The ethylene response factor Pti5 contributes to potato aphid resistance in tomato independent of ethylene signalling

Journal of Experimental Botany

Volumn 66, Issue 2, 2015, Pages 559-570

  Wu, Chengjun ^a   Avila, Carlos A ^a,b   Goggin, Fiona L ^a  

^a UNIVERSITY OF ARKANSAS   (United States)

^b TEXAS A AND M UNIVERSITY   (United States)

Author keywords

Basal resistance; EREBP; ERF; insect resistance; Macrosiphum euphorbiae; Mi 1.2

Indexed keywords

APHIDIDAE; HEXAPODA; LYCOPERSICON ESCULENTUM; MACROSIPHUM EUPHORBIAE; SOLANUM TUBEROSUM;

CYCLOPENTANE DERIVATIVE; ETHYLENE; ETHYLENE DERIVATIVE; JASMONIC ACID; OXYLIPIN; SALICYLIC ACID; VEGETABLE PROTEIN;

ANIMAL; ANTIBIOSIS; APHID; BIOLOGICAL MODEL; DISEASE RESISTANCE; GENE EXPRESSION REGULATION; GENETICS; GENOTYPE; GROWTH, DEVELOPMENT AND AGING; HOST PARASITE INTERACTION; IMMUNOLOGY; METABOLISM; PARASITOLOGY; PHYSIOLOGY; PLANT DISEASE; PLANT GENE; POTATO; SIGNAL TRANSDUCTION; TOMATO; TRANSGENIC PLANT;

ANIMALS; ANTIBIOSIS; APHIDS; CYCLOPENTANES; DISEASE RESISTANCE; ETHYLENES; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GENOTYPE; HOST-PARASITE INTERACTIONS; LYCOPERSICON ESCULENTUM; MODELS, BIOLOGICAL; OXYLIPINS; PLANT DISEASES; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; SALICYLIC ACID; SIGNAL TRANSDUCTION; SOLANUM TUBEROSUM;

EID: 84922445598     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/eru472     Document Type: Article

References (74)

