Disruption of ethylene responses by Turnip mosaic virus mediates suppression of plant defense against the green peach aphid vector

Plant Physiology

Volumn 169, Issue 1, 2015, Pages 209-218

  Casteel, Clare L ^a   De Alwis, Manori ^b   Bak, Aurélie ^a   Dong, Haili ^c   Whitham, Steven A ^c   Jander, Georg ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Boyce Thompson Institute for Plant Research   (United States)

^c IOWA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOPENTANE DERIVATIVE; ETHYLENE; ETHYLENE DERIVATIVE; JASMONIC ACID; OXYLIPIN; PHYTOHORMONE; SALICYLIC ACID;

ANIMAL; APHID; ARABIDOPSIS; GENETICS; HOST PARASITE INTERACTION; IMMUNOLOGY; INSECT VECTOR; METABOLISM; PHYSIOLOGY; PLANT DISEASE; POTYVIRUS; RAPESEED; SIGNAL TRANSDUCTION; VIROLOGY;

ANIMALS; APHIDS; ARABIDOPSIS; BRASSICA NAPUS; CYCLOPENTANES; ETHYLENES; HOST-PARASITE INTERACTIONS; INSECT VECTORS; OXYLIPINS; PLANT DISEASES; PLANT GROWTH REGULATORS; POTYVIRUS; SALICYLIC ACID; SIGNAL TRANSDUCTION;

EID: 84940944400     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.15.00332     Document Type: Article

References (73)

