Fatty Acid-and Retinol-Binding Protein, Mj-FAR-1 Induces Tomato Host Susceptibility to Root-Knot Nematodes

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Iberkleid, Ionit ^a,b   Vieira, Paulo ^c,d   de Almeida Engler, Janice ^c   Firester, Kalia ^a   Spiegel, Yitzhak ^a   Horowitz, Sigal Brown ^a  

^a VOLCANI CENTER   (Israel)

^b HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^c CNRS   (France)

^d UNIVERSITY OF ÉVORA   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED RNA; FATTY ACID BINDING PROTEIN; GAMMA THIONIN; HELMINTH PROTEIN; JASMONIC ACID; MESSENGER RNA; MJ FAR 1 PROTEIN; PROTEIN PIN2; PROTEINASE INHIBITOR; RETINOL BINDING PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BILE; CONTROLLED STUDY; CUTICLE; GENE EXPRESSION; GENE OVEREXPRESSION; HOST PARASITE INTERACTION; IMMUNOLOCALIZATION; INFECTION SENSITIVITY; MELOIDOGYNE JAVANICA; NEMATODAL PLANT DISEASE; NONHUMAN; PARASITE DEVELOPMENT; PARASITE LOAD; PARASITE MIGRATION; PLANT DEFENSE; PLANT ROOT; PROTEIN AGGREGATION; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN SECRETION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TOMATO; TRANSGENIC PLANT;

AMINO ACID SEQUENCE; ANIMALS; FATTY ACIDS; HELMINTH PROTEINS; LYCOPERSICON ESCULENTUM; MOLECULAR SEQUENCE DATA; RETINOL-BINDING PROTEINS; RNA INTERFERENCE; TYLENCHOIDEA;

EID: 84878079826     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0064586     Document Type: Article

References (97)

1. Bird DM, (2004) Signaling between nematodes and plants. Current Opinion in Plant Biology 7: 372-376.
2. Vanholme B, De Meutter J, Tytgat T, Van Montagu M, Coomans A, et al. (2004) Secretions of plant-parasitic nematodes: a molecular update. Gene 332: 13-27.
3. Baum TJ, Hussey RS, Davis EL, (2007) Root-knot and cyst nematode parasitism genes: the molecular basis of plant parasitism. Genet Eng (N Y) 28: 17-43.
4. Davis EL, Hussey RS, Baum TJ, Bakker J, Schots A, et al. (2000) Nematode Parasitism Genes. Annu Rev Phytopathol 38: 365-396.
5. Davis RF, Kemerait RC, (2009) The multi-year effects of repeatedly growing cotton with moderate resistance to Meloidogyne incognita. J Nematol 41: 140-145.
6. Niebel A, De Almeida Engler J, Tire C, Engler G, Van Montagu M, et al. (1993) Induction patterns of an extensin gene in tobacco upon nematode infection. Plant Cell 5: 1697-1710.
7. Sijmons PC, (1993) Plant-nematode interactions. Plant Mol Biol 23: 917-931.
8. Davis EL, Hussey RS, Mitchum MG, Baum TJ, (2008) Parasitism proteins in nematode-plant interactions. Curr Opin Plant Biol 11: 360-366.
9. Hussey RS, Boerma HR, (1989) Tolerance in Maturity Groups V-VIII Soybean Cultivars to Heterodera glycines. J Nematol 21: 686-692.
10. Vieira P, Danchin EG, Neveu C, Crozat C, Jaubert S, et al. (2011) The plant apoplasm is an important recipient compartment for nematode secreted proteins. J Exp Bot 62: 1241-1253.
11. Wyss U, Zunke U, (1986) Observations on the behavior of second-stage juveniles of Heterodera schachtii inside host roots. Revue de Nematologie 9: 153-165.
12. Jones JT, Reavy B, Smant G, Prior AE, (2004) Glutathione peroxidases of the potato cyst nematode Globodera rostochiensis. Gene 324: 47-54.
13. Robertson L, Robertson WM, Sobczak M, Helder J, Tetaud E, et al. (2000) Cloning, expression and functional characterisation of a peroxiredoxin from the potato cyst nematode Globodera rostochiensis. Mol Biochem Parasitol 111: 41-49.
14. Spiegel Y, Kahane I, Cohen L, Sharon E, (1997) Meloidogyne javanica surface proteins: characterization and lability. Parasitology 115 (Pt 5) (): 513-519.
15. Barcala M, Garcia A, Cabrera J, Casson S, Lindsey K, et al. (2010) Early transcriptomic events in microdissected Arabidopsis nematode-induced giant cells. Plant J 61: 698-712.
