IBR5 Modulates Temperature-Dependent, R Protein CHS3-Mediated Defense Responses in

English version České info

Resistance (R) genes play central roles in recognizing pathogens and triggering plant defense responses. CHS3 encodes a TIR-NB-LRR-type R protein harboring a C-terminal LIM domain. A point mutation in CHS3 activates the defense response under chilling stress. Here we identified and characterized ibr5-7, a mutant that suppresses the chilling-induced defense responses of chs3-1. We observed that the enhanced defense responses and cell death in the chs3-1 mutant are synergistically dependent on IBR5 and HSP90. IBR5 physically interacts with CHS3, forming a complex with SGT1b/ HSP90. Moreover, IBR5 is also involved in the R-gene resistance mediated by SNC1, RPS4 and RPM1. Thus, IBR5 plays key roles in regulating defense responses mediated by multiple R proteins.

Vyšlo v časopise: IBR5 Modulates Temperature-Dependent, R Protein CHS3-Mediated Defense Responses in. PLoS Genet 11(10): e32767. doi:10.1371/journal.pgen.1005584
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005584

Souhrn

Zdroje

1. Hua J (2013) Modulation of plant immunity by light, circadian rhythm, and temperature. Curr Opin Plant Biol 16: 406–413. doi: 10.1016/j.pbi.2013.06.017 23856082

2. Alcazar R, Garcia AV, Parker JE, Reymond M (2009) Incremental steps toward incompatibility revealed by Arabidopsis epistatic interactions modulating salicylic acid pathway activation. Proc Natl Acad Sci U S A 106: 334–339. doi: 10.1073/pnas.0811734106 19106299

3. de Jong CF, Takken FL, Cai X, de Wit PJ, Joosten MH (2002) Attenuation of Cf-mediated defense responses at elevated temperatures correlates with a decrease in elicitor-binding sites. Mol Plant Microbe Interact 15: 1040–1049. 12437302

4. Li Y, Pennington BO, Hua J (2009) Multiple R-like genes are negatively regulated by BON1 and BON3 in Aarabidopsis. Mol Plant Microbe Interact 22: 840–848. doi: 10.1094/MPMI-22-7-0840 19522566

5. Xiao S, Charoenwattana P, Holcombe L, Turner JG (2003) The Arabidopsis genes RPW8.1 and RPW8.2 confer induced resistance to powdery mildew diseases in tobacco. Mol Plant Microbe Interact 16: 289–294. 12744457

6. Yang S, Hua J (2004) A haplotype-specific Resistance gene regulated by BONZAI1 mediates temperature-dependent growth control in Arabidopsis. Plant Cell 16: 1060–1071. 15031411

7. Huang X, Li J, Bao F, Zhang X, Yang S (2010) A gain-of-function mutation in the Arabidopsis disease resistance gene RPP4 confers sensitivity to low temperature. Plant Physiol 154: 796–809. doi: 10.1104/pp.110.157610 20699401

8. Wang Y, Zhang Y, Wang Z, Zhang X, Yang S (2013) A missense mutation in CHS1, a TIR-NB protein, induces chilling sensitivity in Arabidopsis. Plant J 75: 553–565. doi: 10.1111/tpj.12232 23651299

9. Cheng C, Gao X, Feng B, Sheen J, Shan L, et al. (2013) Plant immune response to pathogens differs with changing temperatures. Nat Commun 4: 2530. doi: 10.1038/ncomms3530 24067909

10. Kadota Y, Shirasu K (2012) The HSP90 complex of plants. Biochim Biophys Acta 1823: 689–697. doi: 10.1016/j.bbamcr.2011.09.016 22001401

11. Hubert DA, Tornero P, Belkhadir Y, Krishna P, Takahashi A, et al. (2003) Cytosolic HSP90 associates with and modulates the Arabidopsis RPM1 disease resistance protein. EMBO J 22: 5679–5689. 14592967

12. Liu Y, Burch-Smith T, Schiff M, Feng S, Dinesh-Kumar SP (2004) Molecular chaperone Hsp90 associates with resistance protein N and its signaling proteins SGT1 and Rar1 to modulate an innate immune response in plants. J Biol Chem 279: 2101–2108. 14583611

