Abstract
TomloxD is a lipoxygenase from Lycopersicon esculentum Mill, which has lipoxygenase activity. The expression of TomloxD can be stimulated by wounding, pathogen infection, jasmonate, and systemin. To investigate the function of TomloxD, transgenic tomato plants silencing tomloxD gene was produced. The suppression of TomloxD expression led to a marked reduction in the levels of lipoxygenase activity and endogenous jasmonic acid content, which suggested TomloxD can catalyze α-linolenic acids to produce (13S)-hydroperoxyoctadecatrienoic acid (13-HPOT), and the 13-HPOT is metabolized further to synthesize jasmonic acid. Real-time RT-PCR revealed that the expression of defense genes LeHSP90, LePR1 and LePR6 was also less in the transformants than in the wild-type tomato plant. Resistance assay showed that the suppression of TomloxD in transgenic tomato plants reduced thermotolerance of tomato and increased its susceptibility to Cladosporium fulvum. Collectively, the data presented here suggest that the TomloxD plays a role as a component of the octadecanoid defense-signaling pathway and involved in the generation of endogenous jasmonic acid, and in turn regulates the expression of plant defense genes and resistance to high temperature and pathogen attack.
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References
Acosta IF, Laparra H, Romero SP, Schmelz E, Hamberg M, Mottinger JP, Moreno MA, Dellaporta SL (2009) Tasselseed1 is a lipoxygenase affecting jasmonic acid signaling in sex determination of maize. Science 323:262–265
Baldwin IT, Zhang ZP, Diab N, Ohnmeiss TE, McCloud ES, Lynds GY, Schmelz EA (1997) Quantification, correlations and manipulations of wound-induced changes in jasmonic acid and nicotine in Nicotiana sylvestris. Planta 201:397–404
Balint-Kurti RJ, Dixon MS, Jones DA, Norcott KA, Jones JDG (1994) RFLP linkage analysis of the Cf-4 and Cf-9 genes for resistance to Cladosporium fulvum in tomato. Theor Appl Genet 88:691–700
Bell E, Creelman RA, Mullet JE (1995) A chloroplast lipoxygenase is required for wound-induced jasmonic acid accumulation in Arabidopsis. Proc Natl Acad Sci USA 92:8675–8679
Boué SM, Shih BY, Carter-Wientjes CH, Cleveland TE (2005) Effect of soybean lipoxygenase on volatile generation and inhibition of Aspergillus flavus mycelial growth. J Agric Food Chem 53:4778–4783
Brash AR (1999) Lipoxygenases: occurrence, functions, catalysis, and acquisition of substrate. J Biol Chem 274:23679–23682
Browse J (2009) The power of mutants for investigating jasmonate biosynthesis and signaling. Phytochemistry 70:1539–1546
Chen G, Hackett R, Walker D, Taylor A, Lin Z, Grierson D (2004) Identification of a specific isoform of tomato lipoxygenase (TomloxC) involved in the generation of fatty acid-derived flavor compounds. Plant Physiol 136:2641–2651
Csermely P, Schnaider T, Soti C, Prohászka Z, Nardai G (1998) The 90-kDa molecular chaperone family: structure, function, and clinical applications. A comprehensive review. Pharmacol Ther 79:129–168
Feussner I, Wasternack C (2002) Lipoxygenase pathway. Annu Rev Plant Biol 53:275–297
Gao X, Brodhagen M, Isakeit T, Brown SH, Göbel C, Betran J, Feussner I, Keller NP, Kolomiets MV (2009) Inactivation of the lipoxygenase ZmLOX3 increases susceptibility of maize to Aspergillus spp. Mol Plant Microbe Interact 22:222–231
Gfeller A, Dubugnon L, Liechti R, Farmer EE (2010) Jasmonate biochemical pathway. Sci Signal 3:cm3
