Microbiol. Immunol. 192:79-98.
10. Bos, J. I., Kanneganti, T. D., Young, C., Cakir, C., Huitema, E., Win, J., Armstrong, M. R., Birch, P. R., and Kamoun, S. 2006. The C-terminal half of Phytophthora infestans RXLR effector AVR3a is sufficient to trigger R3a-mediated hypersensitivity and suppress INF1-induced cell death in Nicotiana benthamiana. Plant J. 48:165-176.
11. 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.
12. Bouwmeester, K., de Sain, M., Weide, R., Gouget, A., Klamer, S., Canut, H., and Govers, F. 2011. The lectin receptor kinase LecRK-I. 9 is a novel Phytophthora resistance component and a potential host target for a RXLR effector. PLoS Pathog. 7:e1001327.
13. Bozkurt, T. O., Schornack, S., Win, J., Shindo, T., Ilyas, M., Oliva, R., Cano, L. M., Jones, A. M., Huitema, E., van der Hoorn, R. A., and Kamoun, S. 2011. Phytophthora infestans effector AVRblb2 prevents secretion of a plant immune protease at the haustorial interface. Proc. Natl. Acad. Sci. U.S.A. 108:20832-20837.
14. Brigneti, G., Voinnet, O., Li, W.X., Ji, L. H., Ding, S. W., and Baulcombe, D. C. 1998. Viral pathogenicity determinants are suppressors of transgene silencing in Nicotiana benthamiana. EMBO (Eur. Mol. Biol. Organ.) J. 17:6739-6746.
15. Chen, X. 2010. Small RNAs-Secrets and surprises of the genome. Plant J. 61:941-958.
16. Chisholm, S. T., Coaker, G., Day, B., and Staskawicz, B. J. 2006. Hostmicrobe interactions: Shaping the evolution of the plant immune response. Cell 124:803-814.
17. Dangl, J. L., Horvath, D. M., and Staskawicz, B. J. 2013. Pivoting the plant immune system from dissection to deployment. Science 341:746-751.
18. Dong, S., Yin, W., Kong, G., Yang, X., Qutob, D., Chen, Q., Kale, S. D., Sui, Y., Zhang, Z., and Dou, D. 2011. Phytophthora sojae avirulence effector Avr3b is a secreted NADH and ADP-ribose pyrophosphorylase that modulates plant immunity. PLoS Pathog. 7:e1002353.
19. Dong, S., Stam, R., Cano, L. M., Song, J., Sklenar, J., Yoshida, K., Bozkurt, T. O., Oliva, R., Liu, Z., Tian, M., Win, J., Banfield, M. J., Jones, A. M., van der Hoorn, R. A., and Kamoun, S. 2014. Effector specialization in a lineage of the Irish potato famine pathogen. Science 343:552-555.
20. Dou, D., and Zhou, J. M. 2012. Phytopathogen effectors subverting host immunity: Different foes, similar battleground. Cell Host Microbe 12:484-495.
21. Earley, K. W., Haag, J. R., Pontes, O., Opper, K., Juehne, T., Song, K., and Pikaard, C. S. 2006. Gateway-compatible vectors for plant functional genomics and proteomics. Plant J. 45:616-629.
22. Erwin, D. C., and Ribeiro, O. K. 1996. Phytophthora Diseases Worldwide. American Phytopathological Society, St. Paul, MN, U.S.A.
23. Evangelisti, E., Govetto, B., Minet-Kebdani, N., Kuhn, M. L., Attard, A., Ponchet, M., Panabières, F., and Gourgues, M. 2013. The Phytophthora parasitica RXLR effector penetration-specific effector 1 favours Arabidopsis thaliana infection by interfering with auxin physiology. New Phytol. 199:476-489.
24. Gheysen, G., and Mitchum, M. G. 2011. How nematodes manipulate plant development pathways for infection. Curr. Opin. Plant Biol. 14:415-421.
25. Gilroy, E. M., Taylor, R. M., Hein, I., Boevink, P., Sadanandom, A., and Birch, P. R. J. 2011. CMPG1-dependent cell death follows perception of diverse pathogen elicitors at the host plasma membrane and is suppressed by Phytophthora infestans RXLR effector AVR3a. New Phytol. 190:653-666.
26. Giraldo, M. C., and Valent, B. 2013. Filamentous plant pathogen effectors in action. Nat. Rev. Microbiol. 11:800-814.
