GmRIN4 protein family members function nonredundantly in soybean race-specific resistance against Pseudomonas syringae

New Phytologist

Volumn 197, Issue 4, 2013, Pages 1225-1235

  Selote, Devarshi ^a   Robin, Guillaume P ^a   Kachroo, Aardra ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

Author keywords

AvrB; Bacterial blight; Pseudomonas syringae; Resistance protein; RIN4; Soybean (Glycine max)

Indexed keywords

AVRB PROTEIN, PSEUDOMONAS SYRINGAE; BACTERIAL PROTEIN; VEGETABLE PROTEIN;

BACTERIAL DISEASE; DISEASE RESISTANCE; GENE EXPRESSION; HERB; HOST-PATHOGEN INTERACTION; INHIBITION; MOLECULAR ANALYSIS; PROTEIN; SOYBEAN;

ARTICLE; DISEASE RESISTANCE; GENETICS; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; PHOSPHORYLATION; PHYSIOLOGY; PLANT DISEASE; PSEUDOMONAS SYRINGAE; SOYBEAN;

BACTERIAL PROTEINS; DISEASE RESISTANCE; PHOSPHORYLATION; PLANT DISEASES; PLANT PROTEINS; PSEUDOMONAS SYRINGAE; SOYBEANS;

BACTERIA (MICROORGANISMS); GLYCINE MAX; NICOTIANA BENTHAMIANA; PSEUDOMONAS SYRINGAE;

EID: 84873270121     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12093     Document Type: Article

References (42)