1. Anderson JA, Peters DC. 1994. Ethylene production from wheat seedlings infested with biotypes of Schizaphis graminum (Homoptera: Aphididae). Environmental Entomology 23, 992-998.
2. Anderson VA, Haley SD, Peairs FB, van Eck L, Leach JE, Lapitan NL. 2014. Virus-induced gene silencing suggests (1,3;1,4)-β-glucanase is a susceptibility factor in the compatible Russian wheat aphid-wheat interaction. Molecular Plant-Microbe Interactions 27, 913-922.
3. Anstead J, Samuel P, Song N, Wu C, Thompson GA, Goggin F. 2010. Activation of ethylene-related genes in response to aphid feeding on resistant and susceptible melon and tomato plants. Entomologia Experimentalis et Applicata 134, 170-181.
4. Argandona VH, Chaman M, Cardemil L, Munoz O, Zuniga GE, Corcuera LJ. 2001. Ethylene production and peroxidase activity in aphidinfested barley. Journal of Chemical Ecology 27, 53-68.
5. Avila CA, Arevalo-Soliz LM, Jia LL, Navarre DA, Chen Z, Howe GA, Meng QW, Smith JE, Goggin FL. 2012. Loss of function of FATTY ACID DESATURASE7 in tomato enhances basal aphid resistance in a salicylatedependent manner. Plant Physiology 158, 2028-2041.
6. Avila CA, Arevalo-Soliz LM, Lorence A, Goggin FL. 2013. Expression of α-DIOXYGENASE 1 in tomato and Arabidopsis contributes to plant defenses against aphids. Molecular Plant-Microbe Interactions 26, 977-986.
7. Berrocal-Lobo M, Molina A, Solano R. 2002. Constitutive expression of ETHYLENE-RESPONSE-FACTOR1 in Arabidopsis confers resistance to several necrotrophic fungi. The Plant Journal 29, 23-32.
8. Boughton AJ, Hoover K, Felton GW. 2006. Impact of chemical elicitor applications on greenhouse tomato plants and population growth of the green peach aphid, Myzus persicae. Entomologia Experimentalis et Applicata 120, 175-188.
9. Brading PA, Hammond-Kosack KE, Parr A, Jones JDG. 2000. Salicylic acid is not required for Cf-2- and Cf-9-dependent resistance of tomato to Cladosporium fulvum. The Plant Journal 23, 305-318.
10. Büttner M, Singh KB. 1997. Arabidopsis thaliana ethylene-responsive element binding protein (AtEBP), an ethylene-inducible, GCC box DNAbinding protein interacts with an ocs element binding protein. Proceedings of the National Academy of Sciences, USA 94, 5961-5966.
11. Chakravarthy S, Tuori RP, D'Ascenzo MD, Fobert PR, Després C, Martin GB. 2003. The tomato transcription factor Pti4 regulates defenserelated gene expression via GCC box and non-GCC box cis elements. The Plant Cell Online 15, 3033-3050.
12. Cheng M-C, Liao P-M, Kuo W-W, Lin T-P. 2013. The Arabidopsis ETHYLENE RESPONSE FACTOR1 regulates abiotic stress-responsive gene expression by binding to different cis-acting elements in response to different stress signals. Plant Physiology 162, 1566-1582.
13. Dangl JL, Jones JD. 2001. Plant pathogens and integrated defence responses to infection. Nature 411, 826-833.
14. De Boer K, Tilleman S, Pauwels L, Vanden Bossche R, De Sutter V, Vanderhaeghen R, Hilson P, Hamill JD, Goossens A. 2011. APETALA2/ETHYLENE RESPONSE FACTOR and basic helix-loop-helix tobacco transcription factors cooperatively mediate jasmonate-elicited nicotine biosynthesis. The Plant Journal 66, 1053-1065.
15. de Wit PJ. 2007. How plants recognize pathogens and defend themselves. Cellular and Molecular Life Sciences 64, 2726-2732.
16. Dillwith JW, Berberet RC, Bergman DK, Neese PA, Edwards RM, McNew RW. 1991. Plant biochemistry and aphid populations: studies on the spotted alfalfa aphid, Therioaphis maculata. Archives of Insect Biochemistry and Physiology 17, 235-251.
17. Eyal Y, Meller Y, Lev-Yadun S, Fluhr R. 1993. A basic-type PR-1 promoter directs ethylene responsiveness, vascular and abscission zonespecific expression. The Plant Journal 4, 225-234.
18. Fujimoto SY, Ohta M, Usui A, Shinshi H, Ohme-Takagi M. 2000. Arabidopsis ethylene-responsive element binding factors act as transcriptional activators or repressors of GCC box-mediated gene expression. Plant Cell 12, 393-404.
19. Gaffney T, Friedrich L, Vernooij B, Negrotto D, Nye G, Uknes S, Ward E, Kessmann H, Ryals J. 1993. Requirement of salicylic acid for the induction of systemic acquired resistance. Science 261, 754-756.
20. Goggin F, Shah G, Williamson V, Ullman D. 2004. Instability of Mi-mediated nematode resistance in transgenic tomato plants. Molecular Breeding 13, 357-364.
21. Goggin FL, Williamson VM, Ullman DE. 2001. Variability in the response of Macrosiphum euphorbiae and Myzus persicae (Hemiptera: Aphididae) to the tomato resistance gene Mi. Environmental Entomology 30, 101-106.
22. Goggin FL. 2007. Plant-aphid interactions: molecular and ecological perspectives. Current Opinion in Plant Biology 10, 399-408.
23. Gu Y-Q, Yang C, Thara VK, Zhou J, Martin GB. 2000. Pti4 is induced by ethylene and salicylic acid, and its product is phosphorylated by the Pto kinase. Plant Cell 12, 771-785.
24. Harel YM, Mehari ZH, Rav-David D, Elad Y. 2014. Systemic resistance to gray mold induced in tomato by benzothiadiazole and Trichoderma harzianum T39. Phytopathology 104, 150-157.
