Ukr.Biochem.J. 2017; Том 89, № 1, січень-лютий, c. 5-21

doi: https://doi.org/10.15407/ubj89.01.005

Ліпоксигенази та їхні метаболіти у формуванні стресостійкості рослин

Л. М. Бабенко1, М. М. Щербатюк1, Т. Д. Скатерна2, І. В. Косаківська1

1Інститут ботаніки ім. М. Г. Холодного НАН України, Київ;
2Інститут біохімії ім, О. В. Палладіна НАН України, Київ;
e-mail: lilia.babenko@gmail.com

В огляді наведено дані літератури останніх років із молекулярної ензимології ліпоксигеназ – протеїнів, задіяних у реакціях пероксидного окислення ліпідів і знайдених у тварин і рослин. Розглянуто й узагальнено існуючі уявлення щодо особливостей будови, каталітичних властивостей та функціонування ензимів родини ліпоксигеназ і продуктів їхньої каталітичної активності в рослинах. Обговорюються питання локалізації ензиму в рослинних клітинах і тканинах, еволюції та розповсюдження ліпоксигеназ, участі в утворенні сигнальних речовин, задіяних у формуванні адаптаційної відповіді на абіотичні та біотичні стресорні чинники, а також регуляції активності ліпоксигеназної (ЛОГ) сигнальної системи. Розглянуто елементи процесів рецепції та трансдукції сигналів ЛОГ-шляху до геному. Особливу увагу приділено жасмонатам, метаболітам аленоксидсинтазної гілки ліпоксигеназного каскаду. Ці метаболіти виявляють високу біологічну активність, повсюдно поширені в рослинних організмах, а також беруть участь у регуляції життєво важливих процесів. Проаналізовано результати щодо філогенії ліпоксигеназ, можливості існування спільного попередника сучасних ізоформ ензиму про/евкаріот. Подано окремі результати власних досліджень авторів стосовно використання показників каталітичної активності ліпоксигеназ як біологічних маркерів під час дослідження стресостійкості рослин.

Ключові слова: , , , ,


Посилання:

  1. Tarchevsky IA. The metabolism of plants under stress. Kazan: Fen, 2001, 448 p. (In Russian).
  2. Benková E. Plant hormones in interactions with the environment. Plant Mol Biol. 2016 Aug;91(6):597. PubMed, PubMedCentral, CrossRef
  3. Dmitriev AP. Signalling molecules for activation of plant defense reactions in response to biotic stress. Russ J Plant Physiol. 2003;50(3):1-10.
  4. Tarchevsky IA. Signalling system of plant cells. M.: Nayka, 2002. 294 p. (In Russian).
  5. Feussner I, Wasternack C. The lipoxygenase pathway. Annu Rev Plant Biol. 2002;53:275-97. Review. PubMed
  6. Porta H, Rocha-Sosa M. Plant lipoxygenases. Physiological and molecular features. Plant Physiol. 2002 Sep;130(1):15-21. Review. PubMed, PubMedCentral
  7. Santino A, Taurino M, De Domenico S, Bonsegna S, Poltronieri P, Pastor V, Flors V. Jasmonate signaling in plant development and defense response to multiple (a)biotic stresses. Plant Cell Rep. 2013 Jul;32(7):1085-98. Review. PubMed, CrossRef
  8. Savchenko TV, Zastrijnaja OM, Klimov VV. Oxylipins and plant abiotic stress resistance. Biochemistry (Mosc). 2014 Apr;79(4):362-75. Review. PubMed, CrossRef
  9. Babenko LМ, Kosakivska ІV, Skaterna TD. Jasmonic acid: a role in the regulation of biotechnology and biochemical processes in plants. Biotechnologia Acta. 2015; 8(2):36-51. CrossRef