27. Haas, B. J., Kamoun, S., Zody, M. C., Jiang, R. H., Handsaker, R. E., Cano, L. M., Grabherr, M., Kodira, C. D., Raffaele, S., Torto-Alalibo, T., Bozkurt, T. O., Ah-Fong, A. M., Alvarado, L., Anderson, V. L., Armstrong, M. R., Avrova, A., Baxter, L., Beynon, J., Boevink, P. C., Bollmann, S. R., Bos, J. I., Bulone, V., Cai, G., Cakir, C., Carrington, J. C., Chawner, M., Conti, L., Costanzo, S., Ewan, R., Fahlgren, N., Fischbach, M. A., Fugelstad, J., Gilroy, E. M., Gnerre, S., Green, P. J., Grenville-Briggs, L. J., Griffith, J., Grunwald, N. J., Horn, K., Horner, N. R., Hu, C. H., Huitema, E., Jeong, D. H., Jones, A. M., Jones, J. D., Jones, R. W., Karlsson, E. K., Kunjeti, S. G., Lamour, K., Liu, Z., Ma, L., Maclean, D., Chibucos, M. C., McDonald, H., McWalters, J., Meijer, H. J., Morgan, W., Morris, P. F., Munro, C. A., O'Neill, K., Ospina-Giraldo, M., Pinzon, A., Pritchard, L., Ramsahoye, B., Ren, Q., Restrepo, S., Roy, S., Sadanandom, A., Savidor, A., Schornack, S., Schwartz, D. C., Schumann, U. D., Schwessinger, B., Seyer, L., Sharpe, T., Silvar, C., Song, J., Studholme, D. J., Sykes, S., Thines, M., van de Vondervoort, P. J., Phuntumart, V., Wawra, S., Weide, R., Win, J., Young, C., Zhou, S., Fry, W., Meyers, B. C., van West, P., Ristaino, J., Govers, F., Birch, P. R., Whisson, S. C., Judelson, H. S., and Nusbaum, C. 2009. Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 461:393-398.
28. Haldar, K., Kamoun, S., Hiller, N.L., Bhattacharje, S., and van Ooij, C. 2006. Common infection strategies of pathogenic eukaryotes. Nat. Rev. Microbiol. 4:922-931.
29. Heese, A., Hann, D. R., Gimenez-Ibanez, S., Jones, A. M. E., He, K., Li, J., Schroeder, J. I., Peck, S. C., and Rathjen, J. P. 2007. The receptorlike kinase SERK3/BAK1 is a central regulator of innate immunity in plants. Proc. Natl. Acad. Sci. U.S.A. 104:12217-12222.
30. Hofgen, R., and Willmitzer, L. 1988. Storage of competent cells for Agrobacterium transformation. Nucleic Acids Res. 16:9877-9877.
31. Jiang, R. H. Y., 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.
32. Jiang, S., Yao, J., Ma, K. W., Zhou, H., Song, J., He, S. Y., and Ma, W. 2013. Bacterial effector activates jasmonate signaling by directly targeting JAZ transcriptional repressors. PLoS Pathog. 9:e1003715.
33. Jones, J. D. G., and Dangl, J. L. 2006. The plant immune system. Nature 444:323-329.
34. Kale, S. D., Gu, B. A., Capelluto, D. G. S., Dou, D. L., Feldman, E., Rumore, A., Arredondo, F. D., Hanlon, R., Fudal, I., Rouxel, T., Lawrence, C. B., Shan, W. X., and Tyler, B. M. 2010. External lipid PI3P mediates entry of eukaryotic pathogen effectors into plant and animal host cells. Cell 142:284-295. (Erratum in Cell 142:981-983)
35. Kereszt, A., Li, D., Indrasumunar, A., Nguyen, C. D., Nontachaiyapoom, S., Kinkema, M., and Gresshoff, P. M. 2007. Agrobacterium rhizogenes-mediated transformation of soybean to study root biology. Nat. Protocols 2:948-952.
36. King, S. R., McLellan, H., Boevink, P. C., Armstrong, M. R., Bukharova, T., Sukarta, O., Win, J., Kamoun, S., Birch, P. R., and Banfield, M. J. 2014. Phytophthora infestans RXLR effector PexRD2 interacts with host MAPKKK epsilon to suppress plant immune signaling. Plant Cell 26:1345-1359.
37. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
38. Lamour, K. H., Stam, R., Jupe, J., and Huitema, E. 2012. The oomycete broad-host-range pathogen Phytophthora capsici. Mol. Plant Pathol. 13:329-337.
39. Li, F., Pignatta, D., Bendix, C., Brunkard, J. O., Cohn, M. M., Tung, J., Sun, H., Kumar, P., and Baker, B. 2012. MicroRNA regulation of plant innate immune receptors. Proc. Natl. Acad. Sci. U.S.A. 109:1790-1795.
