Functional analysis of the tomato immune receptor Ve1 through domain swaps with its non-functional homolog Ve2

PLoS ONE

Volumn 9, Issue 2, 2014, Pages

  Fradin, Emilie F ^a,b   Zhang, Zhao ^a   Rovenich, Hanna ^a   Song, Yin ^a   Liebrand, Thomas W H ^a   Masini, Laura ^a   Van Den Berg, Grardy C M ^a   Joosten, Matthieu H A J ^a,b   Thomma, Bart P H J ^a,b  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b CENTRE FOR BIOSYSTEMS GENOMICS   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CHIMERIC PROTEIN; SOBIR1 PROTEIN; UNCLASSIFIED DRUG; VE1 PROTEIN; VE2 PROTEIN; VEGETABLE PROTEIN;

ALLERGIC REACTION; AMINO ACID COMPOSITION; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CYTOPLASM; GENE LOCUS; NONHUMAN; PLANT GENE; PLANT IMMUNITY; PLANT RESPONSE; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN DOMAIN SWAPPING; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SEQUENCE HOMOLOGY; TOMATO; VE1 GENE; VE2 GENE; VERTICILLIUM DAHLIAE;

AMINO ACID SEQUENCE; GENE DELETION; GENE EXPRESSION REGULATION, PLANT; HOST-PATHOGEN INTERACTIONS; LYCOPERSICON ESCULENTUM; MOLECULAR SEQUENCE DATA; PLANT DISEASES; PLANT PROTEINS; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, CELL SURFACE; RECEPTORS, IMMUNOLOGIC; VERTICILLIUM;

EID: 84895541789     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0088208     Document Type: Article

References (68)