  10. Wasternack C, Hause B. Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany. Ann Bot. 2013 Jun;111(6):1021-58. Review. PubMed, PubMedCentral, CrossRef
  11. Andreou A, Feussner I. Lipoxygenases – Structure and reaction mechanism. Phytochemistry. 2009 Sep;70(13-14):1504-10. Review. PubMed, CrossRef
  12. Su C, Sahlin M, Oliw EH. A protein radical and ferryl intermediates are generated by linoleate diol synthase, a ferric hemeprotein with dioxygenase and hydroperoxide isomerase activities. J Biol Chem. 1998 Aug 14;273(33):20744-51. PubMed, CrossRef
  13. Brash AR. Lipoxygenases: occurrence, functions, catalysis, and acquisition of substrate. J Biol Chem. 1999 Aug 20;274(34):23679-82. Review. PubMed, CrossRef
  14. Liavonchanka A, Feussner I. Lipoxygenases: occurrence, functions and catalysis. J Plant Physiol. 2006 Feb;163(3):348-57. Review. PubMed, CrossRef
  15. Glickman MH, Klinman JP. Lipoxygenase reaction mechanism: demonstration that hydrogen abstraction from substrate precedes dioxygen binding during catalytic turnover. Biochemistry. 1996 Oct 1;35(39):12882-92. PubMed, CrossRef
  16. Kulkarni S, Das S, Funk CD, Murray D, Cho W. Molecular basis of the specific subcellular localization of the C2-like domain of 5-lipoxygenase. J Biol Chem. 2002 Apr 12;277(15):13167-74. PubMed, CrossRef
  17. Rizo J, Südhof TC. C2-domains, structure and function of a universal Ca2+-binding domain. J Biol Chem. 1998 Jun 26;273(26):15879-82. Review. PubMed, CrossRef
  18. Chahinian H, Sias B, Carrière F. The C-terminal domain of pancreatic lipase: functional and structural analogies with c2 domains. Curr Protein Pept Sci. 2000 Jul;1(1):91-103. Review.  PubMed, CrossRef
  19. Stahelin RV, Rafter JD, Das S, Cho W. The molecular basis of differential subcellular localization of C2 domains of protein kinase C-alpha and group IVa cytosolic phospholipase A2. J Biol Chem. 2003 Apr 4;278(14):12452-60.  PubMed, CrossRef
  20. Banci L, Cavallaro G, Kheifets V, Mochly-Rosen D. Molecular dynamics characterization of the C2 domain of protein kinase Cbeta. J Biol Chem. 2002 Apr 12;277(15):12988-97. PubMed, CrossRef
  21. Ochoa WF, Corbalán-Garcia S, Eritja R, Rodríguez-Alfaro JA, Gómez-Fernández JC, Fita I, Verdaguer N. Additional binding sites for anionic phospholipids and calcium ions in the crystal structures of complexes of the C2 domain of protein kinase calpha. J Mol Biol. 2002 Jul 5;320(2):277-91.  PubMed, CrossRef
  22. Hörnig C, Albert D, Fischer L, Hörnig M, Rådmark O, Steinhilber D, Werz O. 1-Oleoyl-2-acetylglycerol stimulates 5-lipoxygenase activity via a putative (phospho)lipid binding site within the N-terminal C2-like domain. J Biol Chem. 2005 Jul 22;280(29):26913-21.  PubMed, CrossRef
  23. Sudharshan E, Rao AG. Rapid method to separate the domains of soybean lipoxygenase-1: identification of the interdomain interactions. FEBS Lett. 1997 Apr 7;406(1-2):184-8. PubMed, CrossRef