13. Zhang Y, Dorey S, Swiderski M, Jones JD (2004) Expression of RPS4 in tobacco induces an AvrRps4-independent HR that requires EDS1, SGT1 and HSP90. Plant J 40: 213–224. 15447648

14. Holt BF 3rd, Belkhadir Y, Dangl JL (2005) Antagonistic control of disease resistance protein stability in the plant immune system. Science 309: 929–932. 15976272

15. Li Y, Li S, Bi D, Cheng YT, Li X, et al. (2010) SRFR1 negatively regulates plant NB-LRR resistance protein accumulation to prevent autoimmunity. PLoS Pathog 6: e1001111. doi: 10.1371/journal.ppat.1001111 20862316

16. Huang S, Monaghan J, Zhong X, Lin L, Sun T, et al. (2014) HSP90s are required for NLR immune receptor accumulation in Arabidopsis. Plant J 79: 427–439. doi: 10.1111/tpj.12573 24889324

17. Li Y, Tessaro MJ, Li X, Zhang Y (2010) Regulation of the expression of plant resistance gene SNC1 by a protein with a conserved BAT2 domain. Plant Physiol 153: 1425–1434. doi: 10.1104/pp.110.156240 20439546

18. Zhang Y, Li X (2005) A putative nucleoporin 96 Is required for both basal defense and constitutive resistance responses mediated by suppressor of npr1-1,constitutive 1. Plant Cell 17: 1306–1316. 15772285

19. Cheng YT, Germain H, Wiermer M, Bi D, Xu F, et al. (2009) Nuclear pore complex component MOS7/Nup88 is required for innate immunity and nuclear accumulation of defense regulators in Arabidopsis. Plant Cell 21: 2503–2516. doi: 10.1105/tpc.108.064519 19700630

20. Zhu Z, Xu F, Zhang Y, Cheng YT, Wiermer M, et al. (2010) Arabidopsis resistance protein SNC1 activates immune responses through association with a transcriptional corepressor. Proc Natl Acad Sci U S A 107: 13960–13965. doi: 10.1073/pnas.1002828107 20647385

21. Huang Y, Minaker S, Roth C, Huang S, Hieter P, et al. (2014) An E4 ligase facilitates polyubiquitination of plant immune receptor resistance proteins in Arabidopsis. Plant Cell 26: 485–496. doi: 10.1105/tpc.113.119057 24449689

22. Cheng YT, Li Y, Huang S, Huang Y, Dong X, et al. (2011) Stability of plant immune-receptor resistance proteins is controlled by SKP1-CULLIN1-F-box (SCF)-mediated protein degradation. Proc Natl Acad Sci U S A 108: 14694–14699. doi: 10.1073/pnas.1105685108 21873230

23. Yang H, Shi Y, Liu J, Guo L, Zhang X, et al. (2010) A mutant CHS3 protein with TIR-NB-LRR-LIM domains modulates growth, cell death and freezing tolerance in a temperature-dependent manner in Arabidopsis. Plant J 63: 283–296. doi: 10.1111/j.1365-313X.2010.04241.x 20444230

24. Bi D, Johnson K, Huang Y, Zhu Z, Li X, et al. (2011) Mutations in an atypical TIR-NB-LRR-LIM resistance protein confers autoimmunity. Front Plant Sci: doi: 10.3389/fpls.2011.00071

25. Austin MJ, Muskett P, Kahn K, Feys BJ, Jones JD, et al. (2002) Regulatory role of SGT1 in early R gene-mediated plant defenses. Science 295: 2077–2080. 11847308

26. Shirasu K, Lahaye T, Tan MW, Zhou F, Azevedo C, et al. (1999) A novel class of eukaryotic zinc-binding proteins is required for disease resistance signaling in barley and development in C. elegans. Cell 99: 355–366. 10571178

27. Tornero P, Merritt P, Sadanandom A, Shirasu K, Innes RW, et al. (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. 12034893

