Expression of α-DIOXYGENASE 1 in tomato and arabidopsis contributes to plant defenses against aphids

Molecular Plant-Microbe Interactions

Volumn 26, Issue 8, 2013, Pages 977-986

  Avila, Carlos Augusto ^a   Arevalo Soliz, Lirio Milenka ^a,c   Lorence, Argelia ^b   Goggin, Fiona L ^a  

^a UNIVERSITY OF ARKANSAS   (United States)

^b ARKANSAS STATE UNIVERSITY   (United States)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETIC ACID DERIVATIVE; CYCLOPENTANE DERIVATIVE; DIOXYGENASE; JASMONIC ACID METHYL ESTER; OXYLIPIN; VEGETABLE PROTEIN;

ANIMAL; APHID; ARABIDOPSIS; ARTICLE; DRUG EFFECT; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; METABOLISM; PHYSIOLOGY; TOMATO;

ACETATES; ANIMALS; APHIDS; ARABIDOPSIS; CYCLOPENTANES; DIOXYGENASES; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, PLANT; GENE SILENCING; LYCOPERSICON ESCULENTUM; OXYLIPINS; PLANT PROTEINS;

EID: 84880062062     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-01-13-0031-R     Document Type: Article

References (64)

1. Argandona, V. H., Chaman, M., Cardemil, L., Munoz, O., Zuniga, G. E., and Corcuera, L. J. 2001. Ethylene production and peroxidase activity in aphid-infested barley. J. Chem. Ecol. 27: 53-68.
2. Arvidsson, S., Pérez-Rodríguez, P., and Mueller-Roeber, B. 2011. A growth phenotyping pipeline for Arabidopsis thaliana integrating image analysis and rosette area modeling for robust quantification of genotype effects. New Phytol. 191: 895-907.
3. Audenaert, K., De Meyer, G. B., and Höfte, M. M. 2002. Abscisic acid determines basal susceptibility of tomato to Botrytis cinerea and suppresses salicylic acid-dependent signaling mechanisms. Plant Physiol. 128: 491-501.
4. Avila, C. A., Arevalo-Soliz, L. M., Jia, L. L., Navarre, D. A., Chen, Z., Howe, G. A., Meng, Q. W., Smith, J. E., and Goggin, F. L. 2012. Loss of Function of FATTY ACID DESATURASE7 in tomato enhances basal aphid resistance in a salicylate-dependent manner. Plant Physiol. 158: 2028-2041.
5. Bannenberg, G., Martinez, M., Rodriguez, M., Lopez, M., de Leon, I., Hamberg, M., and Castresana, C. 2009. Functional analysis of alpha-DOX2, an active alpha-dioxygenase critical for normal development in tomato Plants. Plant Physiol. 151: 1421-1432.
6. Bell, E., Creelman, R. A., and Mullet, J. E. 1995. A chloroplast lipoxygenase is required for wound-induced jasmonic acid accumulation in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 92: 8675-8679.
7. Berner, J. M., and Van der Westhuizen, A. J. 2010. Inhibition of xanthine oxidase activity results in the inhibition of russian wheat aphid-induced defense enzymes. J. Chem. Ecol. 36: 1375-1380.
8. Blée, E. 2002. Impact of phyto-oxylipins in plant defense. Trends Plant Sci. 7: 315-322.
9. Boyes, D. C., Zayed, A. M., Ascenzi, R., McCaskill, A. J., Hoffman, N. E., Davis, K. R., and Gorlach, J. 2001. Growth stage-based phenotypic analysis of Arabidopsis: A model for high throughput functional genomics in plants. Plant Cell 13: 1499-1510.
10. Brading, P. A., Hammond-Kosack, K. E., Parr, A., and Jones, J. D. G. 2000. Salicylic acid is not required for Cf-2- and Cf-9-dependent resistance of tomato to Cladosporium fulvum. Plant J. 23: 305-318.
11. Chehab, E. W., Perea, J. V., Gopalan, B., Theg, S., and Dehesh, K. 2007. Oxylipin pathway in rice and Arabidopsis. J. Integr. Plant Biol. 49: 43-51.
12. De Vos, M., Van Oosten, V. R., Van Poecke, R. M. P., Van Pelt, J. A., Pozo, M. J., Mueller, M. J., Buchala, A. J., Métraux, J.-P., Van Loon, L. C., Dicke, M., and Pieterse, C. M. J. 2005. Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Mol. Plant-Microbe Interact. 18: 923-937.