16. Jammes F, Lecomte P, de Almeida-Engler J, Bitton F, Martin-Magniette ML, et al. (2005) Genome-wide expression profiling of the host response to root-knot nematode infection in Arabidopsis. Plant Journal 44: 447-458.
17. Feussner I, Wasternack C, (2002) The lipoxygenase pathway. Annual Review of Plant Biology 53: 275-297.
18. Chen G, Hackett R, Walker D, Taylor A, Lin Z, et al. (2004) Identification of a specific isoform of tomato lipoxygenase (TomloxC) involved in the generation of fatty acid-derived flavor compounds. Plant Physiol 136: 2641-2651.
19. Caldelari D, Wang G, Farmer EE, Dong X, (2011) Arabidopsis lox3 lox4 double mutants are male sterile and defective in global proliferative arrest. Plant Mol Biol 75: 25-33.
20. Jalloul A, Montillet JL, Assigbetse K, Agnel JP, Delannoy E, et al. (2002) Lipid peroxidation in cotton: Xanthomonas interactions and the role of lipoxygenases during the hypersensitive reaction. Plant J 32: 1-12.
21. Melan MA, Dong X, Endara ME, Davis KR, Ausubel FM, et al. (1993) An Arabidopsis thaliana lipoxygenase gene can be induced by pathogens, abscisic acid, and methyl jasmonate. Plant Physiol 101: 441-450.
22. Sanz A, Moreno JI, Castresana C, (1998) PIOX, a new pathogen-induced oxygenase with homology to animal cyclooxygenase. Plant Cell 10: 1523-1537.
23. Turner JG, Ellis C, Devoto A, (2002) The jasmonate signal pathway. Plant Cell 14 Suppl: S153-164.
24. Vellosillo T, Martinez M, Lopez MA, Vicente J, Cascon T, et al. (2007) Oxylipins produced by the 9-lipoxygenase pathway in Arabidopsis regulate lateral root development and defense responses through a specific signaling cascade. Plant Cell 19: 831-846.
25. Block A, Schmelz E, Jones JB, Klee HJ, (2005) Coronatine and salicylic acid: the battle between Arabidopsis and Pseudomonas for phytohormone control. Mol Plant Pathol 6: 79-83.
26. Bhattarai KK, Xie QG, Mantelin S, Bishnoi U, Girke T, et al. (2008) Tomato susceptibility to root-knot nematodes requires an intact jasmonic acid signaling pathway. Mol Plant Microbe Interact 21: 1205-1214.
27. Cooper WR, Jia L, Goggin L, (2005) Effects of jasmonate-induced defenses on root-knot nematode infection of resistant and susceptible tomato cultivars. J Chem Ecol 31: 1953-1967.
28. Goverse A, de Engler JA, Verhees J, van der Krol S, Helder JH, et al. (2000) Cell cycle activation by plant parasitic nematodes. Plant Mol Biol 43: 747-761.
29. Grunewald W, Cannoot B, Friml J, Gheysen G, (2009) Parasitic nematodes modulate PIN-mediated auxin transport to facilitate infection. PLoS Pathog 5: e1000266.
30. Karczmarek A, Overmars H, Helder J, Goverse A, (2004) Feeding cell development by cyst and root-knot nematodes involves a similar early, local and transient activation of a specific auxin-inducible promoter element. Mol Plant Pathol 5: 343-346.
31. Soriano IR, Riley IT, Potter MJ, Bowers WS, (2004) Phytoecdysteroids: a novel defense against plant-parasitic nematodes. J Chem Ecol 30: 1885-1899.
32. Uehara T, Sugiyama S, Matsuura H, Arie T, Masuta C, (2010) Resistant and susceptible responses in tomato to cyst nematode are differentially regulated by salicylic acid. Plant Cell Physiol 51: 1524-1536.
33. Wubben MJ 2nd, Su H, Rodermel SR, Baum TJ, (2001) Susceptibility to the sugar beet cyst nematode is modulated by ethylene signal transduction in Arabidopsis thaliana. Mol Plant Microbe Interact 14: 1206-1212.
34. Basavaraju SV, Zhan B, Kennedy MW, Liu Y, Hawdon J, et al. (2003) Ac-FAR-1, a 20 kDa fatty acid- and retinol-binding protein secreted by adult Ancylostoma caninum hookworms: gene transcription pattern, ligand binding properties and structural characterisation. Molecular and Biochemical Parasitology 126: 63-71.
