Isolation and characterization of isochorismate synthase and cinnamate 4-hydroxylase during salinity stress, wounding, and salicylic acid treatment in Carthamus tinctorius

Plant Signaling and Behavior

Volumn 8, Issue 11, 2013, Pages

  Sadeghi, Mahnaz ^a   Dehghan, Sara ^a   Fischer, Rainer ^b   Wenzel, Uwe ^c   Vilcinskas, Andreas ^b,c   Kavousi, Hamid Reza ^a   Rahnamaeian, Mohammad ^b,c  

^a SHAHID BAHONAR UNIVERSITY OF KERMAN   (Iran)

^b FRAUNHOFER INSTITUTE FOR MOLECULAR BIOLOGY AND APPLIED ECOLOGY IME   (Germany)

^c JUSTUS LIEBIG UNIVERSITY   (Germany)

Author keywords

Cinnamate 4 hydroxylase; Isochorismate synthase; Safflower; Salicylic acid; Salinity; Wounding

Indexed keywords

EID: 84890935705     PISSN: 15592316     EISSN: 15592324     Source Type: Journal    
DOI: 10.4161/psb.27335     Document Type: Article

References (64)

1. Martinez N, Sosa M, Higa R, Fornes D, Capobianco E, Jawerbaum A. Dietary treatments enriched in olive and safflower oils regulate seric and placental matrix metalloproteinases in maternal diabetes. Placenta 2012; 33:8-16; PMID:22098918; http://dx.doi. org/10.1016/j.placenta.2011.10.015
2. Hiramatsu M, Takahashi T, Komatsu M, Kido T, Kasahara Y. Antioxidant and neuroprotective activities of Mogami-benibana (safflower, Carthamus tinctorius Linne). Neurochem Res 2009; 34:795-805; PMID:19082884; http://dx.doi.org/10.1007/ s11064-008-9884-5
3. Rahnamaeian M, Vilcinskas A. Defense gene expression is potentiated in transgenic barley expressing antifungal peptide Metchnikowin throughout powdery mildew challenge. J Plant Res 2012; 125:115-24; PMID:21516363; http://dx.doi.org/10.1007/ s10265-011-0420-3
4. Herrmann KM. The shikimate pathway as an entry to aromatic secondary metabolism. Plant Physiol 1995; 107:7-12; PMID:7870841; http://dx.doi.org/10.1104/ pp.107.1.7
5. Maffei ME, Gertsch J, Appendino G. Plant volatiles: production, function and pharmacology. Nat Prod Rep 2011; 28:1359-80; PMID:21670801; http://dx.doi. org/10.1039/c1np00021g
6. Chen Z, Zheng Z, Huang J, Lai Z, Fan B. Biosynthesis of salicylic acid in plants. Plant Signal Behav 2009; 4:493-6; PMID:19816125; http://dx.doi.org/10.4161/ psb.4.6.8392
7. van Tegelen LJP, Moreno PRH, Croes AF, Verpoorte R, Wullems GJ. Purification and cDNA cloning of isochorismate synthase from elicited cell cultures of Catharanthus roseus. Plant Physiol 1999; 119:705-12; PMID:9952467; http://dx.doi.org/10.1104/ pp.119.2.705
8. León J, Shulaev V, Yalpani N, Lawton MA, Raskin I. Benzoic acid 2-hydroxylase, a soluble oxygenase from tobacco, catalyzes salicylic acid biosynthesis. Proc Natl Acad Sci U S A 1995; 92:10413-7; PMID:7479795; http://dx.doi.org/10.1073/pnas.92.22.10413
9. Yu ZZ, Fu CX, Han YS, Li YX, Zhao DX. Salicylic acid enhances Jaceosidin and Syringin production in cell cultures of Saussurea medusa. Biotechnol Lett 2006; 28:1027-31; PMID:16786264; http://dx.doi. org/10.1007/s10529-006-9035-5
10. Havsteen BH. The biochemistry and medical significance of the flavonoids. Pharmacol Ther 2002; 96:67-202; PMID:12453566; http://dx.doi. org/10.1016/S0163-7258(02)00298-X
11. Pourcel L, Irani NG, Koo AJ, Bohorquez-Restrepo A, Howe GA, Grotewold E. A chemical complementation approach reveals genes and interactions of flavonoids with other pathways. Plant J 2013; 74:383-97; PMID:23360095; http://dx.doi.org/10.1111/ tpj.12129