  24. Maccarrone M, Salucci ML, van Zadelhoff G, Malatesta F, Veldink G, Vliegenthart JF, Finazzi-Agrò A. Tryptic digestion of soybean lipoxygenase-1 generates a 60 kDa fragment with improved activity and membrane binding ability. Biochemistry. 2001 Jun 12;40(23):6819-27.  PubMed, CrossRef
  25. Göbel C, Feussner I, Schmidt A, Scheel D, Sanchez-Serrano J, Hamberg M, Rosahl S. Oxylipin profiling reveals the preferential stimulation of the 9-lipoxygenase pathway in elicitor-treated potato cells. J Biol Chem. 2001 Mar 2;276(9):6267-73.  PubMed, CrossRef
  26. Maccarrone M, Melino G, Finazzi-Agrò A. Lipoxygenases and their involvement in programmed cell death. Cell Death Differ. 2001 Aug;8(8):776-84. Review.  PubMed, CrossRef
  27. Taki N, Sasaki-Sekimoto Y, Obayashi T, Kikuta A, Kobayashi K, Ainai T, Yagi K, Sakurai N, Suzuki H, Masuda T, Takamiya K, Shibata D, Kobayashi Y, Ohta H. 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. 2005 Nov;139(3):1268-83. PubMed, PubMedCentral, CrossRef
  28. Vellosillo T, Martínez M, López MA, Vicente J, Cascón T, Dolan L, Hamberg M, Castresana C. Oxylipins produced by the 9-lipoxygenase pathway in Arabidopsis regulate lateral root development and defense responses through a specific signaling cascade. Plant Cell. 2007 Mar;19(3):831-46.  PubMed, PubMedCentral, CrossRef
  29. Mosblech A, Feussner I, Heilmann I. Oxylipins: structurally diverse metabolites from fatty acid oxidation. Plant Physiol Biochem. 2009 Jun;47(6):511-7. Review.  PubMed, http://dx.doi.org/10.1016/j.plaphy.2008.12.011″]
  30. Schwarz K, Walther M, Anton M, Gerth C, Feussner I, Kuhn H. Structural basis for lipoxygenase specificity. Conversion of the human leukocyte 5-lipoxygenase to a 15-lipoxygenating enzyme species by site-directed mutagenesis. J Biol Chem. 2001 Jan 5;276(1):773-9.  PubMed, CrossRef
  31. Delporte A, Lannoo N, Vandenborre G, Ongenaert M, Van Damme EJ. Jasmonate response of the Nicotiana tabacum agglutinin promoter in Arabidopsis thaliana. Plant Physiol Biochem. 2011 Aug;49(8):843-51. PubMed, CrossRef
  32. Ballaré CL. Jasmonate-induced defenses: a tale of intelligence, collaborators and rascals. Trends Plant Sci. 2011 May;16(5):249-57. Review.  PubMed, CrossRef
  33. Piotrowska A, Bajguz A. Conjugates of abscisic acid, brassinosteroids, ethylene, gibberellins, and jasmonates. Phytochemistry. 2011 Dec;72(17):2097-112. Review.  PubMed, CrossRef
  34. Van der Ent S, Van Wees SC, Pieterse CM. Jasmonate signaling in plant interactions with resistance-inducing beneficial microbes. Phytochemistry. 2009 Sep;70(13-14):1581-8. Review.  PubMed, CrossRef
  35. Suza WP, Avila CA, Carruthers K, Kulkarni S, Goggin FL, Lorence A. Exploring the impact of wounding and jasmonates on ascorbate metabolism. Plant Physiol Biochem. 2010 May;48(5):337-50. Review.  PubMed, PubMedCentral, CrossRef
  36. Tamogami S, Rakwal R, Aqrawal GK. Interplant communication: Airborne methyl jasmonate is essentially converted into JA and Witt stock, JA-Ile activating jasmonate signaling pathway and VOCs emission. Biochem Biophys Res Commun. 2008 Nov;376(4):723-727.  CrossRef
