Silencing of OPR3 in tomato reveals the role of OPDA in callose deposition during the activation of defense responses against Botrytis cinerea

Plant Journal

Volumn 81, Issue 2, 2015, Pages 304-315

  Scalschi, Loredana ^a   Sanmartín, Maite ^b   Camañes, Gemma ^a   Troncho, Pilar ^a   Sánchez Serrano, José J ^b   García Agustín, Pilar ^a   Vicedo, Begonya ^a  

^a UNIVERSITAT JAUME I   (Spain)

^b CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

Author keywords

Botrytis; callose; OPDA; OPR3 silencing; tomato plants

Indexed keywords

BIOCHEMISTRY; BIOSYNTHESIS; DEPOSITION; GENE EXPRESSION; PATHOGENS; PLANT CELL CULTURE; PLANTS (BOTANY);

BOTRYTIS; CALLOSE; OPDA; OPR3 SILENCING; TOMATO PLANTS;

FRUITS;

ARABIDOPSIS; BOTRYOTINIA FUCKELIANA; BOTRYTIS; LYCOPERSICON ESCULENTUM;

2-(2'-PYRIDYLDITHIO)BENZYLDIAZOACETATE; CALLOSE; DIAZONIUM COMPOUND; GLUCAN; PYRIDINE DERIVATIVE; VEGETABLE PROTEIN;

BOTRYTIS; GENETICS; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; TOMATO; TRANSGENIC PLANT;

BOTRYTIS; DIAZONIUM COMPOUNDS; GLUCANS; LYCOPERSICON ESCULENTUM; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; PYRIDINES;

EID: 84920727522     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12728     Document Type: Article

References (54)

