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Expression of Tyrosine Hydroxylase Gene from Rat Leads to Oxidative Stress in Potato Plants

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Expression of Tyrosine Hydroxylase Gene from Rat Leads to Oxidative Stress in Potato Plants bioRxiv preprint doi: https://doi.org/10.1101/2020.05.15.098210; this version posted May 17, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 Short title: Oxidative stress upon HT expression in potato. 2 3 Expression of tyrosine hydroxylase gene from rat leads to oxidative stress in potato plants. 4 5 Kamil Kostyn1*, Aleksandra Boba2, Anna Kostyn2,3, Michał Starzycki4, Jan Szopa1,2, Anna Kulma2 6 7 1 Department of Genetics, Plant Breeding and Seed Production, Faculty of Life Sciences and Technology, Wroclaw University 8 of Environmental and Plant Sciences, pl. Grunwaldzki 24A, 50-363 Wroclaw, Poland 9 2 Department of Genetic Biochemistry, Faculty of Biotechnology, University of Wroclaw, Przybyszewskiego 63, 51-148 10 Wroclaw, Poland 11 3 Institute of Genetics and Microbiology, Faculty of Biological Sciences, University of Wroclaw, Przybyszewskiego 63, 51-148 12 Wroclaw, Poland 13 4 The Plant Breeding and Acclimatization Inst. (IHAR)—National Research Inst., Research Div, Poznan, ul. Strzeszyńska 36, 14 60-479 Poznan, Poland 15 * corresponding author ([email protected]; [email protected]) 16 17 One sentence summary: Introduction of rat tyrosine hydroxylase gene to potato disturbs 18 catecholamine synthesis, causes oxidative stress and activates antioxidant response. 19 20 Author Contributions 21 K.K. generated the transgenic lines, analyzed the GC-MS data, performed phenolics assessment with 22 UPLC, performed statistical analysis, wrote the manuscript, agrees to serve as the author responsible 23 for contact and ensures communication; A.B. performed gene transcript level assessment with RT- 24 qPCR; A.K. performed antioxidant potential assays and measured H2O2 levels; M.S. performed 25 infection tests; J.S. conceived the project; A.K. supervised the project. 26 27 Funding information: This study was supported by grant No. 2017/24/C/NZ1/00393 from National 28 Science Centre (NCN, Poland). 29 30 Abstract 31 Catecholamines are biogenic aromatic amines common among both animals and plants. In animals 32 they are synthesized via tyrosine hydroxylation, while in plants, both hydroxylation or 33 decarboxylation of tyrosine are possible, depending on the species, though no tyrosine hydroxylase – 34 a counterpart of animal enzyme has been identified yet. It is known that in potato plants it is the 35 decarboxylation of tyrosine that leads to catecholamine production. In this paper we present the 36 effects of induction of an alternative route of catecholamine production by introducing tyrosine 37 hydroxylase gene from rat. We demonstrate that an animal system can be used by the plant, 38 however, it does not function to synthesize catecholamines. Instead it leads to elevated reactive 1 bioRxiv preprint doi: https://doi.org/10.1101/2020.05.15.098210; this version posted May 17, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 39 oxygen species content and constant stress condition to the plant which responds with elevated 40 antioxidant level and further with improved resistance to infection. 41 42 Keywords 43 catecholamine, potato, tyrosine hydroxylase, ROS, oxidative stress, antioxidants 44 45 Introduction 46 Catecholamines are natural biogenic amines found both in animals and plants. Their biosynthesis 47 route in animals has been well recognized. Shortly, it starts with tyrosine hydroxylation to L-DOPA, 48 catalyzed by tyrosine hydroxylase (TH, EC: 1.14.16.2). L-DOPA is further decarboxylated to dopamine 49 by L-DOPA decarboxylase (DD, EC: 4.1.1.28). This neurotransmitter may undergo hydroxylation by 50 dopamine β-monooxygenase (DH, EC: 1.14.17.1) to norepinephrine, and further to epinephrine by 51 phenylethanolamine N-methyltransferase (PNMT, EC: 2.1.1.28). This main route of catecholamine 52 biosynthesis may be complemented by that employing tyramine as a substrate for dopamine 53 biosynthesis in a reaction driven by a cytochrome P450 isoform (CYP2D6 in human brain or CYP2D in 54 rats) (Wang et al., 2014). Functions of catecholamines in animals (hormones, neurotransmitters) are 55 well recognized, as they have been studied extensively for decades (Goldstein, 2010). 