Evaluating plant immunity using mass spectrometry-based metabolomics workflows

Frontiers in Plant Science

Volumn 5, Issue JUN, 2014, Pages

  Heuberger, Adam L ^a   Robison, Faith M ^a   Lyons, Sarah Marie A ^a   Broeckling, Corey D ^a   Prenni, Jessica E ^a  

^a Department of Ecosystem Science and Sustainability   (United States)

Author keywords

GC MS; LC MS; Metabolomics; Plant defense; Plant pathogen

Indexed keywords

EID: 84979643007     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00291     Document Type: Review

References (87)

1. Aksenov, A. A., Pasamontes, A., Peirano, D. J., Zhao, W., Dandekar, A. M., Fiehn, O., et al. (2014). Detection of huanglongbing disease using differential mobility spectrometry. Anal. Chem. 86, 2481-2488. doi: 10.1021/ac403469y
2. Aliferis, K. A., and Jabaji, S. (2012). FT-ICR/MS and GC-EI/MS metabolomics networking unravels global potato sprout's responses to rhizoctonia solani Infection. PLoS ONE 7:e42576. doi: 10.1371/journal.pone.0042576
3. Allwood, J. W., Ellis, D. I., Heald, J. K., Goodacre, R., and Mur, L. A. J. (2006). Metabolomic approaches reveal that phosphatidic and phosphatidyl glycerol phospholipids are major discriminatory non-polar metabolites in responses by Brachypodium distachyon to challenge by Magnaporthe grisea. Plant J. 46, 351-368. doi: 10.1111/j.1365-313X.2006.02692.x
4. Barros-Rios, J., Malvar, R. A., Jung, H. J. G., and Santiago, R. (2011). Cell wall composition as a maize defense mechanism against corn borers. Phytochemistry 72, 365-371. doi: 10.1016/j.phytochem.2011.01.004
5. Beets, C. A., Huang, J. C., Madala, N. E., and Dubery, I. (2012). Activation of camalexin biosynthesis in Arabidopsis thaliana in response to perception of bacterial lipopolysaccharides: a gene-to-metabolite study. Planta 236, 261-272. doi: 10.1007/s00425-012-1606-1
6. Berger, S., Sinha, A. K., and Roitsch, T. (2007). Plant physiology meets phytopathology: plant primary metabolism and plant-pathogen interactions. J. Exp. Bot. 58, 4019-4026. doi: 10.1093/jxb/erm298
7. Bollina, V., Kumaraswamy, G. K., Kushalappa, A. C., Choo, T. M., Dion, Y., Rioux, S., et al. (2010). Mass spectrometry-based metabolomics application to identify quantitative resistance-related metabolites in barley against Fusarium head blight. Mol. Plant Pathol. 11, 769-782. doi: 10.1111/j.1364-3703.2010.00643.x
8. Bollina, V., Kushalappa, A. C., Choo, T. M., Dion, Y., and Rioux, S. (2011). Identification of metabolites related to mechanisms of resistance in barley against Fusarium graminearum, based on mass spectrometry. Plant Mol. Biol. 77, 355-370. doi: 10.1007/s11103-011-9815-8
9. Bolton, M. D. (2009). Primary metabolism and plant defense-fuel for the fire. Mol. Plant Microbe Interact. 22, 487-497. doi: 10.1094/MPMI-22-5-0487
10. Botanga, C. J., Bethke, G., Chen, Z., Gallie, D. R., Fiehn, O., and Glazebrook, J. (2012). Metabolite profiling of arabidopsis inoculated with alternaria brassicicola reveals that ascorbate reduces disease severity. Mole. Plant Microbe Interact. 25, 1628-1638. doi: 10.1094/MPMI-07-12-0179-R
11. Bradley, D. J., Kjellbom, P., and Lamb, C. J. (1992). Elicitor-induced and wound-induced oxidative cross-linking of a proline-rich plant-cell wall protein-a novel, rapid defense response. Cell 70, 21-30. doi: 10.1016/0092-8674(92)90530-P
12. Broadhurst, D. I., and Kell, D. B. (2006). Statistical strategies for avoiding false discoveries in metabolomics and related experiments. Metabolomics 2, 171-196. doi: 10.1007/s11306-006-0037-z