1. Thomma BPHJ, Nürnberger T, Joosten MHAJ (2011) Of PAMPs and effectors: the blurred PTI-ETI dichotomy. Plant Cell 23: 4-15.
2. Boller T, Felix G (2009) A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol 60: 379-406.
3. Hammond-Kosack KE, Jones JDG (1996) Resistance gene-dependent plant defense responses. Plant Cell 8: 1773-1791. (Pubitemid 27012404)
4. Fradin EF, Thomma BPHJ (2006) Physiology and molecular aspects of Verticillium wilt diseases caused by V. dahliae and V. albo-atrum. Mol Plant Pathol 7: 71-86.
5. Pegg GF, Brady BL (2002) Verticillium Wilts. Wallingford, UK: CABY publishing.
6. Kawchuk LM, Hachey J, Lynch DR, Kulcsar F, van Rooijen G, et al. (2001) Tomato Ve disease resistance genes encode cell surface-like receptors. Proc Natl Acad Sci USA 98: 6511-6515. (Pubitemid 32488268)
7. Pegg GF (1974) Verticillium diseases. Rev Plant Pathol 53: 26.
8. Wang G, Fiers M, Ellendorff U, Wang ZZ, de Wit PJGM, et al. (2010) The diverse roles of extracellular leucine-rich repeat-containing receptor-like proteins in plants. Crit Rev Plant Sci 29: 285-299.
9. Fradin EF, Zhang Z, Juarez Ayala JC, Castroverde CD, Nazar RN, et al. (2009) Genetic dissection of Verticillium wilt resistance mediated by tomato Ve1. Plant Physiol 150: 320-332.
10. Kinoshita T, Cano-Delgado AC, Seto H, Hiranuma S, Fujioka S, et al. (2005) Binding of brassinosteroids to the extracellular domain of plant receptor kinase BRI1. Nature 433: 167-171.
11. Kobe B, Deisenhofer J (1996) Mechanism of ribonuclease inhibition by ribonuclease inhibitor protein based on the crystal structure of its complex with ribonuclease A. J Mol Biol 264: 1028-1043. (Pubitemid 27019490)
12. Kobe B, Kajava AV (2001) The leucine-rich repeat as a protein recognition motif. Curr Opin Struct Biol 11: 725-732. (Pubitemid 34076634)
13. Dunning FM, Sun W, Jansen KL, Helft L, Bent AF (2007) Identification and mutational analysis of Arabidopsis FLS2 leucine-rich repeat domain residues that contribute to flagellin perception. Plant Cell 19: 3297-3313. (Pubitemid 350276726)
14. Hothorn M, Belkhadir Y, Dreux M, Dabi T, Noel JP, et al. (2011) Structural basis of steroid hormone perception by the receptor kinase BRI1. Nature 474: 467-471.
15. She J, Han Z, Kim TW, Wang J, Cheng W, et al. (2011) Structural insight into brassinosteroid perception by BRI1. Nature 474: 472-476.
16. Wulff BB, Heese A, Tomlinson-Buhot L, Jones DA, de la Pena M, et al. (2009) The major specificity-determining amino acids of the tomato Cf-9 disease resistance protein are at hypervariable solvent-exposed positions in the central leucine-rich repeats. Mol Plant Microbe Interact 22: 1203-1213.
17. Jones DA, Thomas CM, Hammond-Kosack KE, Balint-Kurti PJ, Jones JDG (1994) Isolation of the tomato Cf-9 gene for resistance to Cladosporium fulvum by transposon tagging. Science 266: 789-793. (Pubitemid 24359284)
18. Dixon MS, Jones DA, Keddie JS, Thomas CM, Harrison K, et al. (1996) The tomato Cf-2 disease resistance locus comprises two functional genes encoding leucine-rich repeat proteins. Cell 84: 451-459. (Pubitemid 26058570)
19. Dixon MS, Hatzixanthis K, Jones DA, Harrison K, Jones JDG (1998) The tomato Cf-5 disease resistance gene and six homologs show pronounced allelic variation in leucine-rich repeat copy number. Plant Cell 10: 1915-1925.
20. Takken FLW, Thomas CM, Joosten MHAJ, Golstein C, Westerink N, et al. (1999) A second gene at the tomato Cf-4 locus confers resistance to Cladosporium fulvum through recognition of a novel avirulence determinant. Plant J 20: 279-288. (Pubitemid 129515910)
21. Thomas CM, Jones DA, Parniske M, Harrison K, Balint-Kurti PJ, et al. (1997) Characterization of the tomato Cf-4 gene for resistance to Cladosporium fulvum identifies sequences that determine recognitional specificity in Cf-4 and Cf-9. Plant Cell 9: 2209-2224. (Pubitemid 28174057)
22. Panter SN, Hammond-Kosack KE, Harrison K, Jones JDG, Jones DA (2002) Developmental control of promoter activity is not responsible for mature onset of Cf-9B-mediated resistance to leaf mold in tomato. Mol Plant-Microbe Interact 15: 1099-1107. (Pubitemid 36737949)
23. Seear PJ, Dixon MS (2003) Variable leucine-rich repeats of tomato disease resistance genes Cf-2 and Cf-5 determine specificity. Mol Plant Pathol 4: 199-202. (Pubitemid 36639411)
24. Chakrabarti A, Panter SN, Harrison K, Jones JDG, Jones DA (2009) Regions of the Cf-9B disease resistance protein able to cause spontaneous necrosis in Nicotiana benthamiana lie within the region controlling pathogen recognition in tomato. Mol Plant Microbe Interact 22: 1214-1226.
