Apoplastic Venom Allergen-like Proteins of Cyst Nematodes Modulate the Activation of Basal Plant Innate Immunity by Cell Surface Receptors

PLoS Pathogens

Volumn 10, Issue 12, 2014, Pages

  Lozano Torres, Jose L ^a   Wilbers, Ruud H P ^a   Warmerdam, Sonja ^a   Finkers Tomczak, Anna ^a   Diaz Granados, Amalia ^a   van Schaik, Casper C ^a   Helder, Johannes ^a   Bakker, Jaap ^a,b   Goverse, Aska ^a,b   Schots, Arjen ^a   Smant, Geert ^a,b  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b CENTRE FOR BIOSYSTEMS GENOMICS   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SURFACE RECEPTOR; CYSTEINE PROTEINASE; GENOMIC DNA; GR VAP1 PROTEIN; HS VAP1 PROTEIN; HS VAP2 PROTEIN; MICROORGANISM PROTEIN; PROTEINASE; UNCLASSIFIED DRUG; VENOM ALLERGEN LIKE PROTEIN; HELMINTH PROTEIN; PARASITE ANTIGEN; PLANTIBODY; VENOM;

APOPTOSIS; ARABIDOPSIS THALIANA; ARTICLE; CELL WALL; CHLOROPLAST; CONTROLLED STUDY; CYST; DOWN REGULATION; ENZYME ACTIVITY; GLOBODERA ROSTOCHIENSIS; GROWTH INHIBITION; HETERODERA SCHACHTII; HOST RESISTANCE; INTRACELLULAR SIGNALING; MELOIDOGYNE INCOGNITA; NEMATODE; NONHUMAN; NONPHOTOCHEMICAL QUENCHING; NUCLEOTIDE SEQUENCE; PARASITE MIGRATION; PARASITISM; PATHOGENESIS; PLANT IMMUNITY; PLANT ROOT; PROTEIN DEGRADATION; PROTEIN EXPRESSION; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; RNA INTERFERENCE; RNA SEQUENCE; SECRETION (PROCESS); TRANSGENIC CROP; WESTERN BLOTTING; ANIMAL; ARABIDOPSIS; IMMUNOLOGY; INNATE IMMUNITY; NEMATODIASIS; PARASITOLOGY; PLANT DISEASE; TYLENCHOIDEA;

ANIMALIA; ARABIDOPSIS THALIANA; BETA VULGARIS SUBSP. VULGARIS; GLOBODERA ROSTOCHIENSIS; HETERODERA SCHACHTII; MELOIDOGYNE; MELOIDOGYNE INCOGNITA; MELOIDOGYNE JAVANICA; NEMATODA; SOLANUM TUBEROSUM;

ANIMALS; ANTIGENS, HELMINTH; APOPTOSIS; ARABIDOPSIS; HELMINTH PROTEINS; IMMUNITY, INNATE; NEMATODA; NEMATODE INFECTIONS; PLANT DISEASES; PLANT IMMUNITY; PLANTIBODIES; RECEPTORS, CELL SURFACE; TYLENCHOIDEA; VENOMS;

EID: 84919665942     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004569     Document Type: Article

References (90)