12. Sanchez-Ballesta MT, Romero I, Jiménez JB, Orea JM, González-Ureña Á, Escribano MI, Merodio C. Involvement of the phenylpropanoid pathway in the response of table grapes to low temperature and high CO2 levels. Postharvest Biol Technol 2007; 46:29-35; http://dx.doi.org/10.1016/j.postharvbio.2007.04.001
13. Schoch GA, Nikov GN, Alworth WL, Werck-Reichhart D. Chemical inactivation of the cinnamate 4-hydroxylase allows for the accumulation of salicylic acid in elicited cells. Plant Physiol 2002; 130:1022-31; PMID:12376665; http://dx.doi.org/10.1104/ pp.004309
14. Morkunas I, Narożna D, Nowak W, Samardakiewicz S, Remlein-Starosta D. Cross-talk interactions of sucrose and Fusarium oxysporum in the phenylpropanoid pathway and the accumulation and localization of flavonoids in embryo axes of yellow lupine. J Plant Physiol 2011; 168:424-33; PMID:21056513; http:// dx.doi.org/10.1016/j.jplph.2010.08.017
15. Khastkhodaei S, Sharifi G, Salahi R, Rahnamaeian M, Moattar F. Clinical efficacy of Stragol herbal heart drop in ischemic heart failure of stable chest angina. Eur J Intern Med 2011; 3:e201-7; http://dx.doi. org/10.1016/j.eujim.2011.07.004
16. Corpas FJ, Leterrier M, Valderrama R, Airaki M, Chaki M, Palma JM, Barroso JB. Nitric oxide imbalance provokes a nitrosative response in plants under abiotic stress. Plant Sci 2011; 181:604-11; PMID:21893257; http://dx.doi.org/10.1016/j.plantsci.2011.04.005
17. Rakwal R, Agrawal GK. Wound signalingcoordination of the octadecanoid and MAPK pathways. Plant Physiol Biochem 2003; 41:855-61; http://dx.doi.org/10.1016/S0981-9428(03)00142-6
18. Ellard-Ivey M, Douglas CJ. Role of jasmonates in the elicitor-and wound-inducible expression of defense genes in parsley and transgenic tobacco. Plant Physiol 1996; 112:183-92; PMID:12226384
19. Rahnamaeian M. Antimicrobial peptides: modes of mechanism, modulation of defense responses. Plant Signal Behav 2011; 6:1325-32; PMID:21847025; http://dx.doi.org/10.4161/psb.6.9.16319
20. Ouyang B, Yang T, Li H, Zhang L, Zhang Y, Zhang J, Fei Z, Ye Z. Identification of early salt stress response genes in tomato root by suppression subtractive hybridization and microarray analysis. J Exp Bot 2007; 58:507-20; PMID:17210988; http://dx.doi. org/10.1093/jxb/erl258
21. Jamil M, Iqbal W, Bangash A, Rehman SUR, Imran QM, Rha EUIS. Constitutive expression of OSC3H33, OSC3H50 and OSC3H37 genes in rice under salt stress. Pak J Bot 2010; 42:4003-9
22. Gong Z, Koiwa H, Cushman MA, Ray A, Bufford D, Kore-eda S, Matsumoto TK, Zhu J, Cushman JC, Bressan RA, et al. Genes that are uniquely stress regulated in salt overly sensitive (sos) mutants. Plant Physiol 2001; 126:363-75; PMID:11351099; http:// dx.doi.org/10.1104/pp.126.1.363
23. Knight H, Knight MR. Abiotic stress signalling pathways: specificity and cross-talk. Trends Plant Sci 2001; 6:262-7; PMID:11378468; http://dx.doi. org/10.1016/S1360-1385(01)01946-X
24. Rahnamaeian M, Langen G, Imani J, Khalifa W, Altincicek B, von Wettstein D, Kogel KH, Vilcinskas A. Insect peptide metchnikowin confers on barley a selective capacity for resistance to fungal ascomycetes pathogens. J Exp Bot 2009; 60:4105-14; PMID:19734262; http://dx.doi.org/10.1093/jxb/ erp240