1. Ahmad, S., Veyrat, N., Gordon-Weeks, R., et al. (2011) Benzoxazinoid metabolites regulate innate immunity against aphids and fungi in maize. Plant Physiol. 157, 317-327.
2. Asselbergh, B., Curvers, K., Franca, S.C., Audenaert, K., Vuylsteke, M., Van Breusegem, F., and, Hofte, M., (2007) Resistance to Botrytis cinerea in sitiens, an abscisic acid-deficient tomato mutant, involves timely production of hydrogen peroxide and cell wall modifications in the epidermis. Plant Physiol. 144, 1863-1877.
3. Berger, S., (2002) Jasmonate-related mutants of Arabidopsis as tools for studying stress signaling. Planta, 214, 497-504.
4. Blechert, S., Bockelmann, C., Füsslein, M., Schrader, V.T., Stelmach, B., Niesel, U., and, Weiler, E.W., (1999) Structure-activity analyses reveal the existence of two separate groups of active octadecanoids in elicitation of the tendril-coiling response of Bryonia dioica Jacq. Planta, 207, 470-479.
5. Blée, E., (1998) Phytooxylipins and plant defense reactions. Prog. Lipid Res. 37, 33-72.
6. Buseman, C.M., Tamura, P., Sparks, A.A., Baughman, E.J., Maatta, S., Zhao, J., Roth, M.R., Esch, S.W., Shah, J., and, Williams, T.D., (2006) Wounding stimulates the accumulation of glycerolipids containing oxophytodienoic acid and dinor-oxophytodienoic acid in Arabidopsis leaves. Plant Physiol. 142, 28-39.
7. Büttner, P., Koch, F., Voigt, K., Quidde, T., Risch, S., Blaich, R., Brückner, B., and, Tudzynski, P., (1994) Variations in ploidy among isolates of Botrytis cinerea: implications for genetic and molecular analyses. Curr. Genet. 25, 445-450.
8. Chehab, E.W., Kim, S., Savchenko, T., Kliebenstein, D., Dehesh, K., and, Braam, J., (2011) Intronic T-DNA insertion renders Arabidopsis opr3 a conditional jasmonic-acid producing mutant. Plant Physiol. 156, 770-778.
9. Chini, A., Fonseca, S., Fernandez, G., and, Adie, B., (2007) The JAZ family of repressors is the missing link in jasmonate signalling. Nature, 448, 666-671.
10. Creelman, R.A., and, Mullet, J.E., (1995) Jasmonic acid distribution and action in plants: regulation during development and response to biotic and abiotic stress. Proc. Natl Acad. Sci. USA, 92, 4114-4119.
11. Dave, A., and, Graham, I.A., (2012) Oxylipin signaling: a distinct role for the jasmonic acid precursor cis-(+)-12-oxo-phytodienoic acid (cis-OPDA). Front. Plant Sci. 3, 42.
12. Dave, A., Hernández, M.L., He, Z., Andriotis, V.M., Vaistij, F.E., Larson, T.R., and, Graham, I.A., (2011) 12-Oxo-phytodienoic acid accumulation during seed development represses seed germination in Arabidopsis. Plant Cell, 23, 583-599.
13. Denness, L., McKenna, J.F., Segonzac, C., Wormit, A., Madho, P., Bennett, M., Mansfield, J., Zipfel, C., and, Hamann, T., (2011) Cell wall damage-induced lignin biosynthesis is regulated by a reactive oxygen species- and jasmonic acid-dependent process in Arabidopsis. Plant Physiol. 156, 1364-1374.
14. Edwards, K., Johnstone, C., and, Thompson, C., (1991) A simple and rà pid method for the preparation of plant genomic DNA for PCR analysis. Nucleic Acids Res. 19, 1349.
15. Farmer, E.E., and, Ryan, C.A., (1992) Octadecanoid precursors of jasmonic acid activate the synthesis of wound-inducible proteinase inhibitors. Plant Cell, 4, 129-134.
16. Flors, V., Leyva, M.O., Vicedo, B., Finiti, I., Real, M.D., García-Agustín, P., Bennett, A.B., and, González-Bosch, C., (2007) Absence of the endo- β-1,4-glucanases Cel1 and Cel2 reduces susceptibility to Botrytis cinerea in tomato. Plant J. 52, 1027-1040.
17. Flors, V., Ton, J., van Doorn, R., Jakab, G., Garcia-Agustin, P., and, Mauch-Mani, B., (2008) Interplay between JA, SA and ABA signalling during basal and induced resistance against Pseudomonas syringae and Alternaria brassicicola. Plant J. 54, 81-92.
18. 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. 58, 344-350.
19. Glazebrook, J., (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu. Rev. Phytopathol. 43, 205-227.
20. Goetz, S., Hellwege, A., Stenzel, I., et al. (2012) Role of cis-12-oxo-phytodienoic acid in tomato embryo development. Plant Physiol. 158, 1715-1727.
21. Grant, M., and, Lamb, C., (2006) Systemic immunity. Curr. Opin. Plant Biol. 9, 414-420.
22. Hamiduzzaman, M.M., Jakab, G., Barnavon, L., Neuhaus, J.M., and, Mauch-Mani, B., (2005) β-aminobutyricacid induced resistance against downy mildew in grape vine acts through the potentiation of callose formation and jasmonic acid signaling. Mol. Plant Microbe Interact. 18, 819-829.
23. Heil, M., and, McKey, D., (2003) Protective ant-plant interactions as model systems in ecological and evolutionary research. Annu. Rev. Ecol. Evol. Syst. 34, 425-453.
24. 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.
25. Howe, G., and, Schilmiller, A., (2002) Oxylipin metabolism in response to stress. Curr. Opin. Plant Biol. 5, 230-236.
26. Howe, G., Lightner, A.J., Browse, J., and, Ryan, C.A., (1996) An octadecanoid pathway mutant (JL5) of tomato is compromised in signaling for defense against insect attack. Plant Cell, 8, 2067-2077.
27. Iriti, M., and, Faoro, F., (2009) Chitosan as a MAMP, searching for a PRR. Plant Signal. Behav. 4, 66-68.
28. Kravchuk, Z., Vicedo, B., Flors, V., Camañes, G., González-Bosch, C., and, García-Agustín, P., (2011) Priming for JA-dependent defenses using hexanoic acid is an effective mechanism to protect Arabidopsis against B. cinerea. J. Plant Physiol. 168, 359-366.