1. Adams E, Turner J (2010) COI1, a jasmonate receptor, is involved in ethylene-induced inhibition of Arabidopsis root growth in the light. J Exp Bot 61: 4373-4386
2. Alazem M, Lin NS (2015) Roles of plant hormones in the regulation of hostvirus interactions. Mol Plant Pathol 16: 529-540
3. Alonso JM, Hirayama T, Roman G, Nourizadeh S, Ecker JR (1999) EIN2, a bifunctional transducer of ethylene and stress responses in Arabidopsis. Science 284: 2148-2152
4. Amrhein N, Wenker D (1979) Novel inhibitors of ethylene production in higher plants. Plant Cell Physiol 20: 1635-1642
5. Anindya R, Savithri HS (2004) Potyviral NIa proteinase, a proteinase with novel deoxyribonuclease activity. J Biol Chem 279: 32159-32169
6. Argandoña VH, Chaman M, Cardemil L, Muñoz O, Zúñiga GE, Corcuera LJ (2001) Ethylene production and peroxidase activity in aphid-infested barley. J Chem Ecol 27: 53-68
7. Bari R, Jones JD (2009) Role of plant hormones in plant defence responses. Plant Mol Biol 69: 473-488
8. Brown RL, Kazan K, McGrath KC, Maclean DJ, Manners JM (2003) A role for the GCC-box in jasmonate-mediated activation of the PDF1.2 gene of Arabidopsis. Plant Physiol 132: 1020-1032
9. Bush J, Jander G, Ausubel FM (2006) Prevention and control of pests and diseases. In J Salinas, JJ Sanchez-Serrano, eds, Arabidopsis Protocols, Ed 2. Humana Press, Totowa, NJ, pp 13-25
10. Carr JP, Lewsey MG, Palukaitis P (2010) Signaling in induced resistance. Adv Virus Res 76: 57-121
11. Casteel CL, Hansen AK (2014) Evaluating insect-microbiomes at the plantinsect interface. J Chem Ecol 40: 836-847
12. Casteel CL, Jander G (2013) New synthesis: investigating mutualisms in virus-vector interactions. J Chem Ecol 39: 809
13. Casteel CL, Yang C, Nanduri AC, De Jong HN, Whitham SA, Jander G (2014) The NIa-Pro protein of Turnip mosaic virus improves growth and reproduction of the aphid vector, Myzus persicae (green peach aphid). Plant J 77: 653-663
14. Chen L, Zhang L, Li D, Wang F, Yu D (2013) WRKY8 transcription factor functions in the TMV-cg defense response by mediating both abscisic acid and ethylene signaling in Arabidopsis. Proc Natl Acad Sci USA 110: E1963-E1971
15. Clay NK, Adio AM, Denoux C, Jander G, Ausubel FM (2009) Glucosinolate metabolites required for an Arabidopsis innate immune response. Science 323: 95-101
16. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacteriummediated transformation of Arabidopsis thaliana. Plant J 16: 735-743
17. de Vos M, Kim JH, Jander G (2007) Biochemistry and molecular biology of Arabidopsis-aphid interactions. Bio Essays 29: 871-883
18. Ellis C, Karafyllidis I, Turner JG (2002) Constitutive activation of jasmonate signaling in an Arabidopsis mutant correlates with enhanced resistance to Erysiphe cichoracearum, Pseudomonas syringae, and Myzus persicae. Mol Plant Microbe Interact 15: 1025-1030
19. Endres MW, Gregory BD, Gao Z, Foreman AW, Mlotshwa S, Ge X, Pruss GJ, Ecker JR, Bowman LH, Vance V (2010) Two plant viral suppressors of silencing require the ethylene-inducible host transcription factor RAV2 to block RNA silencing. PLoS Pathog 6: e1000729
20. Erb M, Meldau S, Howe GA (2012) Role of phytohormones in insectspecific plant reactions. Trends Plant Sci 17: 250-259
21. Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopath 43: 205-227
22. Guo H, Ecker JR (2003) Plant responses to ethylene gas are mediated by SCF(EBF1/EBF2)-dependent proteolysis of EIN3 transcription factor. Cell 115: 667-677
23. Haikonen T, Rajamäki ML, Tian YP, Valkonen JP (2013) Mutation of a short variable region in HCPro protein of Potato virus A affects interactions with a microtubule-associated protein and induces necrotic responses in tobacco. Mol Plant Microbe Interact 26: 721-733
24. Hall BP, Shakeel SN, Amir M, Ul Haq N, Qu X, Schaller GE (2012) Histidine kinase activity of the ethylene receptor ETR1 facilitates the ethylene response in Arabidopsis. Plant Physiol 159: 682-695
25. Han HE, Sellamuthu S, Shin BH, Lee YJ, Song S, Seo JS, Baek IS, Bae J, Kim H, Yoo YJ, et al (2010) The nuclear inclusion a (NIa) protease of Turnip mosaic virus (TuMV) cleaves amyloid-b. PLoS One 5: e15645
26. Howe GA, Jander G (2008) Plant immunity to insect herbivores. Annu Rev Plant Biol 59: 41-66
27. Jander G, Howe G (2008) Plant interactions with arthropod herbivores: state of the field. Plant Physiol 146: 801-803