35. Fairfax KC, Vermeire JJ, Harrison LM, Bungiro RD, Grant W, et al. (2009) Characterization of a fatty acid and retinol binding protein orthologue from the hookworm Ancylostoma ceylanicum. International Journal of Parasitology 39: 1561-1571.
36. Garofalo A, Kennedy MW, Bradley JE, (2003) The FAR proteins of parasitic nematodes: their possible involvement in the pathogenesis of infection and the use of Caenorhabditis elegans as a model system to evaluate their function. Med Microbiol Immunol 192: 47-52.
37. Garofalo A, Klager SL, Rowlinson MC, Nirmalan N, Klion A, et al. (2002) The FAR proteins of filarial nematodes: secretion, glycosylation and lipid binding characteristics. Molecular and Biochemical Parasitology 122: 161-170.
38. Kennedy MW, Garside LH, Goodrick LE, McDermott L, Brass A, et al. (1997) The Ov20 protein of the parasitic nematode Onchocerca volvulus. A structurally novel class of small helix-rich retinol-binding proteins. Journal of Biological Chemistry 272: 29442-29448.
39. Bath JL, Robinson M, Kennedy MW, Agbasi C, Linz L, et al. (2009) Identification of a Secreted Fatty Acid and Retinol-Binding Protein (Hp-FAR-1) from Heligmosomoides polygyrus. J Nematol 41: 228-233.
40. Prior A, Jones JT, Blok VC, Beauchamp J, McDermott L, et al. (2001) A surface-associated retinol- and fatty acid-binding protein (Gp-FAR-1) from the potato cyst nematode Globodera pallida: lipid binding activities, structural analysis and expression pattern. Biochemistry Journal 356: 387-394.
41. Garofalo A, Rowlinson MC, Amambua NA, Hughes JM, Kelly SM, et al. (2003) The FAR protein family of the nematode Caenorhabditis elegans. Differential lipid binding properties, structural characteristics, and developmental regulation. Journal of Biological Chemistry 278: 8065-8074.
42. Bradley JE, Nirmalan N, Klager SL, Faulkner H, Kennedy MW, (2001) River blindness: a role for parasite retinoid-binding proteins in the generation of pathology? Trends in Parasitology 17: 471-475.
43. Bendtsen JD, Nielsen H, von Heijne G, Brunak S, (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340: 783-795.
44. Nakai K, Horton P, (1999) PSORT: a program for detecting sorting signals in proteins and predicting their subcellular localization. Trends Biochem Sci 24: 34-36.
45. Emanuelsson O, Nielsen H, Brunak S, von Heijne G, (2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 300: 1005-1016.
46. Davis EL, Hussey RS, Baum TJ, (2004) Getting to the roots of parasitism by nematodes. Trends Parasitol 20: 134-141.
47. Rost B, Sander C, (1993) Secondary structure prediction of all-helical proteins in two states. Protein Eng 6: 831-836.
48. Cuff JA, Clamp ME, Siddiqui AS, Finlay M, Barton GJ, (1998) JPred: a consensus secondary structure prediction server. Bioinformatics 14: 892-893.
49. Lupas A, Van Dyke M, Stock J, (1991) Predicting coiled coils from protein sequences. Science 252: 1162-1164.
50. Gleave AP, (1992) A versatile binary vector system with a T-DNA organisational structure conducive to efficient integration of cloned DNA into the plant genome. Plant Mol Biol 20: 1203-1207.
51. Wesley SV, Helliwell CA, Smith NA, Wang MB, Rouse DT, et al. (2001) Construct design for efficient, effective and high-throughput gene silencing in plants. Plant J 27: 581-590.
52. Dowen RH, Engel JL, Shao F, Ecker JR, Dixon JE, (2009) A family of bacterial cysteine protease type III effectors utilizes acylation-dependent and-independent strategies to localize to plasma membranes. J Biol Chem 284: 15867-15879.
53. Bolton MD, van Esse HP, Vossen JH, de Jonge R, Stergiopoulos I, et al. (2008) The novel Cladosporium fulvum lysin motif effector Ecp6 is a virulence factor with orthologues in other fungal species. Mol Microbiol 69: 119-136.
54. Rooney HC, Van't Klooster JW, van der Hoorn RA, Joosten MH, Jones JD, et al. (2005) Cladosporium Avr2 inhibits tomato Rcr3 protease required for Cf-2-dependent disease resistance. Science 308: 1783-1786.
55. Westerink N, Brandwagt BF, de Wit PJ, Joosten MH, (2004) Cladosporium fulvum circumvents the second functional resistance gene homologue at the Cf-4 locus (Hcr9-4E) by secretion of a stable avr4E isoform. Mol Microbiol 54: 533-545.