25. He P, Warren RF, Zhao T, Shan L, Zhu L, Tang X, Zhou J-M. 2001. Overexpression of Pti5 in tomato potentiates pathogen-induced defense gene expression and enhances disease resistance to Pseudomonas syringae pv. tomato. Molecular Plant-Microbe Interactions 14, 1453-1457.
26. Howe GA, Ryan CA. 1999. Suppressors of systemin signaling identify genes in the tomato wound response pathway. Genetics 153, 1411-1421.
27. Huai Q, Xia Y, Chen Y, Callahan B, Li N, Ke H. 2001. Crystal Structures of 1-aminocyclopropane-1-carboxylate (ACC) synthase in complex with aminoethoxyvinylglycine and pyridoxal-5?-phosphate provide new insight into catalytic mechanisms. Journal of Biological Chemistry 276, 38210-38216.
28. Kaloshian I, Yaghoobi J, Liharska T, et al. 1998. Genetic and physical localization of the root-knot nematode resistance locus Mi in tomato. Molecular and General Genetics 257, 376-385.
29. Klee HJ, Hayford MB, Kretzmer KA, Barry GF, Kishore GM. 1991. Control of ethylene synthesis by expression of a bacterial enzyme in transgenic tomato plants. Plant Cell 3, 1187-1193.
30. Knoester M, van Loon LC, van den Heuvel J, Hennig J, Bol JF, Linthorst HJM. 1998. Ethylene-insensitive tobacco lacks nonhost resistance against soil-borne fungi. Proceedings of the National Academy of Sciences,USA 95, 1933-1937.
31. Li C, Liu G, Xu C, Lee GI, Bauer P, Ling HQ, Ganal MW, Howe GA. 2003. The tomato suppressor of prosystemin-mediated responses2 gene encodes a fatty acid desaturase required for the biosynthesis of jasmonic acid and the production of a systemic wound signal for defense gene expression. Plant Cell 15, 1646-1661.
32. Li C, Schilmiller AL, Liu G, et al. 2005. Role of β-oxidation in jasmonate biosynthesis and systemic wound signaling in tomato. Plant Cell 17, 971-986.
33. Li J, Shan L, Zhou J-M, Tang X. 2002. Overexpression of Pto induces a salicylate-independent cell death but inhibits necrotic lesions caused by salicylate-deficiency in tomato plants. Molecular Plant-Microbe Interactions 15, 654-661.
34. Licausi F, Ohme-Takagi M, Perata P. 2013. APETALA2/Ethylene responsive factor (AP2/ERF) transcription factors: mediators of stress responses and developmental programs. New Phytologist 199, 639-649.
35. Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi-Shinozaki K, Shinozaki K. 1998. Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 10, 1391-1406.
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, Gobbato E, Mondal HA, Feys BJ, Parker JE, Shah J. 2012. Discrimination of Arabidopsis PAD4 activities in defense against green peach aphid and pathogens. Plant Physiology 158, 1860-1872.
38. Mantelin S, Bhattarai KK, Kaloshian I. 2009. Ethylene contributes to potato aphid susceptibility in a compatible tomato host. New Phytologist 183, 444-456.
39. Martinez de Ilarduya O, Xie Q, Kaloshian I. 2003. Aphid-induced defense responses in Mi-1-mediated compatible and incompatible tomato interactions. Molecular Plant-Microbe Interactions 16, 699-708.
40. Meng X, Xu J, He Y, Yang K-Y, Mordorski B, Liu Y, Zhang S. 2013. Phosphorylation of an ERF transcription factor by Arabidopsis MPK3/ MPK6 regulates plant defense gene induction and fungal resistance. Plant Cell 25, 1126-1142.
41. Miller HL, Neese PA, Ketring DL, Dillwith JW. 1994. Involvement of ethylene in aphid infestation of barley. Journal of Plant Growth Regulation 13, 167-171.
42. Milligan S, Bodeau J, Yaghoobi J, Kaloshian I, Zabel P, Williamson V. 1998. The root knot nematode resistance gene Mi from tomato is a member of the leucine zipper, nucleotide binding, leucine-rich repeat family of plant genes. Plant Cell 10, 1307-1319.
43. Nakano T, Suzuki K, Fujimura T, Shinshi H. 2006. Genome-wide analysis of the erf gene family in Arabidopsis and rice. Plant Physiology 140, 411-432.
44. Navarro L, Zipfel C, Rowland O, Keller I, Robatzek S, Boller T, Jones JD. 2004. The transcriptional innate immune response to flg22. Interplay and overlap with Avr gene-dependent defense responses and bacterial pathogenesis. Plant Physiology 135, 1113-1128.
45. Niks RE, Marcel TC. 2009. Nonhost and basal resistance: how to explain specificity? New Phytologist 182, 817-828.
46. O'Donnell PJ, Calvert C, Atzorn R, Wasternack C, Leyser HMO, Bowles DJ. 1996. Ethylene as a signal mediating the wound response of tomato plants. Science 274, 1914-1917.
47. Ogata T, Kida Y, Tochigi M, Matsushita Y. 2013. Analysis of the cell death-inducing ability of the ethylene response factors in group VIII of the AP2/ERF family. Plant Science 209, 12-23.
48. Ohme-Takagi M, Shinshi H. 1995. Ethylene-inducible DNA binding proteins that interact with an ethylene-responsive element. Plant Cell 7, 173-182.
49. Pallipparambil GR, Reese JC, Avila CA, Louis JM, Goggin FL. 2010. Mi-mediated aphid resistance in tomato: tissue localization and impact on the feeding behavior of two potato aphid clones with differing levels of virulence. Entomologia Experimentalis et Applicata 135, 295-307.