29. Laudert, D., and, Weiler, E.W., (1998) Allene oxide synthase: a major control point in Arabidopsis thaliana octadecanoid signalling. Plant J. 15, 675-684.
30. 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.
31. Li, L., Zhao, Y., McCaig, B.C., Wingerd, B.A., Wang, J., Whalon, M.E., Pichersky, E., and, Howe, G.A., (2004) The tomato homolog of CORONATINE-INSENSITIVE1 is required for the maternal control of seed maturation, jasmonate-signaled defense responses, and glandular trichome development. Plant Cell, 16, 126-143.
32. Liechti, R., and, Farmer, E.E., (2006) Jasmonate biochemical pathway. Sci. STKE, 322, 1-3.
33. Pastor, V., Luna, E., Mauch-Mani, B., Ton, J., and, Flors, V., (2012) Primed plants do not forget. Environ. Exp. Bot. 94, 46-56.
34. Penninckx, I.A., Eggermont, K., Terras, F.R., Thomma, B.P., De Samblanx, G.W., Buchala, A., Métraux, J.P., Manners, J.M., and, Broekaert, W.F., (1996) Pathogen-induced systemic activation of a plant defensin gene in Arabidopsis follows a salicylic acid-independent pathway. Plant Cell, 8, 2309-2323.
35. Pieterse, C.M., van Wees, S.C., Hoffland, E., van Pelt, J.A., and, van Loon, L.C., (2010) Systemic resistance in Arabidopsis induced by biocontrol bacteria is independent of salicylic acid accumulation and pathogenesis-related gene expression. Plant Cell, 8, 1225-1237.
36. Pinfield-Wells, H., Rylott, E.L., Gilday, A.D., Graham, S., Job, K., Larson, T.R., and, Graham, I.A., (2005) Sucrose rescues seedling establishment but not germination of Arabidopsis mutants disrupted in peroxisomal fatty acid catabolism. Plant J. 43, 861-872.
37. Prost, I., Dhondt, S., Rothe, G., et al. (2005) Evaluation of the antimicrobial activities of plant oxylipins supports their involvement in defense against pathogens. Plant Physiol. 139, 1902-1913.
38. Reymond, P., Weber, H., Damond, M., and, Farmer, E.E., (2000) Differential gene expression in response to mechanical wounding and insect feeding in Arabidopsis. Plant Cell, 12, 707-720.
39. Rosahl, S., and, Feussner, I., (2005) Oxylipins. In Plant Lipids: Biology, Utilization and Manipulation (, Murphy, D.J., ed.). Oxford and Boca Raton: Blackwell Publishing Ltd./CRC Press, pp. 329-354.
40. Scalschi, L., Vicedo, B., Camañes, G., Fernandez-Crespo, E., Lapeña, L., González-Bosch, C., and, García-Agustín, P., (2013) Hexanoic acid is a resistance inducer that protects tomato plants against Pseudomonas syringae by priming the jasmonic acid and salicylic acid pathways. Mol. Plant Pathol. 14, 342-355.
41. Schenk, P.M., Kazan, K., Wilson, I., Anderson, J.P., Richmond, T., Somerville, S.C., and, Manners, J.M., (2000) Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proc. Natl Acad. Sci. USA, 97, 11655-11660.
42. Schilmiller, A.L., Koo, A.J., and, Howe, G.A., (2007) Functional diversification of acyl-coenzyme A oxidases in jasmonic acid biosynthesis and action. Plant Physiol. 143, 812-824.
43. Shahin, E.A., (1985) Totipotency of tomato protoplasts. Theor. Appl. Genet. 69, 235-240.
44. Stenzel, I., Hause, B., Maucher, H., Pitzschke, A., Miersch, O., Ziegler, J., Ryan, C., and, Wasternack, C., (2003) Allene oxide cyclase dependence of the wound response and vascular bundle specific generation of jasmonates in tomato-amplification in wound-signalling. Plant J. 33, 577-589.
45. Stintzi, A., and, Browse, J., (2000) The Arabidopsis male-sterile mutant, opr3, lacks the 12-oxophytodienoic acid reductase required for jasmonate synthesis. Proc. Natl Acad. Sci. USA, 97, 10625-10630.
46. Stintzi, A., Weber, H., Reymond, P., Browse, J., and, Farmer, E.E., (2001) Plant defense in the absence of jasmonic acid: the role of cyclopentenones. Proc. Natl Acad. Sci. USA, 98, 12837-12842.
47. Taki, N., Sasaki-Sekimoto, Y., Obayashi, T., et al. (2005) 12-oxo-phytodienoic acid triggers expression of a distinct set of genes and plays a role in wound-induced gene expression in Arabidopsis. Plant Physiol. 139, 1268-1283.
48. Thines, B., Katsir, L., Melotto, M., and, Niu, Y., (2007) JAZ repressor proteins are targets of the SCF (COI1) complex during jasmonate signalling. Nature, 448, 661-665.
49. Uppalapati, S.R., Ayoubi, P., Weng, H., Palmer, D.A., Mitchell, R.E., Jones, W., and, Bender, C.L., (2005) The phytotoxin coronatine and methyl jasmonate impact multiple phytohormone pathways in tomato. Plant J. 42, 201-217.
50. Vicedo, B., Flors, V., Leyva, M.D., Finiti, I., Kravchuk, Z., Real, M.D., García-Agustín, P., and, González-Bosch, C., (2009) Hexanoic acid-induced resistance against Botrytis cinerea in tomato plants. Mol. Plant-Microbe Interact. 22, 1455-1465.
51. Vijayan, P., Shockey, J., Levesque, C.A., Cook, R.J., and, Browse, J., (1998) A role for jasmonate in pathogen defense of Arabidopsis. Proc. Natl Acad. Sci. USA, 95, 7209-7214.
52. Wang, L., Halitschke, R., Kang, J.H., Berg, A., Harnisch, F., and, Baldwin, I.T., (2007) Independently silencing two JAR family members impairs levels of trypsin proteinase inhibitors but not nicotine. Planta, 226, 159-167.
53. Wasternack, C., (2007) Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann. Bot. 100, 681-697.
54. Yan, J., Zhang, C., Gu, M., et al. (2009) The Arabidopsis CORONATINE INSENSITIVE1 protein is a jasmonate receptor. Plant Cell, 21, 2220-2236.