28. Monroe-Augustus M, Zolman BK, Bartel B (2003) IBR5, a dual-specificity phosphatase-like protein modulating auxin and abscisic acid responsiveness in Arabidopsis. Plant Cell 15: 2979–2991. 14630970

29. Lee JS, Wang S, Sritubtim S, Chen JG, Ellis BE (2009) Arabidopsis mitogen-activated protein kinase MPK12 interacts with the MAPK phosphatase IBR5 and regulates auxin signaling. Plant J 57: 975–985. doi: 10.1111/j.1365-313X.2008.03741.x 19000167

30. Strader LC, Monroe-Augustus M, Bartel B (2008) The IBR5 phosphatase promotes Arabidopsis auxin responses through a novel mechanism distinct from TIR1-mediated repressor degradation. BMC Plant Biol 8: 41. doi: 10.1186/1471-2229-8-41 18423007

31. Pearl LH, Prodromou C (2006) Structure and mechanism of the Hsp90 molecular chaperone machinery. Annu Rev Biochem 75: 271–294. 16756493

32. Bao F, Huang X, Zhu C, Zhang X, Li X, et al. (2014) Arabidopsis HSP90 protein modulates RPP4-mediated temperature-dependent cell death and defense responses. New Phytol 202: 1320–1334. doi: 10.1111/nph.12760 24611624

33. Liu Y, Burch-Smith T, Schiff M, Feng S, Dinesh-Kumar SP (2004) Molecular chaperone Hsp90 associates with resistance protein N and its signaling proteins SGT1 and Rar1 to modulate an innate immune response in plants. J Biol Chem 279: 2101–2108. 14583611

34. Takahashi A, Casais C, Ichimura K, Shirasu K (2003) HSP90 interacts with RAR1 and SGT1 and is essential for RPS2-mediated disease resistance in Arabidopsis. Proc Natl Acad Sci U S A 100: 11777–11782. 14504384

35. Kadota Y, Amigues B, Ducassou L, Madaoui H, Ochsenbein F, et al. (2008) Structural and functional analysis of SGT1-HSP90 core complex required for innate immunity in plants. EMBO Rep 9: 1209–1215. doi: 10.1038/embor.2008.185 18833289

36. Schumacher RJ, Hansen WJ, Freeman BC, Alnemri E, Litwack G, et al. (1996) Cooperative action of Hsp70, Hsp90, and DnaJ proteins in protein renaturation. Biochemistry 35: 14889–14898. 8942653

37. Shaknovich R, Shue G, Kohtz DS (1992) Conformational activation of a basic helix-loop-helix protein (MyoD1) by the C-terminal region of murine HSP90 (HSP84). Mol Cell Biol 12: 5059–5068. 1406681

38. Zhang Y, Goritschnig S, Dong X, Li X (2003) A gain-of-function mutation in a plant disease resistance gene leads to constitutive activation of downstream signal transduction pathways in suppressor of npr1-1, constitutive 1. Plant Cell 15: 2636–2646. 14576290

39. Williams SJ, Sohn KH, Wan L, Bernoux M, Sarris PF, et al. (2014) Structural basis for assembly and function of a heterodimeric plant immune receptor. Science 344: 299–303. doi: 10.1126/science.1247357 24744375

40. Dickinson RJ, Keyse SM (2006) Diverse physiological functions for dual-specificity MAP kinase phosphatases. J Cell Sci 119: 4607–4615. 17093265

41. Bartels S, Gonzalez Besteiro MA, Lang D, Ulm R (2010) Emerging functions for plant MAP kinase phosphatases. Trends Plant Sci 15: 322–329. doi: 10.1016/j.tplants.2010.04.003 20452268

42. Bartels S, Anderson JC, Gonzalez Besteiro MA, Carreri A, Hirt H, et al. (2009) MAP kinase phosphatase1 and protein tyrosine phosphatase1 are repressors of salicylic acid synthesis and SNC1-mediated responses in Arabidopsis. Plant Cell 21: 2884–2897. doi: 10.1105/tpc.109.067678 19789277