13. Farmer, E. E., Alméras, E., and Krishnamurthy, V. 2003. Jasmonates and related oxylipins in plant responses to pathogenesis and herbivory. Curr. Opin. Plant Biol. 6: 372-378.
14. Feussner, I., and Wasternack, C. 2002. The lipoxygenase pathway. Ann. Rev. Plant Biol. 53: 275-297.
15. Fidantsef, A. L., Stout, M. J., Thaler, J. S., Duffey, S. S., and Bostock, R. M. 1999. Signal interactions in pathogen and insect attack: Expression of lipoxygenase, proteinase inhibitor II, and pathogenesis-related protein P4 in the tomato, Lycopersicon esculentum. Physiol. Mol. Plant Pathol. 54: 97-114.
16. Fonseca, S., Chini, A., Hamberg, M., Adie, B., Porzel, A., Kramell, R., Miersch, O., Wasternack, C., and Solano, R. 2009. (+)-7-Iso-jasmonoyl-L- isoleucine is the endogenous bioactive jasmonate. Nat. Chem. Biol. 5: 344-350.
17. Friedrich, L., Lawton, K., Ruess, W., Masner, P., Specker, N., Rella, M. G., Meier, B., Dincher, S., Staub, T., Uknes, S., Métraux, J.-P., Kessmann, H., and Ryals, J. 1996. A benzothiadiazole derivative induces systemic acquired resistance in tobacco. Plant J. 10: 61-70.
18. Gaffney, T., Friedrich, L., Vernooij, B., Negrotto, D., Nye, G., Uknes, S., Ward, E., Kessmann, H., and Ryals, J. 1993. Requirement of salicylic acid for the induction of systemic acquired resistance. Science 261: 754-756.
19. Gaquerel, E., Steppuhn, A., and Baldwin, I. T. 2012. Nicotiana attenuata α-DIOXYGENASE1 through its production of 2-hydroxylinolenic acid is required for intact plant defense expression against attack from Manduca sexta larvae. New Phytol. 196: 574-585
20. Gosset, V., Harmel, N., Gobel, C., Francis, F., Haubruge, E., Wathelet, J.- P., du Jardin, P., Feussner, I., and Fauconnier, M.-L. 2009. Attacks by a piercing-sucking insect (Myzus persicae Sultzer) or a chewing insect (Leptinotarsa decemlineata Say) on potato plants (Solanum tuberosum L.) induce differential changes in volatile compound release and oxylipin synthesis. J. Exp. Bot. 60: 1231-1240.
21. Halitschke, R., Gase, K., Hui, D. Q., Schmidt, D. D., and Baldwin, I. T. 2003. Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. VI. Microarray analysis reveals that most herbivore-specific transcriptional changes are mediated by fatty acid-amino acid conjugates. Plant Physiol. 131: 1894-1902.
22. Hamberg, M., Sanz, A., and Castresana, C. 1999. Alpha-oxidation of fatty acids in higher plants - Identification of a pathogen-inducible oxygenase (PIOX) as an alpha-dioxygenase and biosynthesis of 2- hydroperoxylinolenic acid. J. Biol. Chem. 274: 24503-24513.
23. Hamberg, M., Sanz, A., Rodriguez, M. J., Calvo, A. P., and Castresana, C. 2003. Activation of the fatty acid alpha-dioxygenase pathway during bacterial infection of tobacco leaves-Formation of oxylipins protecting against cell death. J. Biol. Chem. 278: 51796-51805.
24. Hamberg, M., de Leon, I. P., Rodriguez, M. J., and Castresana, C. 2005. Alpha-dioxygenases. Biochem. Biophys. Res. Comm. 338: 169-174.
25. Harmel, N., Delaplace, P., Blée, E., Du Jardin, P., and Fauconnier, M.-L. 2007. Myzus persicae Sulzer aphid contains oxylipins that originate from phloem sap. J. Plant Interact. 2: 31-40.
26. Heidel, A. J., and Baldwin, I. T. 2004. Microarray analysis of salicylic acid-and jasmonic acid-signalling in responses of Nicotiana attenuata to attack by insects from multiple feeding guilds. Plant Cell Environ. 27: 1362-1373.
27. Hermsmeier, D., Schittko, U., and Baldwin, I. T. 2001. Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. I. Large-scale changes in the accumulation of growth-and defense-related plant mRNAs. Plant Physiol. 125: 683-700.
28. Howe, G. A., and Ryan, C. A. 1999. Suppressors of systemin signaling identify genes in the tomato wound response pathway. Genetics 153: 1411-1421.