56. Doehlemann G, van der Linde K, Assmann D, Schwammbach D, Hof A, et al. (2009) Pep1, a secreted effector protein of Ustilago maydis, is required for successful invasion of plant cells. PLoS Pathog 5: e1000290.
57. Shabab M, Shindo T, Gu C, Kaschani F, Pansuriya T, et al. (2008) Fungal effector protein AVR2 targets diversifying defense-related cys proteases of tomato. Plant Cell 20: 1169-1183.
58. Elling AA, Davis EL, Hussey RS, Baum TJ, (2007) Active uptake of cyst nematode parasitism proteins into the plant cell nucleus. Int J Parasitol 37: 1269-1279.
59. Hewezi T, Howe PJ, Maier TR, Hussey RS, Mitchum MG, et al. (2010) Arabidopsis spermidine synthase is targeted by an effector protein of the cyst nematode Heterodera schachtii. Plant Physiol 152: 968-984.
60. Huang G, Dong R, Allen R, Davis EL, Baum TJ, et al. (2006) A root-knot nematode secretory peptide functions as a ligand for a plant transcription factor. Mol Plant Microbe Interact 19: 463-470.
61. Patel N, Hamamouch N, Li C, Hewezi T, Hussey RS, et al. (2010) A nematode effector protein similar to annexins in host plants. J Exp Bot 61: 235-248.
62. Rehman S, Postma W, Tytgat T, Prins P, Qin L, et al. (2009) A secreted SPRY domain-containing protein (SPRYSEC) from the plant-parasitic nematode Globodera rostochiensis interacts with a CC-NB-LRR protein from a susceptible tomato. Mol Plant Microbe Interact 22: 330-340.
63. Sacco MA, Koropacka K, Grenier E, Jaubert MJ, Blanchard A, et al. (2009) The cyst nematode SPRYSEC protein RBP-1 elicits Gpa2- and RanGAP2-dependent plant cell death. PLoS Pathog 5: e1000564.
64. Tytgat T, Vanholme B, De Meutter J, Claeys M, Couvreur M, et al. (2004) A new class of ubiquitin extension proteins secreted by the dorsal pharyngeal gland in plant parasitic cyst nematodes. Mol Plant Microbe Interact 17: 846-852.
65. Wang J, Lee C, Replogle A, Joshi S, Korkin D, et al. (2010) Dual roles for the variable domain in protein trafficking and host-specific recognition of Heterodera glycines CLE effector proteins. New Phytol 187: 1003-1017.
66. Bannenberg G, Martinez M, Rodriguez MJ, Lopez MA, Ponce de Leon I, et al. (2009) Functional analysis of alpha-DOX2, an active alpha-dioxygenase critical for normal development in tomato plants. Plant Physiology 151: 1421-1432.
67. Andersen I, Becker W, Schluter K, Burges J, Parthier B, et al. (1992) The identification of leaf thionin as one of the main jasmonate-induced proteins of barley (Hordeum vulgare). Plant Mol Biol 19: 193.
68. Creelman RA, Mullet JE, (1997) Biosynthesis And Action Of Jasmonates In Plants. Annu Rev Plant Physiol Plant Mol Biol 48: 355-381.
69. Farmer EE, Johnson RR, Ryan CA, (1992) Regulation of expression of proteinase inhibitor genes by methyl jasmonate and jasmonic Acid. Plant Physiol 98: 995-1002.
70. Fujimoto T, Tomitaka Y, Abe H, Tsuda S, Futai K, et al. (2011) Expression profile of jasmonic acid-induced genes and the induced resistance against the root-knot nematode (Meloidogyne incognita) in tomato plants (Solanum lycopersicum) after foliar treatment with methyl jasmonate. J Plant Physiol 168: 1084-1097.
71. Terras FR, Torrekens S, Van Leuven F, Osborn RW, Vanderleyden J, et al. (1993) A new family of basic cysteine-rich plant antifungal proteins from Brassicaceae species. FEBS Lett 316: 233-240.
72. Thevissen K, Ghazi A, De Samblanx GW, Brownlee C, Osborn RW, et al. (1996) Fungal membrane responses induced by plant defensins and thionins. J Biol Chem 271: 15018-15025.
73. Li SS, Gullbo J, Lindholm P, Larsson R, Thunberg E, et al. (2002) Ligatoxin B, a new cytotoxic protein with a novel helix-turn-helix DNA-binding domain from the mistletoe Phoradendron liga. Biochem J 366: 405-413.