40. Lindeberg, M., Cunnac, S., and Collmer, A. 2012. Pseudomonas syringae type III effector repertoires: Last words in endless arguments. Trends Microbiol. 20:199-208.
41. Lu, Y. J., Schornack, S., Spallek, T., Geldner, N., Chory, J., Schellmann, S., Schumacher, K., Kamoun, S., and Robatzek, S. 2012. Patterns of plant subcellular responses to successful oomycete infections reveal differences in host cell reprogramming and endocytic trafficking. Cell Microbiol. 14:682-697.
42. Ma, K. W., Flores, C., and Ma, W. B. 2011. Chromatin configuration as a battlefield in plant-bacteria interactions. Plant Physiol. 157:535-543.
43. Ma, W. B., and Guttman, D. S. 2008. Evolution of prokaryotic and eukaryotic virulence effectors. Curr. Opin. Plant Biol. 11:412-419.
44. Ma, W. B., Dong, F. F. T., Stavrinides, J., and Guttman, D. S. 2006. Type III effector diversification via both pathoadaptation and horizontal transfer in response to a coevolutionary arms race. PLoS Genet. 2:2131-2142.
45. Monaghan, J., and Zipfel, C. 2012. Plant pattern recognition receptor complexes at the plasma membrane. Curr. Opin. Plant Biol. 15:349-357.
46. Morgan, R. L., Zhou, H. B., Lehto, E., Nguyen, N., Bains, A., Wang, X. Q., and Ma, W. B. 2010. Catalytic domain of the diversified Pseudomonas syringae type III effector HopZ1 determines the allelic specificity in plant hosts. Mol. Microbiol. 76:437-455.
47. Pais, M., Win, J., Yoshida, K., Etherington, G. J., Cano, L. M., Raffaele, S., Banfield, M. J., Jones, A., Kamoun, S., and Saunders, D. G. O. 2013. From pathogen genomes to host plant processes: The power of plant parasitic oomycetes. Genome Biol. 14:211.
48. Panstruga, R., and Dodds, P. N. 2009. Terrific protein traffic: The mystery of effector protein delivery by filamentous plant pathogens. Science 324:748-750.
49. Qiao, Y., Liu, L., Xiong, Q., Flores, C., Wong, J., Shi, J., Wang, X., Liu, X., Xiang, Q., Jiang, S., Zhang, F., Wang, Y., Judelson, H. S., Chen, X., and Ma, W. 2013. Oomycete pathogens encode RNA silencing suppressors. Nat. Genet. 45:330-333.
50. Raffaele, S., and Kamoun, S. 2012. Genome evolution in filamentous plant pathogens: Why bigger can be better. Nat. Rev. Microbiol. 10:417-430.
51. Roine, E., Wei, W., Yuan, J., Nurmiaho-Lassila, E. L., Kalkkinen, N., Romantschuk, M., and He, S. Y. 1997. Hrp pilus: An hrp-dependent bacterial surface appendage produced by Pseudomonas syringae pv. tomato DC3000. Proc. Natl. Acad. Sci. U.S.A. 94:3459-3464.
52. Savka, M., Ravillion, B., Noel, G., and Farrand, S. 1990. Induction of hairy roots on cultivated soybean genotypes and their use to propagate the soybean cyst nematode. Phytopathology 80:503-508.
53. Shivaprasad, P. V., Chen, H. M., Patel, K., Bond, D. M., Santos, B. A., and Baulcombe, D. C. 2012. A microRNA superfamily regulates nucleotide binding site-leucine-rich repeats and other mRNAs. Plant Cell 24:859-874.
54. Silvar, C., Duncan, J., Cooke, D., Williams, N., Díaz, J., and Merino, F. 2005. Development of specific PCR primers for identification and detection of Phytophthora capsici Leon. Eur. J. Plant Pathol. 112:43-52.
55. Stassen, J. H. M., and Van den Ackerveken, G. 2011. How do oomycete effectors interfere with plant life? Curr. Opin. Plant Biol. 14:407-414.
56. Stavrinides, J., McCann, H. C., and Guttman, D. S. 2008. Host-pathogen interplay and the evolution of bacterial effectors. Cell Microbiol. 10:285-292.
57. Subramanian, A., Tamayo, P., Mootha, V. K., Mukherjee, S., Ebert, B. L., Gillette, M. A., Paulovich, A., Pomeroy, S. L., Golub, T. R., and Lander, E. S. 2005. Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. U.S.A. 102:15545-15550.
58. Sun, Y., Li, L., Macho, A. P., Han, Z., Hu, Z., Zipfel, C., Zhou, J. M., and Chai, J. 2013. Structural basis for flg22-induced activation of the Arabidopsis FLS2-BAK1 immune complex. Science 342:624-628.