Griffiths A, Prestage S, Linforth R, Zhang J, Taylor A, Grierson D (1999) Fruit-specific lipoxygenase suppression in antisense-transgenic tomatoes. Postharvest Biol Technol 17:163–173
Hayashi S, Gresshoff PM, Kinkema M (2008) Molecular analysis of lipoxygenases associated with nodule development in soybean. Mol Plant Microbe Interact 21:843–853
He S, Tan L, Hu Z, Chen G, Wang G, Hu T (2012) Molecular characterization and functional analysis by heterologous expression in E. coli under diverse abiotic stresses for OsLEA5, the atypical hydrophobic LEA protein from Oryza sativa L. Mol Genet Genomics 287:39–54
Heitz T, Bergey DR, Ryan CA (1997) A gene encoding a chloroplast-targeted lipoxygenase in tomato leaves is transiently induced by wounding, systemin, and methyl jasmonate. Plant Physiol 114:1085–1093
Höfgen R, Willmitzer L (1988) Storage of competent cells for Agrobacterium transformation. Nucleic Acids Res 16:9877
Howe GA, Jander G (2008) Plant immunity to insect herbivores. Annu Rev Plant Biol 59:41–66
Howe GA, Schilmiller AL (2002) Oxylipin metabolism in response to stress. Curr Opin Plant Biol 5:230–236
Hu T, Qv X, Hu Z, Chen G, Chen Z (2011) Expression, molecular characterization and detection of lipoxygenase activity of tomloxD from tomato. Afr J Biotechnol 10:490–498
Hu T, Zeng H, Hu Z, Qv X, Chen G (2013) Overexpression of the tomato 13-lipoxygenase gene TomloxD increases generation of endogenous jasmonic acid and resistance to Cladosporium fulvum and high temperature. Plant Mol Biol Rep 31:1141–1149
Jardim BC, Perdïzio VA, Berbert-Molina MA, Rodrigues DC, Botelho-Júnior S, Vicente AC, Hansen E, Otsuki K, Urmënyi TP, Jacinto T (2010) Herbivore response in passion fruit (Passiflora edulis Sims) plants: induction of lipoxygenase activity in leaf tissue in response to generalist and specialist insect attack. Protein Pept Lett 17:480–484
Kolomiets MV, Hannapel DJ, Chen H, Tymeson M, Gladon RJ (2001) Lipoxygenase is involved in the control of potato tuber development. Plant Cell 13:613–626
Lawrence CB, Joosten MHAJ, Tuzun S (1996) Differential induction of pathogenesis-related proteins in tomato by Alternaria solani and the association of a basic chitinase isozyme with resistance. Physiol Mol Plant Pathol 48:361–377
Liavonchanka A, Feussner I (2006) Lipoxygenases: occurrence, functions and catalysis. J Plant Physiol 163:348–357
Liu S, Han B (2010) Differential expression pattern of an acidic 9/13-lipoxygenase in flower opening and senescence and in leaf response to phloem feeders in the tea plant. BMC Plant Biol 10:228–242
Løvdal T, Lillo C (2009) Reference gene selection for quantitative real-time PCR normalization in tomato subjected to nitrogen, cold, and light stress. Anal Biochem 387:238–242
Mariutto M, Duby F, Adam A, Bureau C, Fauconnier ML, Ongena M, Thonart P, Dommes J (2011) The elicitation of a systemic resistance by Pseudomonas putida BTP1 in tomato involves the stimulation of two lipoxygenase isoforms. BMC Plant Biol 11:29–43
Park YS, Kunze S, Ni X, Feussner I, Kolomiets MV (2010) Comparative molecular and biochemical characterization of segmentally duplicated 9-lipoxygenase genes ZmLOX4 and ZmLOX5 of maize. Planta 231:1425–1437
Prost I, Dhondt S, Rothe G, Vicente J, Rodriguez MJ, Kift N, Carbone F, Griffiths G, Esquerré-Tugayé MT, Rosahl S, Castresana C, Hamberg M, Fournier J (2005) Evaluation of the antimicrobial activities of plant oxylipins supports their involvement in defense against pathogens. Plant Physiol 139:1902–1913