1. Jones JT, Haegeman A, Danchin EGJ, Gaur HS, Helder J, et al. (2013) Top 10 plant-parasitic nematodes in molecular plant pathology. Mol Plant Pathol: 946–961.
2. McCarter JP (2009) Molecular approaches toward resistance to plant-parasitic nematodes. In: Berg RH, Taylor CG, editors. Cell biology of plant nematode parasitism.Berlin Heidelberg: Springer Verlag.239–267.
3. Goverse A, Smant G (2014) The Activation and Suppression of Plant Innate Immunity by Parasitic Nematodes. Annu Rev Phytopathol 52: in press.
4. Williamson VM, Kumar A, (2006) Nematode resistance in plants: the battle underground. Trends Genet 22: 396–403.
5. Gish LA, Clark SE, (2011) The RLK/Pelle family of kinases. Plant J 66: 117–127.
6. 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: 379–407.
7. Schwessinger B, Zipfel C, (2008) News from the frontline: recent insights into PAMP-triggered immunity in plants. Curr Opin Plant Biol 11: 389–395.
8. Chisholm ST, Coaker G, Day B, Staskawicz BJ, (2006) Host-microbe interactions: Shaping the evolution of the plant immune response. Cell 124: 803–814.
9. Kruijt M, De Kock MJD, De Wit PJGM, (2005) Receptor-like proteins involved in plant disease resistance - Review. Mol Plant Pathol 6: 85–97.
10. 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.
11. Wang G, Fiers M, Ellendorff U, Wang Z, 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.
12. Liebrand TWH, van den Burg HA, Joosten MHAJ, (2014) Two for all: receptor-associated kinases SOBIR1 and BAK1. Trends Plant Sci 19: 123–132.
13. Monaghan J, Zipfel C, (2012) Plant pattern recognition receptor complexes at the plasma membrane. Curr Opin Plant Biol 15: 349–357.
14. Lozano-Torres JL, Wilbers RHP, Gawronski P, Boshoven JC, Finkers-Tomczak A, et al. (2012) Dual disease resistance mediated by the immune receptor Cf-2 in tomato requires a common virulence target of a fungus and a nematode. Proc Natl Acad Sci U S A 109: 10119–10124.
15. Krüger J, Thomas CM, Golstein C, Dixon MS, Smoker M, et al. (2002) A tomato cysteine protease required for Cf-2-dependent disease resistance and suppression of autonecrosis. Science 296: 744–747.
16. Rooney HCE, Van't Klooster JW, Van Der Hoorn RAL, Joosten MHAJ, Jones JDG, et al. (2005) Cladosporium Avr2 inhibits tomato Rcr3 protease required for Cf-2-dependent disease resistance. Science 308: 1783–1786.
17. Song J, Win J, Tian M, Schornack S, Kaschani F, et al. (2009) Apoplastic effectors secreted by two unrelated eukaryotic plant pathogens target the tomato defense protease Rcr3. Proc Natl Acad Sci U S A 106: 1654–1659.
18. Cantacessi C, Campbell BE, Visser A, Geldhof P, Nolan MJ, et al. (2009) A portrait of the "SCP/TAPS" proteins of eukaryotes - Developing a framework for fundamental research and biotechnological outcomes. Biotechnol Adv 27: 376–388.
19. Cantacessi C, Gasser RB, (2012) SCP/TAPS proteins in helminths - where to from now? Mol Cell Probes 26: 54–59.
20. Jasmer DP, Goverse A, Smant G, (2003) Parasitic Nematode Interactions with Mammals and Plants. Annu Rev Phytopathol 41: 245–270.
21. Hawdon JM, Jones BF, Hoffman DR, Hotez PJ, (1996) Cloning and characterization of Ancylostoma-secreted protein: A novel protein associated with the transition to parasitism by infective hookworm larvae. J Biol Chem 271: 6672–6678.
22. Hawdon JM, Narasimhan S, Hotez PJ, (1999) Ancylostoma secreted protein 2: cloning and characterization of a second member of a family of nematode secreted proteins from Ancylostoma caninum. Mol Biochem Parasitol 99: 149–165.
23. Datu BJD, Gasser RB, Nagaraj SH, Ong EK, O'Donoghue P, et al. (2008) Transcriptional changes in the hookworm, Ancylostoma caninum, during the transition from a free-living to a parasitic larva. PLoS Negl Trop Dis 2: e130.
24. Mulvenna J, Hamilton B, Nagaraj SH, Smyth D, Loukas A, et al. (2009) Proteomics analysis of the excretory/secretory component of the blood-feeding stage of the hookworm, Ancylostoma caninum. Mol Cell Proteomics 8: 109–121.