28. Jones JD, Dangl JL (2006) The plant immune system. Nature 444: 323-329
29. Kang H, Lee YJ, Goo JH, Park WJ (2001) Determination of the substrate specificity of Turnip mosaic virus NIa protease using a genetic method. J Gen Virol 82: 3115-3117
30. Kennedy JS, Day MF, Eastop VF (1962) A Conspectus of Aphids as Vectors of Plant Viruses. Commonwealth Institute of Entomology, London
31. Kim B, Masuta C, Matsuura H, Takahashi H, Inukai T (2008) Veinal necrosis induced by Turnip mosaic virus infection in Arabidopsis is a form of defense response accompanying HR-like cell death. Mol Plant Microbe Interact 21: 260-268
32. Koyama T (2014) The roles of ethylene and transcription factors in the regulation of onset of leaf senescence. Front Plant Sci 5: 650
33. Lellis AD, Kasschau KD, Whitham SA, Carrington JC (2002) Loss-ofsusceptibility mutants of Arabidopsis thaliana reveal an essential role for eIF(iso)4E during potyvirus infection. Curr Biol 12: 1046-1051
34. Lewsey MG, Murphy AM, Maclean D, Dalchau N, Westwood JH, Macaulay K, Bennett MH, Moulin M, Hanke DE, Powell G, et al (2010) Disruption of two defensive signaling pathways by a viral RNA silencing suppressor. Mol Plant Microbe Interact 23: 835-845
35. Li R, Weldegergis BT, Li J, Jung C, Qu J, Sun Y, Qian H, Tee C, van Loon JJ, Dicke M, et al (2014) Virulence factors of geminivirus interact with MYC2 to subvert plant resistance and promote vector performance. Plant Cell 26: 4991-5008
36. Lorenzo O, Piqueras R, Sánchez-Serrano JJ, Solano R (2003) ETHYLENE RESPONSE FACTOR1 integrates signals from ethylene and jasmonate pathways in plant defense. Plant Cell 15: 165-178
37. Louis J, Shah J (2013) Arabidopsis thaliana-Myzus persicae interaction: shaping the understanding of plant defense against phloem-feeding aphids. Front Plant Sci 4: 213
38. Love AJ, Laval V, Geri C, Laird J, Tomos AD, Hooks MA, Milner JJ (2007) Components of Arabidopsis defense-and ethylene-signaling pathways regulate susceptibility to Cauliflower mosaic virus by restricting longdistance movement. Mol Plant Microbe Interact 20: 659-670
39. Love AJ, Yun BW, Laval V, Loake GJ, Milner JJ (2005) Cauliflower mosaic virus, a compatible pathogen of Arabidopsis, engages three distinct defense-signaling pathways and activates rapid systemic generation of reactive oxygen species. Plant Physiol 139: 935-948
40. Lu J, Li J, Ju H, Liu X, Erb M, Wang X, Lou Y (2014) Contrasting effects of ethylene biosynthesis on induced plant resistance against a chewing and a piercing-sucking herbivore in rice. Mol Plant 7: 1670-1682
41. Mandadi KK, Pyle JD, Scholthof KB (2014) Comparative analysis of antiviral responses in Brachypodium distachyon and Setaria viridis reveals conserved and unique outcomes among C3 and C4 plant defenses. Mol Plant Microbe Interact 27: 1277-1290
42. Mantelin S, Bhattarai KK, Kaloshian I (2009) Ethylene contributes to potato aphid susceptibility in a compatible tomato host. New Phytol 183: 444-456
43. Martín Martín A, Cabrera Poch HL, Martínez Herrera D, Ponz F (1999) Resistances to Turnip mosaic potyvirus in Arabidopsis thaliana. Mol Plant Microbe Interact 12: 1016-1021
44. Mauck KE, De Moraes CM, Mescher MC (2010) Deceptive chemical signals induced by a plant virus attract insect vectors to inferior hosts. Proc Natl Acad Sci USA 107: 3600-3605
45. Mauck KE, De Moraes CM, Mescher MC (2014) Biochemical and physiological mechanisms underlying effects of Cucumber mosaic virus on host-plant traits that mediate transmission by aphid vectors. Plant Cell Environ 37: 1427-1439
46. Mewis I, Appel HM, Hom A, Raina R, Schultz JC (2005) Major signaling pathways modulate Arabidopsis glucosinolate accumulation and response to both phloem-feeding and chewing insects. Plant Physiol 138: 1149-1162
47. Miller HL, Neese PA, Ketring DL, Dillwith JW (1994) Involvement of ethylene in aphid infestation of barley. J Plant Growth Regul 13: 167-171
48. Mur LAJ, Kenton P, Atzorn R, Miersch O, Wasternack C (2006) The outcomes of concentration-specific interactions between salicylate and jasmonate signaling include synergy, antagonism, and oxidative stress leading to cell death. Plant Physiol 140: 249-262
49. Nault LR (1997) Arthropod transmission of plant viruses: a new synthesis. Ann Entomol Soc Am 90: 521-541
