Temperature-dependent autoimmunity mediated by chs1 requires its neighboring TNL gene SOC3

New Phytologist

Volumn 213, Issue 3, 2017, Pages 1330-1345

  Zhang, Yao ^a   Wang, Yuancong ^a,b   Liu, Jingyan ^a   Ding, Yanglin ^a   Wang, Shanshan ^c   Zhang, Xiaoyan ^a   Liu, Yule ^c   Yang, Shuhua ^a  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

^b INSTITUTE OF PLANT PROTECTION   (China)

^c TSINGHUA UNIVERSITY   (China)

Author keywords

Arabidopsis; autoimmunity; chilling stress; CHS1; TIR NB protein; TIR NB LRR protein

Indexed keywords

CHROMOSOME; COLD TOLERANCE; GENE EXPRESSION; GENOME; HERB; IMMUNITY; LOW TEMPERATURE; MUTATION; PROTEIN; TEMPERATURE EFFECT;

ARABIDOPSIS;

ARABIDOPSIS PROTEIN; CHS1 PROTEIN, ARABIDOPSIS; IMMUNOGLOBULIN RECEPTOR; PROTEIN BINDING;

AMINO ACID SEQUENCE; ARABIDOPSIS; AUTOIMMUNITY; BIOLOGICAL MODEL; CELL FRACTIONATION; CHEMISTRY; DOWN REGULATION; GAIN OF FUNCTION MUTATION; GENE EXPRESSION REGULATION; GENE REPRESSION; GENETICS; IMMUNOLOGY; LOSS OF FUNCTION MUTATION; METABOLISM; MOLECULAR CLONING; NUCLEOTIDE SEQUENCE; PHENOTYPE; PLANT GENE; SUPPRESSOR GENE; TEMPERATURE;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; AUTOIMMUNITY; BASE SEQUENCE; CLONING, MOLECULAR; DOWN-REGULATION; GAIN OF FUNCTION MUTATION; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GENES, SUPPRESSOR; LOSS OF FUNCTION MUTATION; MODELS, BIOLOGICAL; PHENOTYPE; PROTEIN BINDING; RECEPTORS, IMMUNOLOGIC; SUBCELLULAR FRACTIONS; SUPPRESSION, GENETIC; TEMPERATURE;

EID: 84994877188     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.14216     Document Type: Article

References (61)