56 Interestingly, the presence of these compounds in plants was shown as early as in the fifties of the 57 previous century (Udenfriend et al., 1959) and confirmed in a number of plant species since (Kulma 58 and Szopa, 2007). The role of catecholamines in plants is not fully recognized. Numerous publications 59 report either on their structural or regulatory functions. They may be substrates for other relevant 60 compounds, like betalains (Gandia-Herrero and Garcia-Carmona, 2013), alkaloids, like mescaline 61 (Aniszewski, 2015), melanins or hydroxycinnamic acid amides. Catecholamine conjugates with 62 hydroxycinnamic acids are important molecules produced upon pathogen infection that may be 63 incorporated into the cell wall reinforcing its structure and providing a tighter barrier for the invading 64 microorganisms (Newman et al., 2001). Their role may be also explained by their antioxidant 65 properties, since catecholamine molecules are potent free radical scavenging agents (Kostyn et al., 66 2012). This activity is even more pronounced in their amide conjugates. Due to neighboring hydroxyl 67 groups in the catechol ring, catecholamines possess remarkable ability to quench free radicals 68 (Kanazawa and Sakakibara, 2000). The DPPH and superoxide scavenging activities of catecholamines 69 were shown to be much higher than those of ascorbic acid and comparable to those of catechin and 70 flavan (Rahman et al., 2006). Moreover, catecholamines reacted with single oxygen distinctively 71 stronger than catechin or sodium azide (Shimizu et al., 2010). Dopamine was shown to be a stronger 72 antioxidant than tocopherol and glutathione (Kostyn et al., 2012), and flavonoids – luteolin and 73 quercetin in vitro (Huang et al., 2019). However, it must be noted that oxidized forms of 74 catecholamines might be toxic and can pose threat to cellular components. Analogously to their 75 function in animals, catecholamines were suggested to control carbohydrate metabolism. In 76 transgenic potatoes they influenced simple sugar content with simultaneous decrease in starch 77 (Swiedrych et al., 2004, Skirycz et al., 2005). Moreover, catecholamine interaction with 78 phytohormones was reported. Catecholamines were shown to stimulate ethylene biosynthesis (Dai 79 et al., 1993) or induce flowering in Lemna paucicostata (Yokoyama et al., 2000). Dopamine was 80 indicated as a mediator of gibberellic acid activity in lettuce hypocotyl (Kamisaka, 1979) and inhibited 81 auxin oxidase in tobacco and Acmella oppositifolia leading to growth stimulation (Protacio et al., 82 1992). 2 bioRxiv preprint doi: https://doi.org/10.1101/2020.05.15.098210; this version posted May 17, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 83 Studies on catecholamine biosynthesis pathway in plants showed their analogy to that found in 84 animals. However, while in animals the route through tyrosine hydroxylation is preferred, in plants 85 both hydroxylation and decarboxylation of tyrosine was confirmed, though not simultaneously, and 86 the active route is probably species-specific (Kulma and Szopa, 2007). Tyrosine decarboxylase (TD) 87 presence in plants has been established and its structure and functions well recognized (Zhu et al., 88 2016). Plant TDs show narrow substrate specificity and can catalyze decarboxylation of tyrosine only 89 or tyrosine and L-DOPA, depending on plant species and/or tissue and developmental stage 90 (Lehmann and Pollmann, 2009, Świędrych et al., 2004). However, despite the fact that the presence 91 of L-DOPA was evidenced in numerous plants (Soares et al., 2014), tyrosine hydroxylase was not 92 found in these organisms. Hydroxylation of tyrosine may be ascribed to other enzymes. For instance, 93 tyrosinase catalyzes the reactions leading to melanin formation, namely the ortho-hydroxylation of 94 monophenols to o-diphenols (monophenolase activity, EC 1.14.18.1) and the subsequent oxidation of 95 o-diphenols to the corresponding o-quinones (diphenolase activity, EC 1.10.3.1). The L-DOPA 96 produced in this pathway is utilized in the synthesis of DOPA-quinone rather than catecholamines 97 (Chung et al., 2015). However, L-DOPA may be decarboxylated to tyramine with the aid of tyrosine 98 decarboxylase, which further is processed to yield catecholamines (Kulma and Szopa, 2007). 99 Nevertheless, tyrosine hydroxylase activity was found in callus cultures of Portulaca grandiflora and 100 it was shown to be different from tyrosinase and polyphenol oxidase activities (Yamamoto et al., 101 2001). In another study an enzyme of tyrosine hydroxylase activity was purified and characterized in 102 Mucuna pruriens (Luthra and Singh, 2010). It was highly specific to tyrosine, but showed also a slight 103 activity to tyramine converting it to dopamine, although catalysis of such reaction is usually ascribed
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