25. Li ZY, Xu ZS, He GY, Yang GX, Chen M, Li LC, Ma YZ. A mutation in Arabidopsis BSK5 encoding a brassinosteroid-signaling kinase protein affects responses to salinity and abscisic acid. Biochem Biophys Res Commun 2012; 426:522-7; PMID:22982312; http://dx.doi.org/10.1016/j.bbrc.2012.08.118
26. Bandurska H, Cieślak M. The interactive effect of water deficit and UV-B radiation on salicylic acid accumulation in barley roots and leaves. Environ Exp Bot 2013; 94:9-18; http://dx.doi.org/10.1016/j. envexpbot.2012.03.001
27. Drzewiecka K, Borowiak K, Bandurska H, Golinski P. Salicylic acid-a potential biomarker of tobacco Bel-W3 cell death developed as a response to ground level ozone under ambient conditions. Acta Biol Hung 2012; 63:231-49; PMID:22695522; http://dx.doi. org/10.1556/ABiol.63.2012.2.6
28. Pan Q, Zhan J, Liu H, Zhang J, Chen J, Wen P, Huang W. Salicylic acid synthesized by benzoic acid 2-hydroxylase participates in the development of thermotolerance in pea plants. Plant Sci 2006; 171:226-33; http://dx.doi.org/10.1016/j.plantsci.2006.03.012
29. Sawada H, Shim I-S, Usui K. Induction of benzoic acid 2-hydroxylase and salicylic acid biosynthesis-Modulation by salt stress in rice seedlings. Plant Sci 2006; 171:263-70; http://dx.doi.org/10.1016/j. plantsci.2006.03.020
30. Harrison AJ, Yu M, Gårdenborg T, Middleditch M, Ramsay RJ, Baker EN, Lott JS. The structure of MbtI from Mycobacterium tuberculosis, the first enzyme in the biosynthesis of the siderophore mycobactin, reveals it to be a salicylate synthase. J Bacteriol 2006; 188:6081-91; PMID:16923875; http://dx.doi. org/10.1128/JB.00338-06
31. Barghouthi S, Payne SM, Arceneaux JE, Byers BR. Cloning, mutagenesis, and nucleotide sequence of a siderophore biosynthetic gene (amoA) from Aeromonas hydrophila. J Bacteriol 1991; 173:5121-8; PMID:1830579
32. Cole ST, Brosch R, Parkhill J, Garnier T, Churcher C, Harris D, Gordon SV, Eiglmeier K, Gas S, Barry CE 3rd, et al. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 1998; 393:537-44; PMID:9634230; http:// dx.doi.org/10.1038/31159
33. Garcion C, Lohmann A, Lamodière E, Catinot J, Buchala A, Doermann P, Métraux JP. Characterization and biological function of the ISOCHORISMATE SYNTHASE2 gene of Arabidopsis. Plant Physiol 2008; 147:1279-87; PMID:18451262; http://dx.doi. org/10.1104/pp.108.119420
34. Gross J, Cho WK, Lezhneva L, Falk J, Krupinska K, Shinozaki K, Seki M, Herrmann RG, Meurer J. A plant locus essential for phylloquinone (vitamin K1) biosynthesis originated from a fusion of four eubacterial genes. J Biol Chem 2006; 281:17189-96; PMID:16617180; http://dx.doi.org/10.1074/jbc. M601754200
35. Bell-Lelong DA, Cusumano JC, Meyer K, Chapple C. Cinnamate-4-hydroxylase expression in Arabidopsis. Regulation in response to development and the environment. Plant Physiol 1997; 113:729-38; PMID:9085570; http://dx.doi.org/10.1104/ pp.113.3.729
36. Mizutani M, Ohta D, Sato R. Isolation of a cDNA and a genomic clone encoding cinnamate 4-hydroxylase from Arabidopsis and its expression manner in planta. Plant Physiol 1997; 113:755-63; PMID:9085571; http://dx.doi.org/10.1104/pp.113.3.755