1. Aarts N, Metz M, Holub E, Staskawicz BJ, Daniels MJ, Parker JE. 1998. Different requirements for EDS1 and NDR1 by disease resistance genes define at least two R gene-mediated signaling pathways in Arabidopsis. Proceedings of the National Academy of Sciences, USA 95: 10306–10311.
2. Alcazar R, Garcia AV, Parker JE, Reymond M. 2009. Incremental steps toward incompatibility revealed by Arabidopsis epistatic interactions modulating salicylic acid pathway activation. Proceedings of the National Academy of Sciences, USA 106: 334–339.
3. Alcazar R, Parker JE. 2011. The impact of temperature on balancing immune responsiveness and growth in Arabidopsis. Trends in Plant Science 16: 666–675.
4. Bernoux M, Ve T, Williams S, Warren C, Hatters D, Valkov E, Zhang X, Ellis JG, Kobe B, Dodds PN. 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.
5. Bi D, Johnson KC, Zhu Z, Huang Y, Chen F, Zhang Y, Li X. 2011. Mutations in an atypical TIR-NB-LRR-LIM resistance protein confer autoimmunity. Frontiers in Plant Science 2: 71.
6. Bomblies K, Lempe J, Epple P, Warthmann N, Lanz C, Dangl JL, Weigel D. 2007. Autoimmune response as a mechanism for a Dobzhansky-Muller-type incompatibility syndrome in plants. PLoS Biology 5: e236.
7. 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.
8. Cesari S, Bernoux M, Moncuquet P, Kroj T, Dodds PN. 2014. A novel conserved mechanism for plant NLR protein pairs: the “integrated decoy” hypothesis. Frontiers in Plant Science 5: 606.
9. Cesari S, Thilliez G, Ribot C, Chalvon V, Michel C, Jauneau A, Rivas S, Alaux L, Kanzaki H, Okuyama Y et al. 2013. The rice resistance protein pair RGA4/RGA5 recognizes the Magnaporthe oryzae effectors AVR-Pia and AVR1-CO39 by direct binding. Plant Cell 25: 1463–1481.
10. Cheng C, Gao X, Feng B, Sheen J, Shan L, He P. 2013. Plant immune response to pathogens differs with changing temperatures. Nature Communications 4: 2530.
11. Clough SJ, Bent AF. 1998. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant Journal 16: 735–743.
12. Combet C, Blanchet C, Geourjon C, Deleage G. 2000. NPS@: network protein sequence analysis. Trends in Biochemical Sciences 25: 147–150.
13. Cui H, Tsuda K, Parker JE. 2015. Effector-triggered immunity: from pathogen perception to robust defense. Annual Review of Plant Biology 66: 487–511.
14. Diener AC, Li H, Zhou W, Whoriskey WJ, Nes WD, Fink GR. 2000. Sterol methyltransferase 1 controls the level of cholesterol in plants. Plant Cell 12: 853–870.
15. Ding Y, Li H, Zhang X, Xie Q, Gong Z, Yang S. 2015. OST1 kinase modulates freezing tolerance by enhancing ICE1 stability in Arabidopsis. Developmental Cell 32: 278–289.
16. Eitas TK, Dangl JL. 2010. NB-LRR proteins: pairs, pieces, perception, partners, and pathways. Current Opinion in Plant Biology 13: 472–477.
17. Frost D, Way H, Howles P, Luck J, Manners J, Hardham A, Finnegan J, Ellis J. 2004. Tobacco transgenic for the flax rust resistance gene L expresses allele-specific activation of defense responses. Molecular Plant-Microbe Interactions 17: 224–232.
18. Garrett KA, Dendy SP, Frank EE, Rouse MN, Travers SE. 2006. Climate change effects on plant disease: genomes to ecosystems. Annual Review of Phytopathology 44: 489–509.
19. Glazebrook J, Rogers EE, Ausubel FM. 1996. Isolation of Arabidopsis mutants with enhanced disease susceptibility by direct screening. Genetics 143: 973–982.
20. Gray WM, Muskett PR, Chuang HW, Parker JE. 2003. Arabidopsis SGT1b is required for SCF(TIR1)-mediated auxin response. Plant Cell 15: 1310–1319.
21. Hammond-Kosack KE, Jones JD. 1996. Resistance gene-dependent plant defense responses. Plant Cell 8: 1773–1791.
22. Hua J. 2013. Modulation of plant immunity by light, circadian rhythm, and temperature. Current Opinion in Plant Biology 16: 406–413.
23. 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 Physiology 154: 796–809.
24. Hugly S, McCourt P, Browse J, Patterson GW, Somerville C. 1990. A chilling sensitive mutant of Arabidopsis with altered steryl-ester metabolism. Plant Physiology 93: 1053–1062.
25. Jacob F, Vernaldi S, Maekawa T. 2013. Evolution and conservation of plant NLR functions. Frontiers in Immunology 4: 297.
26. Jones JD, Dangl JL. 2006. The plant immune system. Nature 444: 323–329.
27. Krasileva KV, Dahlbeck D, Staskawicz BJ. 2010. Activation of an Arabidopsis resistance protein is specified by the in planta association of its leucine-rich repeat domain with the cognate oomycete effector. Plant Cell 22: 2444–2458.
28. Le Roux C, Huet G, Jauneau A, Camborde L, Tremousaygue D, Kraut A, Zhou B, Levaillant M, Adachi H, Yoshioka H et al. 2015. A receptor pair with an integrated decoy converts pathogen disabling of transcription factors to immunity. Cell 161: 1074–1088.
29. Lee H, Guo Y, Ohta M, Xiong L, Stevenson B, Zhu JK. 2002. LOS2, a genetic locus required for cold-responsive gene transcription encodes a bi-functional enolase. EMBO Journal 21: 2692–2702.
30. Li Y, Pennington BO, Hua J. 2009. Multiple R-like genes are negatively regulated by BON1 and BON3 in arabidopsis. Molecular Plant-Microbe Interactions 22: 840–848.
31. Loutre C, Wicker T, Travella S, Galli P, Scofield S, Fahima T, Feuillet C, Keller B. 2009. Two different CC-NBS-LRR genes are required for Lr10-mediated leaf rust resistance in tetraploid and hexaploid wheat. Plant Journal 60: 1043–1054.