74. Bloch C Jr, Richardson M, (1991) A new family of small (5 kDa) protein inhibitors of insect alpha-amylases from seeds or sorghum (Sorghum bicolar (L) Moench) have sequence homologies with wheat gamma-purothionins. FEBS Lett 279: 101-104.
75. Melo FR, Rigden DJ, Franco OL, Mello LV, Ary MB, et al. (2002) Inhibition of trypsin by cowpea thionin: characterization, molecular modeling, and docking. Proteins 48: 311-319.
76. Howe GA, Lightner J, Browse J, Ryan CA, (1996) An octadecanoid pathway mutant (JL5) of tomato is compromised in signaling for defense against insect attack. Plant Cell 8: 2067-2077.
77. McPherson MJ, Harrison DJ, (2001) Protease inhibitors and directed evolution: enhancing plant resistance to nematodes. Biochem Soc Symp pp. 125-142.
78. Takahashi H, Kanayama Y, Zheng MS, Kusano T, Hase S, et al. (2004) Antagonistic interactions between the SA and JA signaling pathways in Arabidopsis modulate expression of defense genes and gene-for-gene resistance to cucumber mosaic virus. Plant Cell Physiol 45: 803-809.
79. Li L, Li C, Lee GI, Howe GA, (2002) Distinct roles for jasmonate synthesis and action in the systemic wound response of tomato. Proc Natl Acad Sci U S A 99: 6416-6421.
80. Conconi A, Miquel M, Browse JA, Ryan CA, (1996) Intracellular Levels of Free Linolenic and Linoleic Acids Increase in Tomato Leaves in Response to Wounding. Plant Physiol 111: 797-803.
81. Hwang D, Rhee SH, (1999) Receptor-mediated signaling pathways: potential targets of modulation by dietary fatty acids. Am J Clin Nutr 70: 545-556.
82. Weisiger RA, (2002) Cytosolic fatty acid binding proteins catalyze two distinct steps in intracellular transport of their ligands. Mol Cell Biochem 239: 35-43.
83. Nahar K, Kyndt T, De Vleesschauwer D, Hofte M, Gheysen G, (2011) The jasmonate pathway is a key player in systemically induced defense against root knot nematodes in rice. Plant Physiol 157: 305-316.
84. Gao X, Starr J, Gobel C, Engelberth J, Feussner I, et al. (2008) Maize 9-lipoxygenase ZmLOX3 controls development, root-specific expression of defense genes, and resistance to root-knot nematodes. Molecular Plant-Microbe Interactions 21: 98-109.
85. Hussey RS, Baker KR, (1973) Comparison of methods of collecting inocula for Meloidogyne spp., including a new technique. Plant Dis Rep 57: 1025-1028.
86. Jansen van Vuuren R, Woodward B, (2001) The response of cassava cultivars to root-knot nematode infestation: An in vitro method. Euphyrica 120: 109-113.
87. Sijmons PC, Grundler FMW, Von Mende N, Burrows PR, Wyss U, (1991) Arabidopsis thaliana as a new model host for plant parasitic nematodes. Plant J 1: 245-254.
88. Goetz M, Godt DE, Guivarc'h A, Kahmann U, Chriqui D, et al. (2001) Induction of male sterility in plants by metabolic engineering of the carbohydrate supply. Proc Natl Acad Sci U S A 98: 6522-6527.
89. Nielsen H, Engelbrecht J, Brunak S, von Heijne G, (1997) Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng 10: 1-6.
90. Horton P, Nakai K, (1997) Better prediction of protein cellular localization sites with the k nearest neighbors classifier. Proc Int Conf Intell Syst Mol Biol 5: 147-152.
91. Gasteiger E, Hoogland C, Gattiker A, Duvaud S, Wilkins MR, et al. (2005) Protein Identification and Analysis Tools on the ExPASy Server. In: Walker JM, editor. The Proteomics Protocols Handbook: Humana Press. pp. 571-607.
92. Thompson JD, Higgins DG, Gibson TJ, (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680.
93. Strimmer K, von Haeseler A, (1997) Likelihood-mapping: a simple method to visualize phylogenetic content of a sequence alignment. Proc Natl Acad Sci U S A 94: 6815-6819.
94. Felsenstein J, (1997) An alternating least squares approach to inferring phylogenies from pairwise distances. Syst Biol 46: 101-111.
95. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, et al. (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3: RESEARCH0034.
96. Shen WJ, Forde BG, (1989) Efflicient transformation of Agrobactenum spp. by high voltage electroporation. Nucleic Acid Research 17: 8385.
97. Bybd DW, Kirkpatrick T, Barker KR, (1983) An improved technique for clearing and staining plant tissues for detection of nematodes. J Nematol 15: 142-143.