25. Haegeman A, Mantelin S, Jones JT, Gheysen G, (2012) Functional roles of effectors of plant-parasitic nematodes. Gene 492: 19–31.
26. Hewezi T, Baum TJ, (2013) Manipulation of plant cells by cyst and root-knot nematode effectors. Mol Plant Microbe Interact 26: 9–16.
27. Mitchum MG, Hussey RS, Baum TJ, Wang X, Elling AA, et al. (2013) Nematode effector proteins: An emerging paradigm of parasitism. New Phytol 199: 879–894.
28. Kyndt T, Vieira P, Gheysen G, de Almeida-Engler J (2013) Nematode feeding sites: unique organs in plant roots. Planta: 1–12.
29. Chronis D, Chen SY, Lu SW, Hewezi T, Carpenter SCD, et al. (2013) A ubiquitin carboxyl extension protein secreted from a plant-parasitic nematode Globodera rostochiensis is cleaved in planta to promote plant parasitism. Plant J 74: 185–196.
30. Postma WJ, Slootweg EJ, Rehman S, Finkers-Tomczak A, Tytgat TOG, et al. (2012) The effector SPRYSEC-19 of Globodera rostochiensis suppresses CC-NB-LRR-mediated disease resistance in plants. Plant Physiol 160: 944–954.
31. Jaouannet M, Magliano M, Arguel MJ, Gourgues M, Evangelisti E, et al. (2013) The root-knot nematode calreticulin Mi-CRT is a key effector in plant defense suppression. Mol Plant Microbe Interact 26: 97–105.
32. Jaubert S, Milac AL, Petrescu AJ, De Almeida-Engler J, Abad P, et al. (2005) In planta secretion of a calreticulin by migratory and sedentary stages of root-knot nematode. Mol Plant Microbe Interact 18: 1277–1284.
33. Carpita N, McCann M, Griffing LR, (1996) The plant extracellular matrix: News from the cell's frontier. Plant Cell 8: 1451–1463.
34. Aumailley M, Gayraud B, (1998) Structure and biological activity of the extracellular matrix. J Mol Med 76: 253–265.
35. Nurnberger T, Brunner F, Kemmerling B, Piater L, (2004) Innate immunity in plants and animals: Striking similarities and obvious differences. Immunol Rev 198: 249–266.
36. Ausubel FM, (2005) Are innate immune signaling pathways in plants and animals conserved? Nat Immunol 6: 973–979.
37. Moyle M, Foster DL, McGrath DE, Brown SM, Laroche Y, et al. (1994) A hookworm glycoprotein that inhibits neutrophil function is a ligand of the integrin CD11b/CD18. J Biol Chem 269: 10008–10015.
38. Bower MA, Constant SL, Mendez S, (2008) Necator americanus: The Na-ASP-2 protein secreted by the infective larvae induces neutrophil recruitment in vivo and in vitro. Exp Parasitol 118: 569–575.
39. Asojo OA, Goud G, Dhar K, Loukas A, Zhan B, et al. (2005) X-ray structure of Na-ASP-2, a pathogenesis-related-1 protein from the nematode parasite, Necator americanus, and a vaccine antigen for human hookworm infection. J Mol Biol 346: 801–814.
40. Del Valle A, Jones BF, Harrison LM, Chadderdon RC, Cappello M, (2003) Isolation and molecular cloning of a secreted hookworm platelet inhibitor from adult Ancylostoma caninum. Mol Biochem Parasitol 129: 167–177.
41. Chinchilla D, Bauer Z, Regenass M, Boller T, Felix G, (2006) The Arabidopsis receptor kinase FLS2 binds flg22 and determines the specificity of flagellin perception. Plant Cell 18: 465–476.
42. Van Esse HP, Van't Klooster JW, Bolton MD, Yadeta KA, Van Baarlen P, et al. (2008) The Cladosporium fulvum virulence protein Avr2 inhibits host proteases required for basal defense. Plant Cell 20: 1948–1963.
43. Kaschani F, Shabab M, Bozkurt T, Shindo T, Schornack S, et al. (2010) An effector-targeted protease contributes to defense against Phytophthora infestans and is under diversifying selection in natural hosts. Plant Physiol 154: 1794–1804.
44. Ding X, Shields J, Allen R, Hussey RS, (2000) Molecular cloning and characterisation of a venom allergen AG5-like cDNA from Meloidogyne incognita. Int J Parasitol 30: 77–81.
45. Gómez-Gómez L, Boller T, (2000) FLS2: An LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol Cell 5: 1003–1011.
46. Kanehisa M, Goto S, (2000) KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res 28: 27–30.