13. Broeckling, C. D., Heuberger, A. L., Prince, J. A., Ingelsson, E., and Prenni, J. E. (2012). Assigning precursor-product ion relationships in indiscriminant MS/MS data from non-targeted metabolite profiling studies. Metabolomics 9, 33-43. doi: 10.1007/s11306-012-0426-4
14. Cao, A., Reid, L. M., Butron, A., Malvar, R. A., Souto, X. C., and Santiago, R. (2011). Role of Hydroxycinnamic acids in the infection of maize silks by fusarium graminearum schwabe. Mol. Plant Microbe Interact. 24, 1020-1026. doi: 10.1094/MPMI-03-11-0079
15. Cevallos-Cevallos, J. M., Futch, D. B., Shilts, T., Folimonova, S. Y., and Reyes-De-Corcuera, J. I. (2012). GC-MS metabolomic differentiation of selected citrus varieties with different sensitivity to citrus huanglongbing. Plant Physiol. Biochem. 53, 69-76. doi: 10.1016/j.plaphy.2012.01.010
16. Chanda, B., Xia, Y., Mandal, M. K., Yu, K. S., Sekine, K. T., Gao, Q. M., et al. (2011). Glycerol-3-phosphate is a critical mobile inducer of systemic immunity in plants. Nat. Genet. 43, 421. doi: 10.1038/ng.798
17. Cho, K., Kim, Y., Wi, S. J., Seo, J. B., Kwon, J., Chung, J. H., et al. (2013). Metabolic survey of defense responses to a compatible hemibiotroph, Phytophthora parasitica var. nicotianae, in ethylene signaling-impaired tobacco. J. Agric. Food Chem. 61, 8477-8489. doi: 10.1021/jf401785w
18. De Livera, A. M., Dias, D. A., De Souza, D., Rupasinghe, T., Pyke, J., Tull, D., et al. (2012). Normalizing and integrating metabolomics data. Anal. Chem. 84, 10768-10776. doi: 10.1021/ac302748b
19. Delledonne, M., Xia, Y. J., Dixon, R. A., and Lamb, C. (1998). Nitric oxide functions as a signal in plant disease resistance. Nature 394, 585-588. doi: 10.1038/29087
20. Dittrich, P., and Raschke, K. (1977). Malate metabolism in isolated epidermis of commelina-communis l in relation to stomatal functioning. Planta 134, 77-81. doi: 10.1007/BF00390098
21. Dixon, R. A. (2001). Natural products and plant disease resistance. Nature 411, 843-847. doi: 10.1038/35081178
22. Ecker, J. R., and Davis, R. W. (1987). Plant defense genes are regulated by ethylene. Proc. Natl. Acad. Sci. U.S.A. 84, 5202-5206. doi: 10.1073/pnas.84.15.5202
23. Fiehn, O., Kloska, S., and Altmann, T. (2001). Integrated studies on plant biology using multiparallel techniques. Curr. Opin. Biotechnol. 12, 82-86. doi: 10.1016/S0958-1669(00)00165-8
24. Fiehn, O., Kopka, J., Dormann, P., Altmann, T., Trethewey, R. N., and Willmitzer, L. (2000a). Metabolite profiling for plant functional genomics. Nat. Biotechnol. 18, 1157-1161. doi: 10.1038/81137
25. Fiehn, O., Kopka, J., Trethewey, R. N., and Willmitzer, L. (2000b). Identification of uncommon plant metabolites based on calculation of elemental compositions using gas chromatography and quadrupole mass spectrometry. Anal. Chem. 72, 3573-3580. doi: 10.1021/ac991142i
26. Foyer, C. H., and Noctor, G. (2005). Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17, 1866-1875. doi: 10.1105/tpc.105.033589
27. Gamir, J., Pastor, V., Cerezo, M., and Flors, V. (2012). Identification of indole-3-carboxylic acid as mediator of priming against Plectosphaerella cucumerina. Plant Physiol. Biochem. 61, 169-179. doi: 10.1016/j.plaphy.2012.10.004
28. Ge, H., Walhout, A. J. M., and Vidal, M. (2003). Integrating “omic” information: a bridge between genomics and systems biology. Trends Genet. 19, 551-560. doi: 10.1016/j.tig.2003.08.009
29. Gershenzon, J., and Dudareva, N. (2007). The function of terpene natural products in the natural world. Nat. Chem. Biol. 3, 408-414. doi: 10.1038/nchembio.2007.5