50. Nguyen HD, Tomitaka Y, Ho SY, Duchêne S, Vetten HJ, Lesemann D, Walsh JA, Gibbs AJ, Ohshima K (2013) Turnip mosaic potyvirus probably first spread to Eurasian Brassica crops from wild orchids about 1000 years ago. PLoS One 8: e55336
51. Penninckx IA, Thomma BP, Buchala A, Métraux JP, Broekaert WF (1998) Concomitant activation of jasmonate and ethylene response pathways is required for induction of a plant defensin gene in Arabidopsis. Plant Cell 10: 2103-2113
52. Pieterse CM, Van der Does D, Zamioudis C, Leon-Reyes A, Van Wees SC (2012) Hormonal modulation of plant immunity. Annu Rev Cell Dev Biol 28: 489-521
53. Qiao H, Chang KN, Yazaki J, Ecker JR (2009) Interplay between ethylene, ETP1/ETP2 F-box proteins, and degradation of EIN2 triggers ethylene responses in Arabidopsis. Genes Dev 23: 512-521
54. Rajamäki ML, Valkonen JPT (2009) Control of nuclear and nucleolar localization of nuclear inclusion protein a of picorna-like Potato virus A in Nicotiana species. Plant Cell 21: 2485-2502
55. Ralhan A, Schöttle S, Thurow C, Iven T, Feussner I, Polle A, Gatz C (2012) The vascular pathogen Verticillium longisporum requires a jasmonic acid-independent COI1 function in roots to elicit disease symptoms in Arabidopsis shoots. Plant Physiol 159: 1192-1203
56. Rasmann S, De Vos M, Casteel CL, Tian D, Halitschke R, Sun JY, Agrawal AA, Felton GW, Jander G (2012) Herbivory in the previous generation primes plants for enhanced insect resistance. Plant Physiol 158: 854-863
57. Sánchez F, Martínez-Herrera D, Aguilar I, Ponz F (1998) Infectivity of Turnip mosaic potyvirus cDNA clones and transcripts on the systemic host Arabidopsis thaliana and local lesion hosts. Virus Res 55: 207-219
58. Shattuck VI (1992) The biology, epidemiology, and control of Turnip mosaic virus. Hortic Rev (Am Soc Hortic Sci) 14: 199-238
59. Sisler EC (2006) The discovery and development of compounds counteracting ethylene at the receptor level. Biotechnol Adv 24: 357-367
60. Soeno K, Goda H, Ishii T, Ogura T, Tachikawa T, Sasaki E, Yoshida S, Fujioka S, Asami T, Shimada Y (2010) Auxin biosynthesis inhibitors, identified by a genomics-based approach, provide insights into auxin biosynthesis. Plant Cell Physiol 51: 524-536
61. Solano R, Stepanova A, Chao Q, Ecker JR (1998) Nuclear events in ethylene signaling: a transcriptional cascade mediated by ETHYLENEINSENSITIVE3 and ETHYLENE-RESPONSE-FACTOR1. Genes Dev 12: 3703-3714
62. Stepanova AN, Alonso JM (2005) Arabidopsis ethylene signaling pathway. Sci STKE 2005: cm4
63. Tomlinson JA (1987) Epidemiology and control of viral diseases of vegetables. Ann Appl Biol 110: 661-681
64. Urcuqui-Inchima S, Haenni AL, Bernardi F (2001) Potyvirus proteins: a wealth of functions. Virus Res 74: 157-175
65. Van der Ent S, Van Wees SC, Pieterse CM (2009) Jasmonate signaling in plant interactions with resistance-inducing beneficial microbes. Phytochemistry 70: 1581-1588
66. van Loon LC, Geraats BPJ, Linthorst HJM (2006) Ethylene as a modulator of disease resistance in plants. Trends Plant Sci 11: 184-191
67. Verhage A, van Wees SCM, Pieterse CMJ (2010) Plant immunity: it’s the hormones talking, but what do they say? Plant Physiol 154: 536-540
68. Walsh JA, Jenner CE (2002) Turnip mosaic virus and the quest for durable resistance. Mol Plant Pathol 3: 289-300
69. Wei T, Zhang C, Hong J, Xiong R, Kasschau KD, Zhou X, Carrington JC, Wang A (2010) Formation of complexes at plasmodesmata for potyvirus intercellular movement is mediated by the viral protein P3N-PIPO. PLoS Patho 6: e1000962
70. Wu C, Avila CA, Goggin FL (2015) The ethylene response factor Pti5 contributes to potato aphid resistance in tomato independent of ethylene signalling. J Exp Bot 66: 559-570
71. Yang JY, Iwasaki M, Machida C, Machida Y, Zhou X, Chua NH (2008) bC1, the pathogenicity factor of TYLCCNV, interacts with AS1 to alter leaf development and suppress selective jasmonic acid responses. Genes Dev 22: 2564-2577
72. Yasaka R, Ohba K, Schwinghamer MW, Fletcher J, Ochoa-Corona FM, Thomas JE, Ho SY, Gibbs AJ, Ohshima K (2015) Phylodynamic evidence of the migration of Turnip mosaic potyvirus from Europe to Australia and New Zealand. J Gen Virol 96: 701-713
73. Zhang T, Luan JB, Qi JF, Huang CJ, Li M, Zhou XP, Liu SS (2012) Begomovirus-whitefly mutualism is achieved through repression of plant defences by a virus pathogenicity factor. Mol Ecol 21: 1294-1304