1. Ashfield T, Bocian A, Held D, Henk AD, Marek LF, Danesh D, Peñuela S, Meksem K, Lightfoot DA, Young ND, et al. 2003. Genetic and physical localization of the soybean Rpg1-b disease resistance gene reveals a complex locus containing several tightly linked families of NBS-LRR genes. Molecular Plant-Microbe Interactions 16: 817-826.
2. Ashfield T, Ong LE, Nobuta K, Schneider CM, Innes RW. 2004. Convergent evolution of disease resistance gene specificity in two flowering plant families. Plant Cell 16: 309-318.
3. Axtell MJ, Staskawicz BJ. 2003. Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4. Cell 112: 369-377.
4. Belkhadir Y, Nimchuk Z, Hubert DA, Mackey D, Dangl JL. 2004. Arabidopsis RIN4 negatively regulates disease resistance mediated by RPS2 and RPM1 downstream or independent of the NDR1 signal modulator and is not required for the virulence functions of bacterial type III effectors AvrRpt2 or AvrRpm1. Plant Cell 16: 2822-2835.
5. Bisgrove SR, Simonich MT, Smith NM, Sattler A, Innes RW. 1994. A disease resistance gene in Arabidopsis with specificity for two different pathogen avirulence genes. Plant Cell 6: 927-933.
6. Buzzell RI, Tu JC. 1984. Inheritance of soybean resistance to soybean mosaic virus. Journal of Heredity 75: 82.
7. Chung EH, da Cunha L, Wu AJ, Gao Z, Cherkis K, Afzal AJ, Mackey D, Dangl JL. 2011. Specific threonine phosphorylation of a host target by two unrelated type III effectors activates a host innate immune receptor in plants. Cell Host and Microbe 9: 125-136.
8. Debener T, Lehnackers H, Arnold M, Dangl JL. 1991. Identification and molecular mapping of a single Arabidopsis thaliana locus determining resistance to a phytopathogenic Pseudomonas syringae isolate. Plant Journal 1: 289-302.
9. Farrington JA, Ebert M, Land EJ, Fletcher K. 1973. Bipyridylium quaternary salts and related compounds. V. Pulse radiolysis studies of the reaction of paraquat radical with oxygen: implications for the mode of action of bipyridyl herbicides. Biochimica et Biophysica Acta 314: 372-381.
10. Flor H. 1971. Current status of gene-for-gene concept. Annual Review of Phytopathology 9: 275-296.
11. Fu DQ, Ghabrial S, Kachroo A. 2009. GmRAR1 and GmSGT1 are required for basal, R gene-mediated and systemic acquired resistance in soybean. Molecular Plant-Microbe Interactions 22: 86-95.
12. Gijzen M, MacGregor T, Bhattacharyya M, Buzzell R. 1996. Temperature induced susceptibility to Phytophthora sojae in soybean isolines carrying different Rps genes. Physiological and Molecular Plant Pathology 48: 209-215.
13. Gomez AB, Vrebalov J, Moffett P, Mueller LA, Martin GB. 2012. A draft genome sequence of Nicotiana benthamiana and web-based tools for its use in plant-microbe biology research. Molecular Plant-Microbe Interactions 25: 1523-1530.
14. Grant MR, Godiard L, Straube E, Ashfield T, Lewald J, Sattler A, Innes RW, Dangl JL. 1995. Structure of the Arabidopsis RPM1 gene enabling dual specificity disease resistance. Science 269: 843-846.
15. Hiyama T, Ohinata A, Kobayashi S. 1993. Paraquat (methylviologen): its interference with primary photochemical reactions. Zeitschrift für Naturforschung 48c: 374-378.
16. Holliday MJ, Keen NT, Long M. 1981. Cell death patterns and accumulation of fluorescent material in the hypersensitive response of soybean leaves to Pseudomonas syringae pv. glycinea. Physiological Plant Pathology 18: 279-287.
17. Innes RW, Bisgrove SR, Smith NM, Bent AF, Staskawicz BJ, Liu YC. 1993. Identification of a disease resistance locus in Arabidopsis that is functionally homologous to the RPG1 locus of soybean. Plant Journal 4: 813-820.
18. Kachroo A, Fu DQ, Havens W, Navarre D, Kachroo P, Ghabrial SA. 2008. An oleic acid-mediated pathway induces constitutive defense signaling and enhanced resistance to multiple pathogens in soybean. Molecular Plant-Microbe Interactions 21: 564-575.
19. Keen NT, Buzzell RI. 1991. New disease resistance genes in soybean against Pseudomonas syringae pv. glycinea: evidence that one of them interacts with a bacterial elicitor. Theoretical and Applied Genetics 81: 133-138.
20. Keen NT, Holliday MJ. 1982. Recognition of bacterial pathogens by plants. In: Mount MS, Lacey GH, eds. Phytopathogenic procaryotes, vol II. New York, NY, USA: Academic Press, Inc., 179-217.