25. van der Hoorn RA, Roth R, de Wit PJGM (2001) Identification of distinct specificity determinants in resistance protein Cf-4 allows construction of a Cf-9 mutant that confers recognition of avirulence protein Avr4. Plant Cell 13: 273-285. (Pubitemid 32207683)
26. Wulff BB, Thomas CM, Smoker M, Grant M, Jones JDG (2001) Domain swapping and gene shuffling identify sequences required for induction of an Avr-dependent hypersensitive response by the tomato Cf-4 and Cf-9 proteins. Plant Cell 13: 255-272. (Pubitemid 32207682)
27. de Jonge R, van Esse HP, Maruthachalam K, Bolton MD, Santhanam P, et al. (2012) Tomato immune receptor Ve1 recognizes effector of multiple fungal pathogens uncovered by genome and RNA sequencing. Proc Natl Acad Sci USA 109: 5110-5115.
28. Zhang Z, Fradin E, de Jonge R, van Esse HP, Smit P, et al. (2013) Optimized agroinfiltration and virus-induced gene silencing to study ve1-mediated Verticillium resistance in tobacco. Mol Plant Microbe Interact 26: 182-190.
29. Fradin EF, Abd-El-Haliem A, Masini L, van den Berg GC, Joosten MHAJ, et al. (2011) Interfamily transfer of tomato Ve1 mediates Verticillium resistance in Arabidopsis. Plant Physiol 156: 2255-2265.
30. Zhang Z, van Esse HP, van Damme M, Fradin EF, Liu CM, et al. (2013b) Ve1-mediated resistance against Verticillium does not involve a hypersensitive response in Arabidopsis. Mol Plant Pathol 14: 719-727.
31. van der Hoorn RA, Wulff BB, Rivas S, Durrant MC, van der Ploeg A, et al. (2005) Structure-function analysis of Cf-9, a receptor-like protein with extracytoplasmic leucine-rich repeats. Plant Cell 17: 1000-1015. (Pubitemid 43138236)
32. Bleckmann A, Weidtkamp-Peters S, Seidel CA, Simon R (2010) Stem cell signaling in Arabidopsis requires CRN to localize CLV2 to the plasma membrane. Plant Physiol 152: 166-176
33. Dalmay T, Hamilton A, Rudd S, Angell S, Baulcombe DC (2000) An RNA-Dependent RNA polymerase gene in Arabidopsis is required for posttranscriptional gene silencing mediated by a transgene but not by a virus. Cell 101: 543-553.
34. Mourrain P, Beclin C, Elmayan T, Feuerbach F, Godon C, et al. (2000) Arabidopsis SGS2 and SGS3 genes are required for posttranscriptional gene silencing and natural virus resistance. Cell 101: 533-542.
35. Butaye KMJ, Goderis IJWM, Wouters PFJ, Pues JMTG, Delauré SL, et al. (2004) Stable high-level transgene expression in Arabidopsis thaliana using gene silencing mutants and matrix attachment regions. Plant J 39: 440-449. (Pubitemid 39040148)
36. Ellendorff U, Fradin EF, de Jonge R, Thomma BPHJ (2009) RNA silencing is required for Arabidopsis defence against Verticillium wilt disease. J Exp Bot 60: 591-602.
37. Liebrand TW, van den Berg GC, Zhang Z, Smit P, Cordewener JH, et al. (2013) The receptor-like kinase SOBIR1/EVR interacts with receptor-like proteins in plant immunity against fungal infection. Proc Natl Acad Sci USA 110: 10010- 10015.
38. Liebrand TW, van den Burg HA, Joosten MHAJ (2013) Two for all: receptor-associated kinases SOBIR1 and BAK1. Trends Plant Sci doi: 10.1016/j.tplants.2013.10.003.
39. Zhang L, Kars I, Essenstam B, Liebrand TW, Wagemakers L, et al (2013) Fungal endopolygalacturonases are recognized as MAMPs by the Arabidopsis Receptor-Like Protein RBPG1. Plant Physiol. doi: http://dx.doi.org/10.1104/pp. 113.230698
40. Zhang W, Fraiture,M, Kolb D, Löffelhardt B, Desaki Y, et al. (2013) Arabidopsis RECEPTOR-LIKE PROTEIN30 and receptor-like kinase SUPPRESSOR OF BIR1-1/EVERSHED mediate innate immunity to necrotrophic fungi. Plant Cell doi: 10.1105/tpc.113.117010.
41. Li J (2011) Direct involvement of leucine-rich repeats in assembling ligand-triggered receptor-coreceptor complexes. Proc Natl Acad Sci USA 108: 8073- 8074.
42. Jaillais Y, Belkhadir Y, Balsemao-Pires E, Dangl JL, Chory J (2011) Extracellular leucine-rich repeats as a platform for receptor/coreceptor complex formation. Proc Natl Acad Sci USA 108: 8503-8507.
43. Zhang Z, Thomma BPHJ (2013). Structure-function aspects of extracellular leucine-rich repeat-containing cell surface receptors in plants. J Integr Plant Biol doi: 10.1111/jipb.12080
44. Fritz-Laylin LK, Krishnamurthy N, Tör M, Sjolander KV, Jones JDG (2005) Phylogenomic analysis of the receptor-like proteins of rice and Arabidopsis. Plant Physiol 138: 611-623. (Pubitemid 43793144)
45. Wang G, Long Y, Thomma BPHJ, de Wit PJGM, Angenent GC, et al. (2010) Functional analyses of the CLAVATA2-like proteins and their domains that contribute to CLAVATA2 specificity. Plant Physiol 152: 320-331.