30. Gundlach, H., Muller, M. J., Kutchan, T. M., and Zenk, M. H. (1992). Jasmonic acid is a signal transducer in elicitor-induced plant-cell cultures. Proc. Natl. Acad. Sci. U.S.A. 89, 2389-2393. doi: 10.1073/pnas.89.6.2389
31. Gunnaiah, R., Kushalappa, A. C., Duggavathi, R., Fox, S., and Somers, D. J. (2012). Integrated metabolo-proteomic approach to decipher the mechanisms by which wheat qtl (fhb1) contributes to resistance against fusarium graminearum. PLoS ONE 7:e40695. doi: 10.1371/journal.pone.0040695
32. Hantao, L. W., Aleme, H. G., Passador, M. M., Furtado, E. L., Ribeiro, F. A. D., Poppi, R. J., (2013). Determination of disease biomarkers in Eucalyptus by comprehensive two-dimensional gas chromatography and multivariate data analysis. J. Chromatogr. A 1279, 86-91. doi: 10.1016/j.chroma.2013.01.013
33. Horai, H., Arita, M., Kanaya, S., Nihei, Y., Ikeda, T., Suwa, K., et al. (2010). MassBank: a public repository for sharing mass spectral data for life sciences. J. Mass Spectrom. 45, 703-714. doi: 10.1002/jms.1777
34. Jung, H. W., Tschaplinski, T. J., Wang, L., Glazebrook, J., and Greenberg, J. T. (2009). Priming in systemic plant immunity. Science 324, 89-91. doi: 10.1126/science.1170025
35. Keerthi, D., Geethu, C., Nair, R. A., and Pillai, P. (2014). Metabolic profiling of Zingiber zerumbet following pythium myriotylum infection: investigations on the defensive role of the principal secondary metabolite, zerumbone. Appl. Biochem. Biotechnol. 172, 2593-2603. doi: 10.1007/s12010-013-0707-z
36. Kishi-Kaboshi, M., Okada, K., Kurimoto, L., Murakami, S., Umezawa, T., Shibuya, N., et al. (2010). A rice fungal MAMP-responsive MAPK cascade regulates metabolic flow to antimicrobial metabolite synthesis. Plant J. 63, 599-612. doi: 10.1111/j.1365-313X.2010.04264.x
37. Kopka, J., Fernie, A., Weckwerth, W., Gibon, Y., and Stitt, M. (2004). Metabolite profiling in plant biology: platforms and destinations. Genome Biol. 5:109. doi: 10.1186/gb-2004-5-6-109
38. Kopka, J., Schauer, N., Krueger, S., Birkemeyer, C., Usadel, B., Bergmuller, E., et al. (2005). The golm metabolome database. Bioinformatics 21, 1635-1638. doi: 10.1093/bioinformatics/bti236
39. Kuhl, C., Tautenhahn, R., Bottcher, C., Larson, T. R., and Neumann, S. (2012). CAMERA: an integrated strategy for compound spectra extraction and annotation of liquid chromatography/mass spectrometry data sets. Anal. Chem. 84, 283-289. doi: 10.1021/ac202450g
40. Lamb, C., and Dixon, R. A. (1997). The oxidative burst in plant disease resistance. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48, 251-275. doi: 10.1146/annurev.arplant.48.1.251
41. Lee, S., Yang, D. S., Uppalapati, S. R., Sumner, L. W., and Mysore, K. S. (2013). Suppression of plant defense responses by extracellular metabolites from Pseudomonas syringae pv. tabaci in Nicotiana benthamiana. BMC Plant Biol. 3:65. doi: 10.1186/1471-2229-13-65
42. Lisec, J., Schauer, N., Kopka, J., Willmitzer, L., and Fernie, A. R. (2006). Gas chromatography mass spectrometry-based metabolite profiling in plants. Nat. Protoc. 1, 387-396. doi: 10.1038/nprot.2006.59
43. Liu, G. S., Ji, Y. Y., Bhuiyan, N. H., Pilot, G., Selvaraj, G., Zou, J. T., et al. (2010). Amino acid homeostasis modulates salicylic acid-associated redox status and defense responses in arabidopsis. Plant Cell 22, 3845-3863. doi: 10.1105/tpc.110.079392
44. Lommen, A. (2009). MetAlign: interface-driven, versatile metabolomics tool for hyphenated full-scan mass spectrometry data preprocessing. Anal. Chem. 81, 3079-3086. doi: 10.1021/ac900036d