  37. Floerl S, Majcherczyk A, Possienke M, Feussner K, Tappe H, Gatz C, Feussner I, Kües U, Polle A. Verticillium longisporum infection affects the leaf apoplastic proteome, metabolome, and cell wall properties in Arabidopsis thaliana. PLoS One. 2012;7(2):e31435.  PubMed, PubMedCentral, CrossRef
  38. Hughes RK, De Domenico S, Santino A. Plant cytochrome CYP74 family: biochemical features, endocellular localisation, activation mechanism in plant defence and improvements for industrial applications. Chembiochem. 2009 May 4;10(7):1122-33.  PubMed, CrossRef
  39. Quaglia M, Fabrizi M, Zazzerini A, Zadra C. Role of pathogen-induced volatiles in the Nicotiana tabacum-Golovinomyces cichoracearum interaction. Plant Physiol Biochem. 2012 Mar;52:9-20.  PubMed, CrossRef
  40. Copolovici L, Kännaste A, Pazouki L, Niinemets U. Emissions of green leaf volatiles and terpenoids from Solanum lycopersicum are quantitatively related to the severity of cold and heat shock treatments. J Plant Physiol. 2012 May 1;169(7):664-72.  PubMed, CrossRef
  41. Stumpe M, Göbel C, Demchenko K, Hoffmann M, Klösgen RB, Pawlowski K, Feussner I. Identification of an allene oxide synthase (CYP74C) that leads to formation of alpha-ketols from 9-hydroperoxides of linoleic and linolenic acid in below-ground organs of potato. Plant J. 2006 Sep;47(6):883-96.  PubMed, CrossRef
  42. Huang FC, Schwab W. Cloning and characterization of a 9-lipoxygenase gene induced by pathogen attack from Nicotiana benthamiana for biotechnological application. BMC Biotechnol. 2011 Mar 30;11:30.  PubMed, PubMedCentral, CrossRef
  43. Royo J, Vancanneyt G, Pérez AG, Sanz C, Störmann K, Rosahl S, Sánchez-Serrano JJ. Characterization of three potato lipoxygenases with distinct enzymatic activities and different organ-specific and wound-regulated expression patterns. J Biol Chem. 1996 Aug 30;271(35):21012-9.  PubMed, CrossRef
  44. Kimura H, Yokota K. Characterization of metabolic pathway of linoleic acid 9-hydroperoxide in cytosolic fraction of potato tubers and identification of reaction products. Appl Biochem Biotechnol. 2004 Jul-Sep;118(1-3):115-32.  PubMed, CrossRef
  45. Droillard MJ, Rouet-Mayer MA, Bureau JM, Lauriere C. Membrane-Associated and Soluble Lipoxygenase Isoforms in Tomato Pericarp (Characterization and Involvement in Membrane Alterations). Plant Physiol. 1993 Dec;103(4):1211-1219.  PubMed, PubMedCentral, CrossRef
  46. Braidot E, Petrussa E, Micolini S, Tubaro F, Vianello A, Macrì F. Biochemical and immunochemical evidences for the presence of lipoxygenase in plant mitochondria. J Exp Bot. 2004 Aug;55(403):1655-62.  PubMed, CrossRef
  47. Kongrit D, Jisaka M, Kobayasi K, Nishigaichi Y, Nishimura K, Nagaya T, Yokota K. Molecular cloning, functional expression, and tissue distribution of a potato sprout allene oxide synthase involved in a 9-lipoxygenase pathway. Biosci Biotechnol Biochem. 2006 Sep;70(9):2160-8.  PubMed, CrossRef
  48. Xu Y, Ishida H, Reisen D, Hanson MR. Upregulation of a tonoplast-localized cytochrome P450 during petal senescence in Petunia inflata. BMC Plant Biol. 2006 Apr 13;6:8.