29. Howe, G. A., and Schilmiller, A. L. 2002. Oxylipin metabolism in response to stress. Curr. Opin. Plant Biol. 5: 230-236.
30. Howe, G. A., and Jander, G. 2008. Plant immunity to insect herbivores. Ann. Rev. Plant Biol. 59: 41-46.
31. Kerchev, P. I., Fenton, B., Foyer, C. H., and Hancock, R. D. 2011. Infestation of potato (Solanum tuberosum L.) by the peach-potato aphid (Myzus persicae Sulzer) alters cellular redox status and is influenced by ascorbate. Plant Cell Environ. 35: 430-440.
32. Kim, Y. C., Yi, S. Y., Mang, H. G., Kim, W. T., and Choi, D. 2002. Pathogen-induced expression of cylo-oxygenase homologue in hot pepper (Capsicum annuum cv. Pukang). J. Exp. Bot. 53: 383-385.
33. Koeduka, T., Matsui, K., Akakabe, Y., and Kajiwara, T. 2002. Catalytic properties of rice α-oxygenase. J. Biol. Chem. 277: 22648-22655.
34. Koeduka, T., Matsui, K., Hasegawa, M., Akakabe, Y., and Kajiwara, T. 2005. Rice fatty acid alpha-dioxygenase is induced by pathogen attack and heavy metal stress: Activation through jasmonate signaling. Plant Physiol. 162: 912-920.
35. Koszelak-Rosenblum, M., Krol, A. C., Simmons, D. M., Goulah, C. C., Wroblewski, L., and Malkowski, M. G. 2008. His-311 and Arg-559 are key residues involved in fatty acid oxygenation in pathogen-inducible oxygenase. J. Biol. Chem. 283: 24962-24971.
36. Li, C., Liu, G., Xu, C., Lee, G. I., Bauer, P., Ling, H. Q., Ganal, M. W., and Howe, G. A. 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.
37. Li, C., Schilmiller, A. L., Liu, G., Lee, G. I., Jayanty, S., Sageman, C., Vrebalov, J., Giovannoni, J. J., Yagi, K., Kobayashi, Y., and Howe, G. A. 2005. Role of beta-oxidation in jasmonate biosynthesis and systemic wound signaling in tomato. Plant Cell 17: 971-986.
38. Li, J., Shan, L., Zhou, J.-M., and Tang, X. 2002. Overexpression of Pto induces a salicylate-independent cell death but inhibits necrotic lesions caused by salicylate-deficiency in tomato plants. Mol. Plant-Microbe Interact. 15: 654-661.
39. Li, Q., Xie, Q.-G., Smith-Becker, J., Navarre, D. A., and Kaloshian, I. 2006. Mi-1-mediated aphid resistance involves salicylic acid and mitogen-activated protein kinase signaling cascades. Mol. Plant-Microbe Interact. 19: 655-664.
40. Madey, E., Nowack, L., and Thompson, J. 2002. Isolation and characterization of lipid in phloem sap of canola. Planta 214: 625-634.
41. Martinez de Ilarduya, O., Xie, Q. G., and Kaloshian, I. 2003. Aphidinduced defense responses in Mi-1-mediated compatible and incompatible tomato interactions. Mol. Plant-Microbe Interact. 16: 699-708.
42. McConn, M., Creelman, R. A., Bell, E., Mullet, J. E., and Browse, J. 1997. Jasmonate is essential for insect defense in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 94: 5473-5477.
43. Mohase, L., and van der Westhuizen, A. J. 2002. Salicylic acid is involved in resistance responses in the Russian wheat aphid-wheat interaction. Plant Physiol. 159: 585-590.
44. Moloi, M. J., and van der Westhuizen, A. J. 2006. The reactive oxygen species are involved in resistance responses of wheat to the Russian wheat aphid. Plant Physiol. 163: 1118-1125.
45. Mosblech, A., Feussner, I., and Heilmann, I. 2009. Oxylipins: Structurally diverse metabolites from fatty acid oxidation. Plant Physiol. Biochem. 47: 511-517.
46. Ozturk, Z. N., Talamé, V., Deyholos, M., Michalowski, C. B., Galbraith, D. W., Gozukirmizi, N., Tuberosa, R., and Bohnert, H. J. 2002. Monitoring large-scale changes in transcript abundance in drought-and salt-stressed barley. Plant Mol. Biol. 48: 551-573.
47. Pegadaraju, V., Knepper, C., Reese, J., and Shah, J. 2005. Premature leaf senescence modulated by the Arabidopsis PHYTOALEXIN DEFICIENT4 gene Is associated with defense against the phloem-feeding green peach aphid. Plant Physiology 139: 1927-1934.