43. Ulm R, Ichimura K, Mizoguchi T, Peck SC, Zhu T, et al. (2002) Distinct regulation of salinity and genotoxic stress responses by Arabidopsis MAP kinase phosphatase 1. EMBO J 21: 6483–6493. 12456655

44. Anderson JC, Bartels S, Gonzalez Besteiro MA, Shahollari B, Ulm R, et al. (2011) Arabidopsis MAP Kinase Phosphatase 1 (AtMKP1) negatively regulates MPK6-mediated PAMP responses and resistance against bacteria. Plant J 67: 258–268. doi: 10.1111/j.1365-313X.2011.04588.x 21447069

45. Lumbreras V, Vilela B, Irar S, Sole M, Capellades M, et al. (2010) MAPK phosphatase MKP2 mediates disease responses in Arabidopsis and functionally interacts with MPK3 and MPK6. Plant J 63: 1017–1030. doi: 10.1111/j.1365-313X.2010.04297.x 20626661

46. Vilela B, Pages M, Lumbreras V (2010) Regulation of MAPK signaling and cell death by MAPK phosphatase MKP2. Plant Signal Behav 5: 1497–1500. 21057191

47. Lim CW, Luan S, Lee SC (2014) A prominent role for RCAR3-mediated ABA signaling in response to Pseudomonas syringae pv. tomato DC3000 infection in Arabidopsis. Plant Cell Physiol 55: 1691–1703. doi: 10.1093/pcp/pcu100 25063782

48. Mang HG, Qian W, Zhu Y, Qian J, Kang HG, et al. (2012) Abscisic acid deficiency antagonizes high-temperature inhibition of disease resistance through enhancing nuclear accumulation of resistance proteins SNC1 and RPS4 in Arabidopsis. Plant Cell 24: 1271–1284. doi: 10.1105/tpc.112.096198 22454454

49. Mosher S, Moeder W, Nishimura N, Jikumaru Y, Joo SH, et al. (2010) The lesion-mimic mutant cpr22 shows alterations in abscisic acid signaling and abscisic acid insensitivity in a salicylic acid-dependent manner. Plant Physiol 152: 1901–1913. doi: 10.1104/pp.109.152603 20164209

50. Xu X, Chen C, Fan B, Chen Z (2006) Physical and functional interactions between pathogen-induced Arabidopsis WRKY18, WRKY40, and WRKY60 transcription factors. Plant Cell 18: 1310–1326. 16603654

51. Swiderski MR, Birker D, Jones JD (2009) The TIR domain of TIR-NB-LRR resistance proteins is a signaling domain involved in cell death induction. Mol Plant Microbe Interact 22: 157–165. doi: 10.1094/MPMI-22-2-0157 19132868

52. Bernoux M, Ve T, Williams S, Warren C, Hatters D, et al. (2011) Structural and functional analysis of a plant resistance protein TIR domain reveals interfaces for self-association, signaling, and autoregulation. Cell Host Microbe 9: 200–211. doi: 10.1016/j.chom.2011.02.009 21402359

53. Feys BJ, Parker JE (2000) Interplay of signaling pathways in plant disease resistance. Trends Genet 16: 449–455. 11050331

54. Caplan JL, Mamillapalli P, Burch-Smith TM, Czymmek K, Dinesh-Kumar SP (2008) Chloroplastic protein NRIP1 mediates innate immune receptor recognition of a viral effector. Cell 132: 449–462. doi: 10.1016/j.cell.2007.12.031 18267075

55. Burch-Smith TM, Dinesh-Kumar SP (2007) The functions of plant TIR domains. Sci STKE 2007: pe46. 17726177

56. Burch-Smith TM, Schiff M, Caplan JL, Tsao J, Czymmek K, et al. (2007) A novel role for the TIR domain in association with pathogen-derived elicitors. PLoS Biol 5: e68. 17298188

57. Shirasu K (2009) The HSP90-SGT1 chaperone complex for NLR immune sensors. Annu Rev Plant Biol 60: 139–164. doi: 10.1146/annurev.arplant.59.032607.092906 19014346