47. Kanehisa M (2013) Molecular network analysis of diseases and drugs in KEGG. In: Mamitsuka H, Kanehisa M, DeLisi C, editors.263–275.
48. Kanehisa M, Goto S, Hattori M, Aoki-Kinoshita KF, Itoh M, et al. (2006) From genomics to chemical genomics: new developments in KEGG. Nucleic Acids Res 34: D354–357.
49. Schaller A, Stintzi A, Graff L, (2012) Subtilases - versatile tools for protein turnover, plant development, and interactions with the environment. Physiol Plant 145: 52–66.
50. Ramírez V, López A, Mauch-Mani B, Gil MJ, Vera P, (2013) An Extracellular Subtilase Switch for Immune Priming in Arabidopsis. PLoS Pathog 9: e1603445.
51. Li XP, Björkman O, Shih C, Grossman AR, Rosenquist M, et al. (2000) A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403: 391–395.
52. Göhre V, Jones AME, Sklenár J, Robatzek S, Weber APM, (2012) Molecular crosstalk between PAMP-triggered immunity and photosynthesis. Mol Plant Microbe Interact 25: 1083–1092.
53. Jankanpaa HJ, Frenkel M, Zulfugarov I, Reichelt M, Krieger-Liszkay A, et al. (2013) Non-Photochemical Quenching Capacity in Arabidopsis thaliana Affects Herbivore Behaviour. PLoS One 8: e53232.
54. Demmig-Adams B, Cohu CM, Amiard V, Zadelhoff G, Veldink GA, et al. (2013) Emerging trade-offs - impact of photoprotectants (PsbS, xanthophylls, and vitamin E) on oxylipins as regulators of development and defense. New Phytol 197: 720–729.
55. Danon A, Miersch O, Felix G, den Camp RGLO, Apel K, (2005) Concurrent activation of cell death-regulating signaling pathways by singlet oxygen in Arabidopsis thaliana. Plant J 41: 68–80.
56. Rehman S, Butterbach P, Popeijus H, Overmars H, Davis EL, et al. (2009) Identification and characterization of the most abundant cellulases in stylet secretions from Globodera rostochiensis. Phytopathol 99: 194–202.
57. Heil M, (2012) Damaged-self recognition as a general strategy for injury detection. Plant Signaling and Behavior 7: 576–580.
58. Sinha D, Gupta MK, Patel HK, Ranjan A, Sonti RV, (2013) Cell Wall Degrading Enzyme Induced Rice Innate Immune Responses Are Suppressed by the Type 3 Secretion System Effectors XopN, XopQ, XopX and XopZ of Xanthomonas oryzae pv. oryzae. PLoS One 8: e75867.
59. Bouwmeester K, Govers F, (2009) Arabidopsis L-type lectin receptor kinases: Phylogeny, classification, and expression profiles. J Exp Bot 60: 4383–4396.
60. Nakhamchik A, Zhao Z, Provart NJ, Shiu SH, Keatley SK, et al. (2004) A comprehensive expression analysis of the Arabidopsis proline-rich extensin-like receptor kinase gene family using bioinformatic and experimental approaches. Plant Cell Physiol 45: 1875–1881.
61. Silva NF, Goring DR, (2002) The proline-rich, extensin-like receptor kinase-1 (PERK1) gene is rapidly induced by wounding. Plant Mol Biol 50: 667–685.
62. 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.
63. Rautengarten C, Steinhauser D, Bussis D, Stintzi A, Schaller A, et al. (2005) Inferring hypotheses on functional relationships of genes: Analysis of the Arabidopsis thaliana subtilase gene family. PLoS Comput Biol 1: 297–312.
64. Li XP, Gilmore AM, Caffarri S, Bassi R, Golan T, et al. (2004) Regulation of photosynthetic light harvesting involves intrathylakoid lumen pH sensing by the PsbS protein. J Biol Chem 279: 22866–22874.
65. Roach T, Krieger-Liszkay A, (2012) The role of the PsbS protein in the protection of photosystems I and II against high light in Arabidopsis thaliana. BBA Bioenergetics 1817: 2158–2165.
66. Triantaphylides C, Havaux M, (2009) Singlet oxygen in plants: production, detoxification and signaling. Trends Plant Sci 14: 219–228.
67. Li XP, Muller-Moule P, Gilmore AM, Niyogi KK, (2002) PsbS-dependent enhancement of feedback de-excitation protects photosystem II from photoinhibition. Proc Natl Acad Sci U S A 99: 15222–15227.
68. Frenkel M, Kulheim C, Jankanpaaa HJ, Skogstrom O, Dall'Osto L, et al. (2009) Improper excess light energy dissipation in Arabidopsis results in a metabolic reprogramming. BMC Plant Biol 9.