    PubMed, PubMedCentral
  49. Mita G, Quarta A, Fasano P, De Paolis A, Di Sansebastiano GP, Perrotta C, Iannacone R, Belfield E, Hughes R, Tsesmetzis N, Casey R, Santino A. Molecular cloning and characterization of an almond 9-hydroperoxide lyase, a new CYP74 targeted to lipid bodies. J Exp Bot. 2005 Sep;56(419):2321-33.  PubMed, CrossRef
  50. Farmaki T, Sanmartín M, Jiménez P, Paneque M, Sanz C, Vancanneyt G, León J, Sánchez-Serrano JJ. Differential distribution of the lipoxygenase pathway enzymes within potato chloroplasts. J Exp Bot. 2007;58(3):555-68.  PubMed, CrossRef
  51. Schaller A, Stintzi A. Enzymes in jasmonate biosynthesis – structure, function, regulation. Phytochemistry. 2009 Sep;70(13-14):1532-8. Review.  PubMed, CrossRef
  52. Cho K, Han Y, Woo JC, Baudisch B, Klösgen RB, Oh S, Han J, Han O. Cellular localization of dual positional specific maize lipoxygenase-1 in transgenic rice and calcium-mediated membrane association. Plant Sci. 2011 Sep;181(3):242-8.  PubMed, CrossRef
  53. Jensen AB, Poca E, Rigaud M, Freyssinet G, Pagès M. Molecular characterization of L2 lipoxygenase from maize embryos. Plant Mol Biol. 1997 Mar;33(4):605-14.  PubMed
  54. Eiben HG, Slusarenko AJ. Complex spatial and temporal expression of lipoxygenase genes during Phaseolus vulgaris (L.) development. Plant J. 1994 Jan;5(1):123-35.  PubMed, CrossRef
  55. Howe GA, Jander G. Plant immunity to insect herbivores. Annu Rev Plant Biol. 2008;59:41-66. Review.  PubMed, CrossRef
  56. Kazan K, Manners JM. Jasmonate signaling: toward an integrated view. Plant Physiol. 2008 Apr;146(4):1459-68.  PubMed, PubMedCentral, CrossRef
  57. Ryan CA, Pearce G. Systemin: a polypeptide signal for plant defensive genes. Annu Rev Cell Dev Biol. 1998;14:1-17. Review.  PubMed, CrossRef
  58. Kolupaev YuE, Ystreb TA, Lugovaya AA. Jasmonates role in the adaptation of plants to action for abiotic stressors. Fiziol Rasten Genet. 2016; 48(2): 95– 111. (In Russian).
  59. Narváez-Vásquez J, Ryan CA. The cellular localization of prosystemin: a functional role for phloem parenchyma in systemic wound signaling. Planta. 2004 Jan;218(3):360-9. PubMed, CrossRef
  60. Seo HS, Song JT, Cheong JJ, Lee YH, Lee YW, Hwang I, Lee JS, Choi YD. Jasmonic acid carboxyl methyltransferase: a key enzyme for jasmonate-regulated plant responses. Proc Natl Acad Sci USA. 2001 Apr 10;98(8):4788-93.  PubMed, PubMedCentral, CrossRef
  61. Stuhlfelder C, Mueller MJ, Warzecha H. Cloning and expression of a tomato cDNA encoding a methyl jasmonate cleaving esterase. Eur J Biochem. 2004 Jul;271(14):2976-83. PubMed, CrossRef
  62. Holková I, Bezáková L, Bilka F, Balažová A, Vanko M, Blanáriková V. Involvement of lipoxygenase in elicitor-stimulated sanguinarine accumulation in Papaver somniferum suspension cultures. Plant Physiol Biochem. 2010 Oct-Nov;48(10-11):887-92. PubMed, CrossRef
  63. Sivasankar S, Sheldrick B, Rothstein SJ. Expression of allene oxide synthase determines defense gene activation in tomato. Plant Physiol. 2000 Apr;122(4):1335-42.  PubMed, PubMedCentral, CrossRef
  64. Howe GA, Lee GI, Itoh A, Li L, DeRocher AE. Cytochrome P450-dependent metabolism of oxylipins in tomato. Cloning and expression of allene oxide synthase and fatty acid hydroperoxide lyase. Plant Physiol. 2000 Jun;123(2):711-24.  PubMed, PubMedCentral, CrossRef
  65. Noordermeer MA, Feussner I, Kolbe A, Veldink GA, Vliegenthart JF. Oxygenation of (3Z)-alkenals to 4-hydroxy-(2E)-alkenals in plant extracts: a nonenzymatic process. Biochem Biophys Res Commun. 2000 Oct 14;277(1):112-6.  PubMed, CrossRef