32. Meyers BC, Morgante M, Michelmore RW. 2002. TIR-X and TIR-NBS proteins: two new families related to disease resistance TIR-NBS-LRR proteins encoded in Arabidopsis and other plant genomes. Plant Journal 32: 77–92.
33. Michael Weaver L, Swiderski MR, Li Y, Jones JD. 2006. The Arabidopsis thaliana TIR-NB-LRR R-protein, RPP1A; protein localization and constitutive activation of defence by truncated alleles in tobacco and Arabidopsis. Plant Journal 47: 829–840.
34. Nandety RS, Caplan JL, Cavanaugh K, Perroud B, Wroblewski T, Michelmore RW, Meyers BC. 2013. The role of TIR-NBS and TIR-X proteins in plant basal defense responses. Plant Physiology 162: 1459–1472.
35. Narusaka M, Shirasu K, Noutoshi Y, Kubo Y, Shiraishi T, Iwabuchi M, Narusaka Y. 2009. RRS1 and RPS4 provide a dual Resistance-gene system against fungal and bacterial pathogens. Plant Journal 60: 218–226.
36. Ni M, Cui D, Einstein J, Narasimhulu S, Vergara CE, Gelvin SB. 1995. Strength and tissue specificity of chimeric promoters derived from the octopine and mannopine synthase genes. Plant Journal 7: 661–676.
37. Peart JR, Mestre P, Lu R, Malcuit I, Baulcombe DC. 2005. NRG1, a CC-NB-LRR protein, together with N, a TIR-NB-LRR protein, mediates resistance against tobacco mosaic virus. Current Biology 15: 968–973.
38. Qi Y, Tsuda K, Glazebrook J, Katagiri F. 2011. Physical association of pattern-triggered immunity (PTI) and effector-triggered immunity (ETI) immune receptors in Arabidopsis. Molecular Plant Pathology 12: 702–708.
39. Sarris PF, Duxbury Z, Huh SU, Ma Y, Segonzac C, Sklenar J, Derbyshire P, Cevik V, Rallapalli G, Saucet SB et al. 2015. A plant immune receptor detects pathogen effectors that target WRKY transcription factors. Cell 161: 1089–1100.
40. Schwab R, Ossowski S, Riester M, Warthmann N, Weigel D. 2006. Highly specific gene silencing by artificial microRNAs in Arabidopsis. Plant Cell 18: 1121–1133.
41. Sinapidou E, Williams K, Nott L, Bahkt S, Tor M, Crute I, Bittner-Eddy P, Beynon J. 2004. Two TIR:NB:LRR genes are required to specify resistance to Peronospora parasitica isolate Cala2 in Arabidopsis. Plant Journal 38: 898–909.
42. Sohn KH, Hughes RK, Piquerez SJ, Jones JD, Banfield MJ. 2012. Distinct regions of the Pseudomonas syringae coiled-coil effector AvrRps4 are required for activation of immunity. Proceedings of the National Academy of Sciences, USA 109: 16371–16376.
43. 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. Molecular Plant-Microbe Interactions 22: 157–165.
44. Tameling WI, Vossen JH, Albrecht M, Lengauer T, Berden JA, Haring MA, Cornelissen BJ, Takken FL. 2006. Mutations in the NB-ARC domain of I-2 that impair ATP hydrolysis cause autoactivation. Plant Physiology 140: 1233–1245.
45. Tapping RI. 2009. Innate immune sensing and activation of cell surface Toll-like receptors. Seminars in Immunology 21: 175–184.
46. 2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant Journal 11: 1187–1194.
47. Tsuda K, Katagiri F. 2010. Comparing signaling mechanisms engaged in pattern-triggered and effector-triggered immunity. Current Opinion in Plant Biology 13: 459–465.
48. Walter M, Chaban C, Schutze K, Batistic O, Weckermann K, Nake C, Blazevic D, Grefen C, Schumacher K, Oecking C et al. 2004. Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. Plant Journal 40: 428–438.
49. Wang Y, Bao Z, Zhu Y, Hua J. 2009. Analysis of temperature modulation of plant defense against biotrophic microbes. Molecular Plant–Microbe Interactions 22: 498–506.
50. Wang Z, Meng P, Zhang X, Ren D, Yang S. 2011. BON1 interacts with the protein kinases BIR1 and BAK1 in modulation of temperature-dependent plant growth and cell death in Arabidopsis. Plant Journal 67: 1081–1093.
51. 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 Journal 75: 553–565.
52. Williams SJ, Sohn KH, Wan L, Bernoux M, Sarris PF, Segonzac C, Ve T, Ma Y, Saucet SB, Ericsson DJ. 2014. Structural basis for assembly and function of a heterodimeric plant immune receptor. Science 344: 299–303.
53. Xing HL, Dong L, Wang ZP, Zhang HY, Han CY, Liu B, Wang XC, Chen QJ. 2014. A CRISPR/Cas9 toolkit for multiplex genome editing in plants. BMC Plant Biology 14: 327.
54. Xu F, Zhu C, Cevik V, Johnson K, Liu Y, Sohn K, Jones JD, Holub EB, Li X. 2015. Autoimmunity conferred by chs3-2D relies on CSA1, its adjacent TNL-encoding neighbour. Scientific Reports 5: 8792.
55. Yang H, Shi Y, Liu J, Guo L, Zhang X, Yang S. 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 Journal 63: 283–296.
56. 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.
57. Yi H, Richards EJ. 2007. A cluster of disease resistance genes in Arabidopsis is coordinately regulated by transcriptional activation and RNA silencing. Plant Cell 19: 2929–2939.
58. Zbierzak AM, Porfirova S, Griebel T, Melzer M, Parker JE, Dormann P. 2013. A TIR-NBS protein encoded by Arabidopsis Chilling Sensitive 1 (CHS1) limits chloroplast damage and cell death at low temperature. Plant Journal 75: 539–552.
59. 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.
60. Zhao T, Rui L, Li J, Nishimura MT, Vogel JP, Liu N, Liu S, Zhao Y, Dangl JL, Tang D. 2015. A truncated NLR protein, TIR-NBS2, is required for activated defense responses in the exo70B1 mutant. PLoS Genetics 11: e1004945.
61. Zhu Y, Qian W, Hua J. 2010. Temperature modulates plant defense responses through NB-LRR proteins. PLoS Pathogens 6: e1000844.