69. Golinowski W, Grundler FMW, Sobczak M, (1996) Changes in the structure of Arabidopsis thaliana during female development of the plant-parasitic nematode Heterodera schachtii. Protoplasma 194: 103–116.
70. Szakasits D, Heinen P, Wieczorek K, Hofmann J, Wagner F, et al. (2009) The transcriptome of syncytia induced by the cyst nematode Heterodera schachtii in Arabidopsis roots. Plant J 57: 771–784.
71. Decreux A, Messiaen J, (2005) Wall-associated kinase WAK1 interacts with cell wall pectins in a calcium-induced conformation. Plant Cell Physiol 46: 268–278.
72. Brutus A, Sicilia F, Macone A, Cervone F, De Lorenzo G, (2010) A domain swap approach reveals a role of the plant wall-associated kinase 1 (WAK1) as a receptor of oligogalacturonides. Proc Natl Acad Sci U S A 107: 9452–9457.
73. D'Ovidio R, Mattei B, Roberti S, Bellincampi D, (2004) Polygalacturonases, polygalacturonase-inhibiting proteins and pectic oligomers in plant-pathogen interactions. BBA Proteins Proteom 1696: 237–244.
74. Moerschbacher BM, Mierau M, Graeßner B, Noll U, Mort AJ, (1999) Small oligomers of galacturonic acid are endogenous suppressors of disease resistance reactions in wheat leaves. J Exp Bot 50: 605–612.
75. Chen Q, Rehman S, Smant G, Jones JT, (2005) Functional analysis of pathogenicity proteins of the potato cyst nematode Globodera rostochiensis using RNAi. Mol Plant Microbe Interact 18: 621.
76. Greenbaum D, Medzihradszky KF, Burlingame A, Bogyo M, (2000) Epoxide electrophiles as activity-dependent cysteine protease profiling and discovery tools. Chem Biol 7: 569–581.
77. Curtis MD, Grossniklaus U, (2003) A Gateway Cloning Vector Set for High-Throughput Functional Analysis of Genes in Planta. Plant Physiol 133: 462–469.
78. De Boer JM, Overmars HA, Bakker J, Gommers FJ, (1992) Analysis of two-dimensional protein patterns from developmental stages of the potato cyst-nematode, Globodera rostochiensis. Parasitology 105: 461–474.
79. Martin J, Abubucker S, Heizer E, Taylor CM, Mitreva M, (2012) Nematode.net update 2011: Addition of data sets and tools featuring next-generation sequencing data. Nucleic Acids Res 40: D720–D728.
80. 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 Biotech Biochem 71: 2095–2100.
81. Clough SJ, Bent AF, (1998) Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735–743.
82. 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.
83. Baum TJ, Wubben MTE, IiHardy KA, Su H, Rodermel SR, (2000) A screen for Arabidopsis thaliana mutants with altered susceptibility to Heterodera schachtii. J Nematol 32: 166–173.
84. Van Esse HP, Bolton MD, Stergiopoulos I, De Wit PJGM, Thomma BPHJ, (2007) The chitin-binding Cladosporium fulvum effector protein Avr4 is a virulence factor. Mol Plant Microbe Interact 20: 1092–1101.
85. Bouwmeester K, de Sain M, Weide R, Gouget A, Klamer S, et al. (2011) The lectin receptor kinase LecRK-I.9 is a novel Phytophthora resistance component and a potential host target for a RXLR effector. PLoS Pathog 7: e1001327.
86. van de Mortel JE, de Vos RCH, Dekkers E, Pineda A, Guillod L, et al. (2012) Metabolic and transcriptomic changes induced in arabidopsis by the rhizobacterium Pseudomonas fluorescens SS101. Plant Physiol 160: 2173–2188.
87. Pieterse CMJ, Van Wees SCM, Hoffland E, Van Pelt JA, Van Loon LC, (1996) Systemic resistance in Arabidopsis induced by biocontrol bacteria is independent of salicylic acid accumulation and pathogenesis-related gene expression. Plant Cell 8: 1225–1237.
88. Gómez-Gómez L, Felix G, Boller T, (1999) A single locus determines sensitivity to bacterial flagellin in Arabidopsis thaliana. Plant J 18: 277–284.
89. Robinson MD, McCarthy DJ, Smyth GK, (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139–140.
90. Tanz SK, Castleden I, Hooper CM, Vacher M, Small I, et al. (2013) SUBA3: A database for integrating experimentation and prediction to define the SUBcellular location of proteins in Arabidopsis. Nucleic Acids Res 41: D1185–D1191.