58. Azevedo C, Betsuyaku S, Peart J, Takahashi A, Noel L, et al. (2006) Role of SGT1 in resistance protein accumulation in plant immunity. EMBO J 25: 2007–2016. 16619029

59. Bieri S, Mauch S, Shen QH, Peart J, Devoto A, et al. (2004) RAR1 positively controls steady state levels of barley MLA resistance proteins and enables sufficient MLA6 accumulation for effective resistance. Plant Cell 16: 3480–3495. 15548741

60. Leister RT, Dahlbeck D, Day B, Li Y, Chesnokova O, et al. (2005) Molecular genetic evidence for the role of SGT1 in the intramolecular complementation of Bs2 protein activity in Nicotiana benthamiana. Plant Cell 17: 1268–1278. 15749757

61. de la Fuente van Bentem S, Vossen JH, de Vries KJ, van Wees S, Tameling WI, et al. (2005) Heat shock protein 90 and its co-chaperone protein phosphatase 5 interact with distinct regions of the tomato I–2 disease resistance protein. Plant J 43: 284–298. 15998314

62. He Y, Chung EH, Hubert DA, Tornero P, Dangl JL (2012) Specific missense alleles of the arabidopsis jasmonic acid co-receptor COI1 regulate innate immune receptor accumulation and function. PLoS Genet 8: e1003018. doi: 10.1371/journal.pgen.1003018 23093946

63. Kitagawa K, Skowyra D, Elledge SJ, Harper JW, Hieter P (1999) SGT1 encodes an essential component of the yeast kinetochore assembly pathway and a novel subunit of the SCF ubiquitin ligase complex. Mol Cell 4: 21–33. 10445024

64. Gray WM, Muskett PR, Chuang HW, Parker JE (2003) Arabidopsis SGT1b is required for SCF(TIR1)-mediated auxin response. Plant Cell 15: 1310–1319. 12782725

65. Gou M, Shi Z, Zhu Y, Bao Z, Wang G, et al. (2012) The F-box protein CPR1/CPR30 negatively regulates R protein SNC1 accumulation. Plant J 69: 411–420. doi: 10.1111/j.1365-313X.2011.04799.x 21967323

66. Cheng YT, Li Y, Huang S, Huang Y, Dong X, et al. (2011) Stability of plant immune-receptor resistance proteins is controlled by SKP1-CULLIN1-F-box (SCF)-mediated protein degradation. Proc Natl Acad Sci U S A 108: 14694–14699. doi: 10.1073/pnas.1105685108 21873230

67. Consortium AIM (2011) Evidence for network evolution in an Arabidopsis interactome map. Science 333: 601–607. doi: 10.1126/science.1203877 21798944

68. Jirage D, Tootle TL, Reuber TL, Frost LN, Feys BJ, et al. (1999) Arabidopsis thaliana PAD4 encodes a lipase-like gene that is important for salicylic acid signaling. Proc Natl Acad Sci U S A 96: 13583–13588. 10557364

69. Bowling SA, Clarke JD, Liu Y, Klessig DF, Dong X (1997) The cpr5 mutant of Arabidopsis expresses both NPR1-dependent and NPR1-independent resistance. Plant Cell 9: 1573–1584. 9338960

70. Thordal-Christensen H, Zhang Z, Wei Y, Collinge DB (1997) Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J 11: 1187–1194.

71. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735–743. 10069079

72. Walter M, Chaban C, Schutze K, Batistic O, Weckermann K, et al. (2004) Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. Plant J 40: 428–438. 15469500

73. Chen H, Zou Y, Shang Y, Lin H, Wang Y, et al. (2008) Firefly luciferase complementation imaging assay for protein-protein interactions in plants. Plant Physiol 146: 368–376. 18065554

74. Buchner J, Grallert H, Jakob U (1998) Analysis of chaperone function using citrate synthase as nonnative substrate protein. Methods Enzymol 290: 323–338. 9534173

75. Yoo SD, Cho YH, Sheen J (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc 2: 1565–1572. 17585298