37. Richard S, Lapointe G, Rutledge RG, Séguin A. Induction of chalcone synthase expression in white spruce by wounding and jasmonate. Plant Cell Physiol 2000; 41:982-7; PMID:11038059; http://dx.doi. org/10.1093/pcp/pcd017
38. Campos R, Nonogaki H, Suslow T, Saltveit ME. Isolation and characterization of a wound inducible phenylalanine ammonia-lyase gene (LsPAL1) from Romaine lettuce leaves. Physiol Plant 2004; 121:429-38; http://dx.doi.org/10.1111/j.1399-3054.2004.00336.x
39. Mellway RD, Tran LT, Prouse MB, Campbell MM, Constabel CP. The wound-, pathogen-, and ultraviolet B-responsive MYB134 gene encodes an R2R3 MYB transcription factor that regulates proanthocyanidin synthesis in poplar. Plant Physiol 2009; 150:924-41; PMID:19395405; http://dx.doi.org/10.1104/ pp.109.139071
40. Schulz W, Eiben HG, Hahlbrock K. Expression in Escherichia coli of catalytically active phenylalanine ammonia-lyase from parsley. FEBS Lett 1989; 258:335-8; PMID:2689222; http://dx.doi. org/10.1016/0014-5793(89)81687-4
41. Logemann E, Parniske M, Hahlbrock K. Modes of expression and common structural features of the complete phenylalanine ammonia-lyase gene family in parsley. Proc Natl Acad Sci U S A 1995; 92:5905-9; PMID:7597051; http://dx.doi.org/10.1073/ pnas.92.13.5905
42. Chapple C. Molecular-genetic analysis on plant cytochrome P450-dependent monooxygenases. Annu Rev Plant Physiol Plant Mol Biol 1998; 49:311-43; PMID:15012237; http://dx.doi.org/10.1146/annurev. arplant.49.1.311
43. Batard Y, Schalk M, Pierrel MA, Zimmerlin A, Durst F, Werck-Reichhart D. Regulation of the Cinnamate 4-Hydroxylase (CYP73A1) in Jerusalem Artichoke Tubers in Response to Wounding and Chemical Treatments. Plant Physiol 1997; 113:951-9; PMID:12223655
44. Singh K, Kumar S, Rani A, Gulati A, Ahuja PS. Phenylalanine ammonia-lyase (PAL) and cinnamate 4-hydroxylase (C4H) and catechins (flavan-3-ols) accumulation in tea. Funct Integr Genomics 2009; 9:125-34; PMID:18679731; http://dx.doi. org/10.1007/s10142-008-0092-9
45. Kim JK, Bamba T, Harada K, Fukusaki E, Kobayashi A. Time-course metabolic profiling in Arabidopsis thaliana cell cultures after salt stress treatment. J Exp Bot 2007; 58:415-24; PMID:17118972; http://dx.doi. org/10.1093/jxb/erl216
46. Walia H, Wilson C, Condamine P, Liu X, Ismail AM, Zeng L, Wanamaker SI, Mandal J, Xu J, Cui X, et al. Comparative transcriptional profiling of two contrasting rice genotypes under salinity stress during the vegetative growth stage. Plant Physiol 2005; 139:822-35; PMID:16183841; http://dx.doi. org/10.1104/pp.105.065961
47. Al-Whaibi MH, Siddiqui MH, Basalah MO. Salicylic acid and calcium-induced protection of wheat against salinity. Protoplasma 2012; 249:769-78; PMID:21979309; http://dx.doi.org/10.1007/ s00709-011-0322-1
48. Lee S, Kim SG, Park CM. Salicylic acid promotes seed germination under high salinity by modulating antioxidant activity in Arabidopsis. New Phytol 2010; 188:626-37; PMID:20663063; http://dx.doi. org/10.1111/j.1469-8137.2010.03378.x
49. Catinot J, Buchala A, Abou-Mansour E, Métraux JP. Salicylic acid production in response to biotic and abiotic stress depends on isochorismate in Nicotiana benthamiana. FEBS Lett 2008; 582:473-8; PMID:18201575; http://dx.doi.org/10.1016/j. febslet.2007.12.039