Royo J, León J, Vancanneyt G, Albar JP, Rosahl S, Ortego F, Castañera P, Sánchez-Serrano JJ (1999) Antisense-mediated depletion of a potato lipoxygenase reduces wound induction of proteinase inhibitors and increases weight gain of insect pests. Proc Natl Acad Sci USA 96:146–1151
Rudolph M, Schlereth A, Körner M, Feussner K, Berndt E, Melzer M, Hornung E, Feussner I (2011) The lipoxygenase-dependent oxygenation of lipid body membranes is promoted by a patatin-type phospholipase in cucumber cotyledons. J Exp Bot 62:749–760
Shen J, Tieman D, Jones JB, Taylor MG, Schmelz E, Huffaker A, Bies D, Chen K, Klee HJ (2014) A 13-lipoxygenase, TomloxC, is essential for synthesis of C5 flavour volatiles in tomato. J Exp Bot 65:419–428
Tornero P, Gadea J, Conejero V, Vera P (1997) Two PR-1 genes from tomato are differentially regulated and reveal a novel mode of expression for a pathogenesis related genes during the hypersensitive response and development. Mol Plant Microbe Interact 10:624–634
Veronico P, Giannino D, Melillo MT, Leone A, Reyes A, Kennedy MW, Bleve-Zacheo T (2006) A novel lipoxygenase in pea roots. Its function in wounding and biotic stress. Plant Physiol 141:1045–1055
Vicente J, Cascón T, Vicedo B, García-Agustín P, Hamberg M, Castresana C (2012) Role of 9-lipoxygenase and α-dioxygenase oxylipin pathways as modulators of local and systemic defense. Mol Plant 5:914–928
Wang R, Shen W, Liu L, Jiang L, Liu Y, Su N, Wan J (2008) A novel lipoxygenase gene from developing rice seeds confers dual position specificity and responds to wounding and insect attack. Plant Mol Biol 66:401–414
Wasternack C, Kombrink E (2010) Jasmonates: structural requirements for lipid-derived signals active in plant stress responses and development. ACS Chem Biol 15:63–77
Wren JJ, Wiggall PH (1965) An improved colorimetric method for the determination of proline in the presence of other ninhydrin-positive compounds. Biochem J 94:216–220
Xue Y, Peng R, Xiong A, Li X, Zha D, Yao Q (2009) Yeast heat-shock protein gene HSP26 enhances freezing tolerance in Arabidopsis. J Plant Physiol 166:844–850
Yan L, Zhai Q, Wei J, Li S, Wang B, Huang T, Du M, Sun J, Kang L, Li CB, Li C (2013) Role of tomato lipoxygenase D in wound-induced jasmonate biosynthesis and plant immunity to insect herbivores. PLoS Genet 9:e1003964. doi:10.1371/journal.pgen.1003964
Yemm EW, Willis AJ (1954) The estimation of carbohydrates in plant extracts by anthrone. Biochem J 57:508–514
Zhang L, Xiao S, Li W, Feng W, Li J, Wu Z, Gao X, Liu F, Shao M (2011) Overexpression of a Harpin-encoding gene hrf1 in rice enhances drought tolerance. J Exp Bot 62:4229–4238
Zhou G, Qi J, Ren N, Cheng J, Erb M, Mao B, Lou Y (2009) Silencing OsHI-LOX makes rice more susceptible to chewing herbivores, but enhances resistance to a phloem feeder. Plant J 60:638–648
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This work was supported by National Natural Science Foundation of China (nos. 31000911 and 31171968), “Chun Hui Project” Foundation of Education Ministry of China (no. Z2008-1-63004).
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Hu, T., Hu, Z., Zeng, H. et al. Tomato lipoxygenase D involved in the biosynthesis of jasmonic acid and tolerance to abiotic and biotic stress in tomato. Plant Biotechnol Rep 9, 37–45 (2015). https://doi.org/10.1007/s11816-015-0341-z
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DOI: https://doi.org/10.1007/s11816-015-0341-z