  66. Grechkin AN. Hydroperoxide lyase and divinyl ether synthase. Prostaglandins Other Lipid Mediat. 2002 Aug;68-69:457-70. Review.  PubMed, CrossRef
  67. Froehlich JE, Itoh A, Howe GA. Tomato allene oxide synthase and fatty acid hydroperoxide lyase, two cytochrome P450s involved in oxylipin metabolism, are targeted to different membranes of chloroplast envelope. Plant Physiol. 2001 Jan;125(1):306-17.  PubMed, PubMedCentral, CrossRef
  68. Laudert D, Weiler EW. Allene oxide synthase: a major control point in Arabidopsis thaliana octadecanoid signalling. Plant J. 1998 Sep;15(5):675-84.  PubMed, CrossRef
  69. Gullner G, Ktinstler M, Kiraly L, Pogany M, Tobias I. Up-regulated expression of lipoxygenase and divinyl ether synthase genes in pepper leaves inoculated with Tobamoviruses. Physiol Mol Plant Pathol. 2010 Sep;74(5-6):387-393.  CrossRef
  70. Ivanov I, Heydeck D, Hofheinz K, Roffeis J, O’Donnell VB, Kuhn H, Walther M. Molecular enzymology of lipoxygenases. Arch Biochem Biophys. 2010 Nov 15;503(2):161-74. PubMed, CrossRef
  71. Babenko LM, Voytenko LV, Skaterna TD, Musatenko LI. Lipoxygenase activity in Equisetum arvense L. ontogenesis. Fiziol Rast Genet. 2014;46(1):37–44. (In Ukrainian).
  72. Babenko LM, Skaterna TD, Kosakivska IV. Lypoxigenase activity of Salvinia natans (L.) All. in ontogenesis. Dopov Nac Akad Nauk Ukr. 2016;8:101-108.   (In Ukrainian).
    CrossRef
  73. Shin JH, Van K, Kim DH, Kim KD, Jang YE, Choi BS, Kim MY, Lee SH. The lipoxygenase gene family: a genomic fossil of shared polyploidy between Glycine max and Medicago truncatula. BMC Plant Biol. 2008 Dec 23;8:133.  PubMed, PubMedCentral, CrossRef
  74. Sagan L. On the origin of mitosing cells. J Theor Biol. 1967 Mar;14(3):255-74.  PubMed, CrossRef
  75. Timmis JN, Ayliffe MA, Huang CY, Martin W. Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat Rev Genet. 2004 Feb;5(2):123-35. Review. PubMed, CrossRef
  76. Lorenzo O, Solano R. Molecular players regulating the jasmonate signalling network. Curr Opin Plant Biol. 2005 Oct;8(5):532-40. PubMed, CrossRef
  77. Fabbri AA, Fanelli C, Reverberi M, Ricelli A, Camera E, Urbanelli S, Rossini A, Picardo M, Altamura MM. Early physiological and cytological events induced by wounding in potato tuber. J Exp Bot. 2000 Jul;51(348):1267-75. PubMed, CrossRef
  78. Kosakivska IV, Babenko LM, Ustinova AYu, Skaterna TD. The influence of temperature conditions on lipoxygenase activity in seedling of rape Brassica napus var. Оleifera. Dopov Nac Akad Nauk Ukr. 2012;6:134-137.(In Ukrainian).
  79. Kosakivska IV, Babenko LM, Skaterna TD, Ustinova AYu. Influence оf hypo- and hyperthermia on lipoxygenase activity, content of pigments and soluble proteins in Triticum aestivum L. cv. Yatran 60 seedlings. Fiziol Rast Genet. 2014;46(3):212-220. (In Ukrainian).
  80. Babenko LМ, Kosakivska IV, Akimov YuA, Klymchuk DO, Skaternya TD. Еffect of temperature stresses on pigment content, lipoxygenase activity and cell ultrastructure of winter wheat seedlings. Genet Plant Physiol. 2014; 4(1–2):117-125.
  81. Chandra S, Heinstein PF, Low PS. Activation of Phospholipase A by Plant Defense Elicitors. Plant Physiol. 1996 Mar;110(3):979-986.  PubMed, PubMedCentral, CrossRef
  82. Kolupaev YuE, Karpets YuV. Formation of adaptive responses of plants to abiotic stressful Action. K.: Osnova, 2010. 352 p. (In Russian).