45. Lorenzo, O., Piqueras, R., Sanchez-Serrano, J. J., and Solano, R. (2003). ETHYLENE RESPONSE FACTOR1 integrates signals from ethylene and jasmonate pathways in plant defense. Plant Cell 15, 165-178. doi: 10.1105/tpc.007468
46. Madala, N. E., Steenkamp, P. A., Piater, L. A., and Dubery, I. A. (2013). Metabolomic analysis of isonitrosoacetophenone-induced perturbations in phenolic metabolism of Nicotiana tabacum cells. Phytochemistry 94, 82-90. doi: 10.1016/j.phytochem.2013.05.010
47. Malacarne, G., Vrhovsek, U., Zulini, L., Cestaro, A., Stefanini, M., Mattivi, F., et al. (2011). Resistance to Plasmopara viticola in a grapevine segregating population is associated with stilbenoid accumulation and with specific host transcriptional responses. BMC Plant Biol. 11:114. doi: 10.1186/1471-2229-11-114
48. Maleck, K., Levine, A., Eulgem, T., Morgan, A., Schmid, J., Lawton, K. A., et al. (2000). The transcriptome of Arabidopsis thaliana during systemic acquired resistance. Nat. Genet. 26, 403-410. doi: 10.1038/82521
49. Matros, A., Amme, S., Kettig, B., Buck-Sorlin, G. H., Sonnewald, U., and Mock, H. P. (2006). Growth at elevated CO2 concentrations leads to modified profiles of secondary metabolites in tobacco cv. SamsunNN and to increased resistance against infection with potato virus Y. Plant Cell Environ. 29, 126-137. doi: 10.1111/j.1365-3040.2005.01406.x
50. Mishina, T. E., and Zeier, J. (2007). Pathogen-associated molecular pattern recognition rather than development of tissue necrosis contributes to bacterial induction of systemic acquired resistance in Arabidopsis. Plant J. 50, 500-513. doi: 10.1111/j.1365-313X.2007.03067.x
51. Ng, C. K. Y., Carr, K., Mcainsh, M. R., Powell, B., and Hetherington, A. M. (2001). Drought-induced guard cell signal transduction involves sphingosine-1-phosphate. Nature 410, 596-599. doi: 10.1038/35069092
52. O'brien, J. A., Daudi, A., Finch, P., Butt, V. S., Whitelegge, J. P., Souda, P., et al. (2012). A peroxidase-dependent apoplastic oxidative burst in cultured arabidopsis cells functions in MAMP-elicited defense. Plant Physiol. 158, 2013-2027. doi: 10.1104/pp.111.190140
53. Pare, P. W., and Tumlinson, J. H. (1999). Plant volatiles as a defense against insect herbivores. Plant Physiol. 121, 325-331. doi: 10.1104/pp.121.2.325
54. Park, S. W., Kaimoyo, E., Kumar, D., Mosher, S., and Klessig, D. F. (2007). Methyl salicylate is a critical mobile signal for plant systemic acquired resistance. Science 318, 113-116. doi: 10.1126/science.1147113
55. Peluffo, L., Lia, V., Troglia, C., Maringolo, C., Norma, P., Escande, A., et al. (2010). Metabolic profiles of sunflower genotypes with contrasting response to Sclerotinia sclerotiorum infection. Phytochemistry 71, 70-80. doi: 10.1016/j.phytochem.2009.09.018
56. Rajjou, L., Belghazi, M., Huguet, R., Robin, C., Moreau, A., Job, C., et al. (2006). Proteomic investigation of the effect of salicylic acid on Arabidopsis seed germination and establishment of early defense mechanisms. Plant Physiol. 141, 910-923. doi: 10.1104/pp.106.082057
57. Rojas, C. M., Senthil-Kumar, M., Tzin, V., and Mysore, K. (2014). Regulation of primary plant metabolism during plant-pathogen interactions and its contribution to plant defense. Front. Plant Sci. 5:17. doi: 10.3389/fpls.2014.00017
58. Ronicke, S., Hahn, V., Vogler, A., and Friedt, W. (2005). Quantitative trait loci analysis of resistance to Sclerotinia sclerotiorum in sunflower. Phytopathology 95, 834-839. doi: 10.1094/PHYTO-95-0834