46. Wulff BB, Thomas CM, Parniske M, Jones JDG (2004) Genetic variation at the tomato Cf-4 / Cf-9 locus induced by EMS mutagenesis and intralocus recombination. Genetics 167: 459-470. (Pubitemid 38736402)
47. Zhang YX, Yang YA, Fang B, Gannon P, Ding PT, et al. (2010) Arabidopsis snc2-1D activates receptor-like protein-mediated immunity transduced through WRKY70. Plant Cell 22: 3153-3163.
48. Wang X, Kota U, He K, Blackburn K, Li J, et al. (2008) Sequential transphosphorylation of the BRI1/BAK1 receptor kinase complex impacts early events in brassinosteroid signaling. Dev Cell 15: 220-235.
49. Leslie ME, Lewis MW, Youn JY, Daniels MJ, Liljegren SJ (2010) The EVERSHED receptor-like kinase modulates floral organ shedding in Arabidopsis. Development 137: 467-476.
50. Gao M, Wang X, Wang D, Xu F, Ding X, et al. (2009) Regulation of cell death and innate immunity by two receptor-like kinases in Arabidopsis. Cell Host Microbe 6: 34-44.
51. Jones DA, Jones JDG (1997) The role of leucine-rich repeat proteins in plant defences. Adv Bot Res 24: 89-167.
52. Matsushima N, Mikami T, Tanaka T, Miyashita H, Yamada K, et al. (2009) Analyses of non-leucine-rich repeat (non-LRR) regions intervening between LRRs in proteins. Biochim Biophysica Acta 1790: 1217-1237.
53. Li JM, Chory J (1997) A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 90: 929-938.
54. Matsubayashi Y, Ogawa M, Morita A, Sakagami Y (2002) An LRR receptor kinase involved in perception of a peptide plant hormone, phytosulfokine. Science 296: 1470-1472. (Pubitemid 34553092)
55. Shinohara H, Ogawa M, Sakagami Y, Matsubayashi Y (2007) Identification of ligand binding site of phytosulfokine receptor by on-column photoaffinity labeling. J Biol Chem 282: 124-131. (Pubitemid 47076642)
56. Ruthardt N, Kawchuk LM, Fischer R (2007) Tomato protein of the resistance gene Ve2 to Verticillium wilt [Verticillium spp.] is located in the endoplasmic reticulum. Can J Plant Pathol 29: 3-8. (Pubitemid 46932062)
57. Zhang Y, Wang X, Yang S, Chi J, Zhang G, et al. (2011) Cloning and characterization of a Verticillium wilt resistance gene from Gossypium barbadense and functional analysis in Arabidopsis thaliana. Plant Cell Rep 30: 2085-2096.
58. Piedras P, Rivas S, Droge S, Hillmer S, Jones JDG (2000) Functional, c-myctagged Cf-9 resistance gene products are plasma-membrane localized and glycosylated. Plant J 21: 529-536. (Pubitemid 30221300)
59. Benghezal M, Wasteneys GO, Jones DA (2000) The C-terminal dilysine motif confers endoplasmic reticulum localisation to type I membrane proteins in plants. Plant Cell 12: 1179-1201. (Pubitemid 30622721)
60. Rivas S, Thomas CM (2005) Molecular interactions between tomato and the leaf mold pathogen Cladosporium fulvum. Annu Rev Phytopathol 43: 395-436. (Pubitemid 41318878)
61. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735-743.
62. Karimi M, Inzé D, Depicker A (2002) GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends in Plant Science 7: 193-195. (Pubitemid 36725938)
63. Honée G, Buitink J, Jabs T, De Kloe J, Sijbolts F, et al. (1998) Induction of defense-related responses in Cf9 tomato cells by the AVR9 elicitor peptide of Cladosporium fulvum is developmentally regulated. Plant Physiol 117: 809-820. (Pubitemid 128652854)
64. Nakagawa T, Suzuki T, Murata S, Nakamura S, Hino T, et al. (2007) Improved gateway binary vectors: High-performance vectors for creation of fusion constructs in Transgenic analysis of plants. Biosci Biotechnol Biochem 71: 2095-2100. (Pubitemid 350113146)
65. Shimada TL, Shimada T, Hara-Nishimura I (2010) A rapid and non-destructive screenable marker, FAST, for identifying transformed seeds of Arabidopsis thaliana. Plant J. 61:519-528.
66. Van der Hoorn RA, Laurent F, Roth R, De Wit PJ (2000) Agroinfiltration is a versatile tool that facilitates comparative analyses of Avr9/Cf-9-induced and Avr4/Cf-4-induced necrosis. Mol Plant Microbe Interact. 13: 439-446. (Pubitemid 30174527)
67. Liebrand TW, Smit P, Abd-El-Haliem A, de Jonge R, Cordewener JH, et al. (2012) Endoplasmic reticulum-quality control chaperones facilitate the biogenesis of Cf receptor-like proteins involved in pathogen resistance of tomato. Plant Physiol 159: 1819-1833.
68. Pietraszewska-Bogiel A, Lefebvre B, Koini MA, Klaus-Heisen D, Takken FLW, et al. (2013) Interaction of Medicago truncatula Lysin motif receptor-like kinases, NFP and LYK3, produced in Nicotiana benthamiana induces defence-like responses. PLoS One 8: e65055.