59. Talbot, N. J. 2007. Plant pathology: Deadly special deliveries. Nature 450:41-43.
60. Thines, M., and Kamoun, S. 2010. Oomycete-plant coevolution: Recent advances and future prospects. Curr. Opin. Plant Biol. 13:427-433.
61. Torto-Alalibo, T., Collmer, C. W., Lindeberg, M., Bird, D., Collmer, A., and Tyler, B. M. 2009. Common and contrasting themes in host celltargeted effectors from bacterial, fungal, oomycete and nematode plant symbionts described using the Gene Ontology. BMC Microbiol. 9 (Suppl.)1:S3.
62. Tyler, B. M. 2007. Phytophthora sojae: Root rot pathogen of soybean and model oomycete. Mol. Plant Pathol. 8:1-8.
63. 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.
64. Wang, Q., Han, C., Ferreira, A. O., Yu, X., Ye, W., Tripathy, S., Kale, S. D., Gu, B., Sheng, Y., and Sui, Y. 2011. Transcriptional programming and functional interactions within the Phytophthora sojae RXLR effector repertoire. Plant Cell Online 23:2064-2086.
65. Wang, Y., Bouwmeester, K., van de Mortel, J. E., Shan, W., and Govers, F. 2013a. A novel Arabidopsis-oomycete pathosystem: Differential interactions with Phytophthora capsici reveal a role for camalexin, indole glucosinolates and salicylic acid in defence. Plant Cell Environ. 36:1192-1203.
66. Wang, Y., Bouwmeester, K., van de Mortel, J. E., Shan, W., and Govers, F. 2013b. Induced expression of defense-related genes in Arabidopsis upon infection with Phytophthora capsici. Plant Signal. Behav. 8:e24618.
67. Whisson, S. C., Boevink, P. C., Moleleki, L., Avrova, A. O., Morales, J. G., Gilroy, E. M., Armstrong, M. R., Grouffaud, S., van West, P., Chapman, S., Hein, I., Toth, I. K., Pritchard, L., and Birch, P. R. 2007. A translocation signal for delivery of oomycete effector proteins into host plant cells. Nature 450:115-118.
68. Wildermuth, M. C., Dewdney, J., Wu, G., and Ausubel, F. M. 2001. Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414:562-565.
69. Win, J., Morgan, W., Bos, J., Krasileva, K. V., Cano, L. M., Chaparro-Garcia, A., Ammar, R., Staskawicz, B. J., and Kamoun, S. 2007. Adaptive evolution has targeted the C-terminal domain of the RXLR effectors of plant pathogenic oomycetes. Plant Cell Online 19:2349-2369.
70. Wong, J., Gao, L., Yang, Y., Zhai, J., Arikit, S., Yu, Y., Duan, S., Chan, V., Xiong, Q., Yan, J., Li, S., Liu, R., Wang, Y., Tang, G., Meyers, B. C., Chen, X., and Ma, W. 2014. Roles of small RNAs in soybean defense against Phytophthora sojae infection. Plant J. 79:928-940.
71. Wroblewski, T., Tomczak, A., and Michelmore, R. 2005. Optimization of Agrobacterium-mediated transient assays of gene expression in lettuce, tomato and Arabidopsis. Plant Biotechnol. J. 3:259-273.
72. Zhai, J. X., Jeong, D. H., De Paoli, E., Park, S., Rosen, B. D., Li, Y. P., Gonzalez, A. J., Yan, Z., Kitto, S. L., Grusak, M. A., Jackson, S. A., Stacey, G., Cook, D. R., Green, P. J., Sherrier, D. J., and Meyers, B. C. 2011. MicroRNAs as master regulators of the plant NB-LRR defense gene family via the production of phased, trans-acting siRNAs. Gene Dev. 25:2540-2553.
73. Zhang, M., Lu, J., Tao, K., Ye, W. W., Li, A. N., Liu, X. Y., Kong, L., Dong, S. M., Zheng, X. B., and Wang, Y. C. 2012. A Myb transcription factor of Phytophthora sojae, regulated by MAP kinase PsSAK1, is required for zoospore development. PLoS One 7:e40246.
74. Zhou, H., Lin, J., Johnson, A., Morgan, R. L., Zhong, W., and Ma, W. 2011. Pseudomonas syringae type III effector HopZ1 targets a host enzyme to suppress isoflavone biosynthesis and promote infection in soybean. Cell Host Microbe 9:177-186.
75. Zipfel, C. 2009. Early molecular events in PAMP-triggered immunity. Curr. Opin. Plant Biol. 12:414-420.