50. Pedley KF, Martin GB. 2003. Molecular basis of Pto-mediated resistance to bacterial speck disease in tomato. Annual Review of Phytopathology 41, 215-243.
51. Pfaffl MW. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research 29, e45.
52. Powell G, Tosh CR, Hardie J. 2006. Host plant selection by aphids: behavioral, evolutionary, and applied perspectives. Annual Review of Entomology 51, 309-330.
53. Rasmussen R. 2000. Quantification on the LightCycler. In: Meuer S, Wittwer C, Nakagawara K, eds. Rapid cycle real-time PCR: methods and applications. Heidelberg: Springer Press, 21-34.
54. Reed AJ, Magin KM, Anderson JS, Austin GD, Rangwala T, Linde DC, Love JN, Rogers SG, Fuchs RL. 1995. Delayed ripening tomato plants expressing the enzyme 1-aminocyclopropane-1-carboxylic acid deaminase. 1. Molecular characterization, enzyme expression, and fruit ripening traits. Journal of Agricultural and Food Chemistry 43, 1954-1962.
55. Rossi M, Goggin FL, Milligan SB, Kaloshian I, Ullman DE, Williamson VM. 1998. The nematode resistance gene Mi of tomato confers resistance against the potato aphid. Proceedings of the National Academy of Sciences, USA 95, 9750-9754.
56. Salmeron JM, Oldroyd GE, Rommens CM, Scofield SR, Kim HS, Lavelle DT, Dahlbeck D, Staskawicz BJ. 1996. Tomato Prf is a member of the leucine-rich repeat class of plant disease resistance genes and lies embedded within the Pto kinase gene cluster. Cell 86, 123-133.
57. Sewelam N, Kazan K, Thomas-Hall SR, Kidd BN, Manners JM, Schenk PM. 2013. Ethylene response factor 6 is a regulator of reactive oxygen species signaling in Arabidopsis. PLoS One 8, e70289.
58. Shoji T, Kajikawa M, Hashimoto T. 2010. Clustered transcription factor genes regulate nicotine biosynthesis in tobacco. Plant Cell 22, 3390-3409.
59. Smith CM, Chuang W-P. 2014. Plant resistance to aphid feeding: behavioral, physiological, genetic and molecular cues regulate aphid host selection and feeding. Pest Management Science 70, 528-540.
60. Solano R, Ecker JR. 1998. Ethylene gas: perception, signaling and response. Current Opinion in Plant Biology 1, 393-398.
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 & Development 12, 3703-3714.
62. Stockinger EJ, Gilmour SJ, Thomashow MF. 1997. Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the C-repeat/DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. Proceedings of the National Academy of Sciences, USA 94, 1035-1040.
63. Suzuki K, Suzuki N, Ohme-Takagi M, Shinshi H. 1998. Immediate early induction of mRNAs for ethylene-responsive transcription factors in tobacco leaf strips after cutting. The Plant Journal 15, 657-665.
64. Thara VK, Tang X, Gu YQ, Martin GB, Zhou J-M. 1999. Pseudomonas syringae pv tomato induces the expression of tomato EREBP-like genes Pti4 and Pti5 independent of ethylene, salicylate and jasmonate. The Plant Journal 20, 475-483.
65. Van der Does D, Leon-Reyes A, Koornneef A, et al. 2013. Salicylic acid suppresses jasmonic acid signaling downstream of SCFCOI1-JAZ by targeting GCC promoter motifs via transcription factor ORA59. Plant Cell 25, 744-761.
66. van der Fits L, Memelink J. 2000. ORCA3, a jasmonate-responsive transcriptional regulator of plant primary and secondary metabolism. Science 289, 295-297.
67. Vogel MO, Moore M, König K, Pecher P, Alsharafa K, Lee J, Dietz K-J. 2014. Fast retrograde signaling in response to high light involves metabolite export, MITOGEN-ACTIVATED PROTEIN KINASE6, and AP2/ ERF transcription factors in Arabidopsis. Plant Cell 26, 1151-1165.
68. von Dahl C, Baldwin I. 2007. Deciphering the role of ethylene in plantherbivore interactions. Journal of Plant Growth Regulation 26, 201-209.
69. Wu C, Jia L, Goggin FL. 2011. The reliability of TRV-based VIGS experiments in tomato is influenced by the size of the vector control. Molecular Plant Pathology 12, 299-305.
70. Xu Z-S, Chen M, Li L-C, Ma Y-Z. 2011. Functions and application of the AP2/ERF transcription factor family in crop improvement. Journal of Integrative Plant Biology 53, 570-585.
71. Yamamoto S, Suzuki K, Shinshi H. 1999. Elicitor-responsive, ethyleneindependent activation of GCC box-mediated transcription that is regulated by both protein phosphorylation and dephosphorylation in cultured tobacco cells. The Plant Journal 20, 571-579.
72. Yang Z, Tian L, Latoszek-Green M, Brown D, Wu K. 2005. Arabidopsis ERF4 is a transcriptional repressor capable of modulating ethylene and abscisic acid responses. Plant Molecular Biology 58, 585-596.
73. Yu Y-B, Yang SF. 1979. Auxin-induced ethylene production and its inhibition by aminoethyoxyvinylglycine and cobalt ion. Plant Physiology 64, 1074-1077.
74. Zhou J, Tang X, Martin GB. 1997. The Pto kinase conferring resistance to tomato bacterial speck disease interacts with proteins that bind a cis-element of pathogenesis-related genes. EMBO J 16, 3207-3218.