  83. Nishiuchi T, Hamada T, Kodama H, Iba K. Wounding changes the spatial expression pattern of the arabidopsis plastid omega-3 fatty acid desaturase gene (FAD7) through different signal transduction pathways. Plant Cell. 1997 Oct;9(10):1701-12.  PubMed, PubMedCentral, CrossRef
  84. Cohen Y, Gisi U, Niderman T. Local and systemic protection against Phytophthora infestans induced in potato and tomato plants by jasmonic acid and jasmonic-methyl-ester. Phytopathology. 1993;83(10):1054-1062.  CrossRef
  85. Ozeretskovskaya OL, Vasyukova NI, Chalenko GI, Gerasimova NG, Revina TA, Valueva TA. Wound healing and induced resistance in potato tubers. Appl Biochem Microbiol. 2009 March;45(2):199-203. (In Russian).  PubMed, CrossRef
  86. Birkenmeier GF, Ryan CA. Wound signaling in tomato plants. Evidence that aba is not a primary signal for defense gene activation. Plant Physiol. 1998 Jun;117(2):687-93.
    PubMed, PubMedCentral, CrossRef
  87. Campos-Vargas R, Saltveit ME. Involvement of putative chemical wound signals in the induction of phenolic metabolism in wounded lettuce. Physiol Plant. 2002 Jan;114(1):73-84.  PubMed, CrossRef
  88. Strassner J, Schaller F, Frick UB, Howe GA, Weiler EW, Amrhein N, Macheroux P, Schaller A. Characterization and cDNA-microarray expression analysis of 12-oxophytodienoate reductases reveals differential roles for octadecanoid biosynthesis in the local versus the systemic wound response. Plant J. 2002 Nov;32(4):585-601.  PubMed, CrossRef
  89. Stenzel I, Hause B, Maucher H, Pitzschke A, Miersch O, Ziegler J, Ryan CA, Wasternack C. Allene oxide cyclase dependence of the wound response and vascular bundle-specific generation of jasmonates in tomato – amplification in wound signalling. Plant J. 2003 Feb;33(3):577-89. PubMed, CrossRef
  90. Moore JP, Paul ND, Whittaker JB, Taylor JE. Exogenous jasmonic acid mimics herbivore-induced systemic increase in cell wall bound peroxidase activity and reduction in leaf expansion. Funct Ecol. 2003;17(4):549-554.  CrossRef
  91. Park JH, Halitschke R, Kim HB, Baldwin IT, Feldmann KA, Feyereisen R. A knock-out mutation in allene oxide synthase results in male sterility and defective wound signal transduction in Arabidopsis due to a block in jasmonic acid biosynthesis. Plant J. 2002 Jul;31(1):1-12.  PubMedCrossRef
  92. Koshio K, Takahashi H, Ota Y. Induction of browning of male flowers of Cryptomeria japonica by treatment with fatty acids: mechanism and the role of trans-2-hexenal. Plant Cell Physiol. 1995;36(8):1511-1517.
  93. Fukuda A, Nakamura Y, Ohigashi H, Osawa T, Uchida K. Cellular response to the redox active lipid peroxidation products: induction of glutathione S-transferase P by 4-hydroxy-2-nonenal. Biochem Biophys Res Commun. 1997 Jul 18;236(2):505-9.  PubMed, CrossRef
  94. Peña-Cortés H, Fisahn J, Willmitzer L. Signals involved in wound-induced proteinase inhibitor II gene expression in tomato and potato plants. Proc Natl Acad Sci USA. 1995 May 9;92(10):4106-13.  PubMed, PubMedCentral, CrossRef
  95. Royo J, Vancanneyt G, Pérez AG, Sanz C, Störmann K, Rosahl S, Sánchez-Serrano JJ. Characterization of three potato lipoxygenases with distinct enzymatic activities and different organ-specific and wound-regulated expression patterns. J Biol Chem. 1996 Aug 30;271(35):21012-9.  PubMed, CrossRef
  96. Roychoudhury A, Basu S, Sengupta DN. Effects of exogenous abscisic acid on some physiological responses in a popular aromatic indicia rice compared with those from two traditional non-aromatic indicia rice cultivars. Acta Physiol Plant. 2009;31(5):915-926.  CrossRef
  97. Deluc LG, Quilici DR, Decendit A, Grimplet J, Wheatley MD, Schlauch KA, Mérillon JM, Cushman JC, Cramer GR. Water deficit alters differentially metabolic pathways affecting important flavor and quality traits in grape berries of Cabernet Sauvignon and Chardonnay. BMC Genomics. 2009 May 8;10:212.  PubMed, PubMedCentral, CrossRef
  98. Turner JG, Ellis C, Devoto A. The jasmonate signal pathway. Plant Cell. 2002;14 Suppl:S153-64. Review.  PubMed, PubMedCentral
  99. Zhang KW, An Y, Hu Z. Relationship between lipoxygenase and ABA and JA in wounded signal transduction of healthy populous seedlings. Forest Research. 2005;18(3):300-304.