59. Roos, W., Viehweger, K., Dordschbal, B., Schumann, B., Evers, S., Steighardt, J., et al. (2006). Intracellular pH signals in the induction of secondary pathways-The case of Eschscholzia californica. J. Plant Physiol. 163, 369-381. doi: 10.1016/j.jplph.2005.11.012
60. Saglam, A., Terzi, R., Nar, H., Saruhan, N., Ayaz, F. A., and Kadioglu, A. (2010). Inorganic and organic solutes in apoplastic and symplastic spaces contribute to osmotic adjustment during leaf rolling in ctenanthe setosa. Acta Biol. Cracov. Ser. Bot. 52, 37-44. doi: 10.2478/v10182-010-0005-9
61. Sakano, K. (2001). Metabolic regulation of pH in plant cells: role of cytoplasmic on in defense reaction and secondary metabolism. Int. Rev. Cytol. 206, 1-44. doi: 10.1016/S0074-7696(01)06018-1
62. Saubeau, G., Goulitquer, S., Barloy, D., Potin, P., Andrivon, D., and Val, F. (2013). Differential induction of oxylipin pathway in potato and tobacco cells by bacterial and oomycete elicitors. Plant Cell Rep. 32, 579-589. doi: 10.1007/s00299-012-1377-y
63. Scharte, J., Schon, H., and Weis, E. (2005). Photosynthesis and carbohydrate metabolism in tobacco leaves during an incompatible interaction with Phytophthora nicotianae. Plant Cell Environ. 28, 1421-1435. doi: 10.1111/j.1365-3040.2005.01380.x
64. Schlupmann, H., Bacic, A., and Read, S. M. (1993). A novel callose synthase from pollen tubes of nicotiana. Planta 191, 470-481. doi: 10.1007/BF00195748
65. Schweer, H. (1982). Gas chromatography-mass spectrometry of aldoses as o-methoxime, O-2-Methyl-2-Propoxime and O-normal-butoxime pertrifluoroacetyl derivatives on Ov-225 with methylpropane as ionization agent.2. hexoses. J. Chromatogr. 236, 361-367. doi: 10.1016/S0021-9673(00)84886-4
66. Smith, C. A., O'maille, G., Want, E. J., Qin, C., Trauger, S. A., Brandon, T. R., et al. (2005). METLIN-A metabolite mass spectral database. Ther. Drug Monit. 27, 747-751. doi: 10.1097/01.ftd.0000179845.53213.39
67. Smith, C. A., Want, E. J., O'maille, G., Abagyan, R., and Siuzdak, G. (2006). XCMS: processing mass spectrometry data for metabolite profiling using nonlinear peak alignment, matching, and identification. Anal. Chem. 78, 779-787. doi: 10.1021/ac051437y
68. Staswick, P. E., and Tiryaki, I. (2004). The oxylipin signal jasmonic acid is activated by an enzyme that conjugates it to isoleucine in Arabidopsis. Plant Cell 16, 2117-2127. doi: 10.1105/tpc.104.023549
69. Stein, S. E. (1999). An integrated method for spectrum extraction and compound identification from gas chromatography/mass spectrometry data. J. Am. Soc. Mass Spectrom. 10, 770-781. doi: 10.1016/S1044-0305(99)00047-1
70. Sumner, L., Amberg, A., Barrett, D., Beale, M., Beger, R., Daykin, C., et al. (2007). Proposed minimum reporting standards for chemical analysis. Metabolomics 3, 211-221. doi: 10.1007/s11306-007-0082-2
71. Sysi-Aho, M., Katajamaa, M., Yetukuri, L., and Oresic, M. (2007). Normalization method for metabolomics data using optimal selection of multiple internal standards. BMC Bioinformatics 8:93. doi: 10.1186/1471-2105-8-93
72. Tautenhahn, R., Bottcher, C., and Neumann, S. (2007). Annotation of LC/ESI-MS mass signals. Bioinformatics Res. Dev. Proc. 4414, 371-380. doi: 10.1007/978-3-540-71233-6_29
73. Tavernier, V., Cadiou, S., Pageau, K., Lauge, R., Reisdorf-Cren, M., Langin, T., et al. (2007). The plant nitrogen mobilization promoted by Colletotrichum lindemuthianum in Phaseolus leaves depends on fungus pathogenicity. J. Exp. Bot. 58, 3351-3360. doi: 10.1093/jxb/erm182