48. Pfaffl, M. W. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29: e45-.
49. Ponce de Leon, I., Sanz, A., Hamberg, M., and Castresana, C. 2002. Involvement of the Arabidopsis α-DOX1 fatty acid dioxygenase in protection against oxidative stress and cell death. Plant J. 29: 61-72.
50. Prost, I., Dhondt, S., Rothe, G., Vicente, J., Rodriguez, M. J., Kift, N., Carbonne, F., Griffiths, G., Esquerre-Tugaye, M.-T., Rosahl, S., Castresana, C., Hamberg, M., and Fournier, J. 2005. Evaluation of the antimicrobial activities of plant oxylipins supports their involvement in defense against pathogens. Plant Physiol. 139: 1902-1913.
51. Rasmussen, R. 2000. Quantification on the LightCycler. Pages 21-34 in: Rapid cycle real-time PCR: Methods and applications, S. Meuer, C. Wittwer, and K. Nakagawara, eds. Springer Press, Heidelberg, Germany.
52. Sanz, A., Moreno, J. I., and Castresana, C. 1998. PIOX, a new pathogeninduced oxygenase with homology to animal cyclooxygenase. Plant Cell 10: 1523-1537.
53. Schuhegger, R., Ihring, A., Gantner, S., Bahnweg, G., Knappe, C., Vogg, G., Hutzler, P., Schmid, M., Van Breusegem, F., Eberl, L. E. O., Hartmann, A., and Langebartels, C. 2006. Induction of systemic resistance in tomato by N-acyl-L-homoserine lactone-producing rhizosphere bacteria. Plant Cell Environ. 29: 909-918.
54. Seki, M., Narusaka, M., Ishida, J., Nanjo, T., Fujita, M., Oono, Y., Kamiya, A., Nakajima, M., Enju, A., and Sakurai, T. 2002. Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J. 31: 279-292.
55. Sheard, L. B., Tan, X., Mao, H., Withers, J., Ben-Nissan, G., Hinds, T. R., Kobayashi, Y., Hsu, F.-F., Sharon, M., Browse, J., He, S. Y., Rizo, J., Howe, G. A., and Zheng, N. 2010. Jasmonate perception by inositol phosphate-potentiated COI1-JAZ co-receptor. Nature 468: 400-405.
56. Steppuhn, A., Gaquerel, E., and Baldwin, I. 2010. The two alpha-dox genes of Nicotiana attenuata: Overlapping but distinct functions in development and stress responses. BMC Plant Biol. 10: 171.
57. Tirajoh, A., Aung, T. S. T., McKay, A. B., and Plant, A. L. 2005. Stressresponsive alpha-dioxygenase expression in tomato roots. J. Exp. Bot. 56: 713-723.
58. Tjallingii, W. F., and Esch, T. H. 1993. Fine structure of aphid stylet routes in plant tissues in correlation with EPG signals. Physiol. Entomol. 18: 317-328.
59. Turner, J. G., Ellis, C., and Devoto, A. 2002. The jasmonate signal pathway. Plant Cell Online 14: S153-S164.
60. van der Biezen, E. A., Brandwagt, B. F., vanLeeuwen, W., Nijkamp, H. J. J., and Hille, J. 1996. Identification and isolation of the FEEBLY gene from tomato by transposon tagging. Mol. Gen. Genet. 251: 267-280.
61. Van Kan, J. A. L., Cozijnsen, T., Danhash, N., and Wit, P. J. G. M. 1995. Induction of tomato stress protein mRNAs by ethephon, 2,6-dichloroisonicotinic acid and salicylate. Plant Mol. Biol. 27: 1205-1213.
62. Vicente, J., Cascón, T., Vicedo, B., García-Agustín, P., Hamberg, M., and Castresana, C. 2012. Role of 9-Lipoxygenase and α-dioxygenase oxylipin pathways as modulators of local and systemic defense. Mol. Plant 5: 914-928.
63. Wang, L., Allmann, S., Wu, J., and Baldwin, I. T. 2008. Comparisons of LIPOXYGENASE3- and JASMONATE-RESISTANT4/6- silenced plants reveal that jasmonic acid and jasmonic acid-amino acid conjugates play different roles in herbivore resistance of Nicotiana attenuata. Plant Physiol. 146: 904-915.
64. Wu, C., Jia, L., and Goggin, F. L. 2011. The reliability of TRV-based VIGS experiments in tomato is influenced by the size of the vector control. Mol. Plant Pathol. 12: 299-305. Technology Initiative