  100. Fedina EO, Karimova FG, Chechetkin IR, Tarchevsky IA, Khripach VA. Contribution of lipoxygenase metabolism to the brassinosteroid signaling pathway. Dokl Biochem Biophys. 2004 Mar-Apr;395:80-3.  PubMed
  101. Kopich VN, Kretynin SV, Kharchenko OV, Litvinovskaya RP, Chashina NM, Khripach VA. Effect of 24-epibrassinolide on lipoxygenase activity in maize seedlings under cold stress. Biopolym Cell. 2010;26(3):218-224. (In Ukrainian).  CrossRef
  102. Ren C, Han C, Peng W, Huang Y, Peng Z, Xiong X, Zhu Q, Gao B, Xie D. A leaky mutation in DWARF4 reveals an antagonistic role of brassinosteroid in the inhibition of root growth by jasmonate in Arabidopsis. Plant Physiol. 2009 Nov;151(3):1412-20.  PubMed, PubMedCentral, CrossRef
  103. Pokotylo IV, Kolesnikov YS, Derevyanchuk MV, Kharitonenko AI, Kravets VS. Lipoxygenases and plant cell metabolism regulation. Ukr Biochem J. 2015 Mar-Apr;87(2):41-55. Review. (In Ukrainian).  PubMed, CrossRef
  104. Ben-Hayyim G, Gueta-Dahan Y, Avsian-Kretchmer O, Weichert H, Feussner I. Preferential induction of a 9-lipoxygenase by salt in salt-tolerant cells of Citrus sinensis L. Osbeck. Planta. 2001 Feb;212(3):367-75.  PubMedCrossRef
  105. Yang XY, Jiang WJ, Yu HJ. The expression profiling of the lipoxygenase (LOX) family genes during fruit development, abiotic stress and hormonal treatments in cucumber (Cucumis sativus L.). Int J Mol Sci. 2012;13(2):2481-500.  PubMed, PubMedCentral, CrossRef
  106. Mao LC , Wang GZ , Zhu CG , Pang HQ.  Involvement of phospholipase D and lipoxygenase in response to chilling stress in postharvest cucumber fruits. Plant Sci. 2007;172(2):400-405.  CrossRef
  107. Skaterna TD, Kharchenko OV. Effect of phosphatidic acid on the reaction of linoleic acid oxidation by 5-lipooxygenase from potato nodules. Ukr Biokhim Zhurn. 2008 May-Jun;80(3):21-30. (In Ukrainian).  PubMed
  108. Kopich VM, Kharchenko OV. The influence of salt stress and abscisic acid on the activity of lipoxygenase corn. Dopov Nac Akad Nauk Ukr. 2011;12:148–152. (In Ukrainian).
  109. Kosakivska IV, Konturska OO, Ustinova AYu. Hypo- and hyperthermia effect on lipoxygenase activity in leaves of plants with different ecological strategies. Ukr Botan Zhurn. 2011;68(6):883-889.(In Ukrainian).

Creative CommonsThis work is licensed under a Creative Commons Attribution 4.0 International License.