50. Belchí-Navarro S, Almagro L, Sabater-Jara AB, Fernández-Pérez F, Bru R, Pedreño MA. Induction of trans-resveratrol and extracellular pathogenesis-related proteins in elicited suspension cultured cells of Vitis vinifera cv Monastrell. J Plant Physiol 2013; 170:258-64; PMID:23127362; http://dx.doi.org/10.1016/j. jplph.2012.10.003
51. Hunter LJR, Westwood JH, Heath G, Macaulay K, Smith AG, Macfarlane SA, Palukaitis P, Carr JP. Regulation of RNA-dependent RNA polymerase 1 and isochorismate synthase gene expression in Arabidopsis. PLoS One 2013; 8:e66530; PMID:23799112; http:// dx.doi.org/10.1371/journal.pone.0066530
52. Simoh S, Linthorst HJ, Lefeber AW, Erkelens C, Kim HK, Choi YH, Verpoorte R. Metabolic changes of Brassica rapa transformed with a bacterial isochorismate synthase gene. J Plant Physiol 2010; 167:1525-32; PMID:20705362; http://dx.doi. org/10.1016/j.jplph.2010.06.022
53. Kunkel BN, Brooks DM. Cross talk between signaling pathways in pathogen defense. Curr Opin Plant Biol 2002; 5:325-31; PMID:12179966; http://dx.doi. org/10.1016/S1369-5266(02)00275-3
54. Lee S, Ishiga Y, Clermont K, Mysore KS. Coronatine inhibits stomatal closure and delays hypersensitive response cell death induced by nonhost bacterial pathogens. PeerJ 2013; 1:e34; PMID:23638370; http://dx.doi.org/10.7717/peerj.34
55. Hayat Q, Hayat S, Irfan M, Ahmad A. Effect of exogenous salicylic acid under changing environment: a review. Environ Exp Bot 2012; 68:14-25; http:// dx.doi.org/10.1016/j.envexpbot.2009.08.005
56. Saghai-Maroof MA, Soliman KM, Jorgensen RA, Allard RW. Ribosomal DNA spacer-length polymorphisms in barley: mendelian inheritance, chromosomal location, and population dynamics. Proc Natl Acad Sci U S A 1984; 81:8014-8; PMID:6096873; http://dx.doi.org/10.1073/pnas.81.24.8014
57. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, et al. ClustalW and ClustalX version 2. Bioinformatics 2007; 23:2947-8; PMID:17846036; http://dx.doi.org/10.1093/ bioinformatics/btm404
58. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987; 4:406-25; PMID:3447015
59. Zuckerkandl E, Pauling L. Evolutionary divergence and convergence in proteins. In: Evolving Genes and Proteins. Bryson V and Vogel HJ, eds. New York: Academic Press, 1965: 97-166
60. Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, Chevenet F, Dufayard JF, Guindon S, Lefort V, Lescot M, et al. Phylogeny. fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 2008; 36:W465-9; PMID:18424797; http://dx.doi.org/10.1093/nar/ gkn180
61. Maeda H, Dudareva N. The shikimate pathway and aromatic amino Acid biosynthesis in plants. Annu Rev Plant Biol 2012; 63:73-105; http://dx.doi.org/10.1146/ annurev-arplant-042811-105439; PMID:22554242
62. Naoumkina MA, Zhao Q, Gallego-Giraldo L, Dai X, Zhao PX, Dixon RA. Genome-wide analysis of phenylpropanoid defence pathways. Mol Plant Pathol 2010; 11:829-46; http://dx.doi.org/10.1111/j.1364-3703.2010.00648.x; PMID:21029326
63. Vogt T. Phenylpropanoid biosynthesis. Mol Plant 2010; 3:2-20; http://dx.doi.org/10.1093/mp/ssp106; PMID:20035037
64. Wang X. Structure, function, and engineering of enzymes in isoflavonoid biosynthesis. Funct Integr Genomics 2011; 11:13-22; http://dx.doi.org/10.1007/ s10142-010-0197-9; PMID:21052759