74. Torres, M. A., Jones, J. D. G., and Dangl, J. L. (2006). Reactive oxygen species signaling in response to pathogens. Plant Physiol. 141, 373-378. doi: 10.1104/pp.106.079467
75. Truman, W. M., Bennett, M. H., Turnbull, C. G. N., and Grant, M. R. (2010). Arabidopsis auxin mutants are compromised in systemic acquired resistance and exhibit aberrant accumulation of various indolic compounds. Plant Physiol. 152, 1562-1573. doi: 10.1104/pp.109.152173
76. Tugizimana, F., Steenkamp, P. A., Piater, L. A., and Dubery, I. A. (2014). Multi-platform metabolomic analyses of ergosterol-induced dynamic changes in Nicotiana tabacum cells. PLoS ONE 9:e87846. doi: 10.1371/journal.pone.0087846
77. Veselkov, K. A., Vingara, L. K., Masson, P., Robinette, S. L., Want, E., Li, J. V., et al. (2011). Optimized preprocessing of ultra-performance liquid chromatography/mass spectrometry urinary metabolic profiles for improved information recovery. Anal. Chem. 83, 5864-5872. doi: 10.1021/ac201065j
78. Vicente, M. R. S., Larios-Zarate, G., and Plasencia, J. (2013). Disruption of sphingolipid biosynthesis in Nicotiana benthamiana activates salicylic acid-dependent responses and compromises resistance to Alternaria alternata f. sp lycopersici. Planta 237, 121-136. doi: 10.1007/s00425-012-1758-z
79. Wang, J. W., and Wu, J. Y. (2005). Nitric oxide is involved in methyl jasmonate-induced defense responses and secondary metabolism activities of Taxus cells. Plant Cell Physiol. 46, 923-930. doi: 10.1093/pcp/pci098
80. Weinberger, F., Lion, U., Delage, L., Kloareg, B., Potin, P., Beltran, J., et al. (2011). Up-regulation of lipoxygenase, phospholipase, and oxylipin-production in the induced chemical defense of the red alga Gracilaria chilensis against epiphytes. J. Chem. Ecol. 37, 677-686. doi: 10.1007/s10886-011-9981-9
81. Wishart, D. S. (2011). Advances in metabolite identification. Bioanalysis 3, 1769-1782. doi: 10.4155/bio.11.155
82. Wojakowska, A., Muth, D., Narozna, D., Madrzak, C., Stobiecki, M., and Kachlicki, P. (2013). Changes of phenolic secondary metabolite profiles in the reaction of narrow leaf lupin (Lupinus angustifolius) plants to infections with Colletotrichum lupini fungus or treatment with its toxin. Metabolomics 9, 575-589. doi: 10.1007/s11306-012-0475-8
83. Wolf, S., Schmidt, S., Muller-Hannemann, M., and Neumann, S. (2010). In silico fragmentation for computer assisted identification of metabolite mass spectra. BMC Bioinformatics 11:148. doi: 10.1186/1471-2105-11-148
84. Xia, J. G., Psychogios, N., Young, N., and Wishart, D. S. (2009). MetaboAnalyst: a web server for metabolomic data analysis and interpretation. Nucleic Acids Res. 37, W652-W660. doi: 10.1093/nar/gkp356
85. Yang, Z. N., Rogers, L. M., Song, Y. D., Guo, W. J., and Kolattukudy, P. E. (2005). Homoserine and asparagine are host signals that trigger in planta expression of a pathogenesis gene in Nectria haematococca. Proc. Natl. Acad. Sci. U.S.A. 102, 4197-4202. doi: 10.1073/pnas.0500312102
86. Yun, Z., Gao, H. J., Liu, P., Liu, S. Z., Luo, T., Jin, S., et al. (2013). Comparative proteomic and metabolomic profiling of citrus fruit with enhancement of disease resistance by postharvest heat treatment. BMC Plant Biol. 13:44. doi: 10.1186/1471-2229-13-44
87. Zhao, N., Guan, J., Ferrer, J. L., Engle, N., Chern, M., Ronald, P., et al. (2010). Biosynthesis and emission of insect-induced methyl salicylate and methyl benzoate from rice. Plant Physiol. Biochem. 48, 279-287. doi: 10.1016/j.plaphy.2010.01.023