21. Keen NT, Tamaki S, Kobayashi D, Gerhold D, Stayton M, Shen H, Gold S, Lorang J, Thordal-Christensen H, Dahlbeck D, et al. 1990. Bacteria expressing avirulence gene D produce a specific elicitor of the soybean hypersensitive reaction. Molecular Plant-Microbe Interactions 3: 112-121.
22. Keen NT, Tamaki S, Kobayashi D, Trollinger D. 1988. Improved broad-host-range plasmids for DNA cloning in gram-negative bacteria. Gene 70: 191-197.
23. Keith LW, Boyd C, Keen NT, Partridge JE. 1997. Comparison of avrD alleles from Pseudomonas syringae pv. glycinea. Molecular Plant-Microbe Interactions 10: 416-422.
24. Kobayashi DY, Tamaki SJ, Keen NT. 1990a. Molecular characterization of avirulence gene D from Pseudomonas syringae pv. tomato. Molecular Plant-Microbe Interactions 3: 94-102.
25. Kobayashi DY, Tamaki SJ, Trollinger DJ, Gold S, Keen NT. 1990b. A gene from Pseudomonas syringae pv. glycinea with homology to avirulence gene D from P. s. pv. tomato but devoid of the avirulence phenotype. Molecular Plant-Microbe Interactions 3: 103-111.
26. Lim SM. 1985. Resistance to soybean mosaic virus in soybeans. Phytopathology 75: 199-201.
27. Lindeberg M, Stavrinides J, Chang JH, Alfano JR, Collmer A, Dangl JL, Greenberg JT, Mansfield JW, Guttman DS. 2005. Unified nomenclature and phylogenetic analysis of extracellular proteins delivered by the type III secretion system of the plant pathogenic bacterium Pseudomonas syringae. Molecular Plant-Microbe Interactions 18: 275-282.
28. Liu J, Elmore JM, Fuglsang AT, Palmgren MG, Staskawicz BJ, Coaker G. 2009. RIN4 functions with plasma membrane H + -ATPases to regulate stomatal apertures during pathogen attack. PLoS Biology 7: e1000139.
29. Liu J, Elmore JM, Lin ZJ, Coaker G. 2011. A receptor-like cytoplasmic kinase phosphorylates the host target RIN4, leading to the activation of a plant innate immune receptor. Cell Host and Microbe 9: 137-146.
30. Mackey D, Belkhadir Y, Alfonso JM, Ecker JR, Dangl JL. 2003. Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell 112: 379-389.
31. Mackey D, Holt BF 3rd, Wiig A, Dangl JL. 2002. RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell 108: 743-754.
32. Martin K, Kopperud K, Chakrabarty R, Banerjee R, Brooks R, Goodin MM. 2009. Transient expression in Nicotiana benthamiana fluorescent marker lines provides enhanced definition of protein localization, movement and interactions in planta. Plant Journal 59: 150-162.
33. Napoli C, Staskawicz B. 1987. Molecular characterization and nucleic acid sequence of an avirulence gene from race 6 of Pseudomonas syringae pv. glycinea. Journal of Bacteriology 169: 572-578.
34. Selote D, Kachroo A. 2010a. RPG1-B-derived resistance to AvrB-expressing Pseudomonas syringae requires RIN4-like proteins in soybean. Plant Physiology 153: 1199-1211.
35. Selote D, Kachroo A. 2010b. RIN4-like proteins mediate resistance protein-derived soybean defense against Pseudomonas syringae. Plant Signaling and Behavior 5: 1453-1456.
36. Staskawicz B, Dahlbeck D, Keen N. 1984. Cloned avirulence gene of Pseudomonas syringae pv. glycinea determines race-specific incompatibility on Glycine max (L.) Merr. Proceedings of the National Academy of Sciences, USA 81: 6024-6028.
37. Staskawicz B, Dahlbeck D, Keen N, Napoli C. 1987. Molecular characterization of cloned avirulence genes from race 0 and race 1 of Pseudomonas syringae pv. glycinea. Journal of Bacteriology 0169: 5789-5794.
38. Tamaki S, Dahlbeck D, Staskawicz B, Keen NT. 1988. Characterization and expression of two avirulence genes cloned from Pseudomonas syringae pv. glycinea. Journal of Bacteriology 170: 4846-4854.
39. Tornero P, Merritt P, Sadanandom A, Shirasu K, Innes RW, Dangl JL. 2002. RAR1 and NDR1 contribute quantitatively to disease resistance in Arabidopsis, and their relative contributions are dependent on the R gene assayed. Plant Cell 14: 1005-1015.
40. Torp J, Jorgensen JH. 1986. Modification of barley powdery mildew resistance gene Mla12 by induced mutation. Canadian Journal of Genetics and Cytology 28: 725-731.
41. Whisson SC, Drenth A, Maclean DJ, Irwin JAG. 1995. Phytophthora sojae avirulence genes, RAPD, and RFLP markers used to construct a detailed genetic linkage map. Molecular Plant-Microbe Interactions 8: 988-995.
42. Zhang C, Ghabrial SA. 2006. Development of Bean pod mottle virus-based vectors for stable protein expression and sequence-specific virus-induced gene silencing in soybean. Virology 344: 401-411.