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Modulation of Polyamine Metabolism in Arabidopsis Thaliana by Salicylic Acid

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Modulation of Polyamine Metabolism in Arabidopsis Thaliana by Salicylic Acid bioRxiv preprint doi: https://doi.org/10.1101/2020.10.28.359752; this version posted October 29, 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 The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.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 1 Title: Modulation of polyamine metabolism in Arabidopsis thaliana by salicylic acid 2 Running title: Salicylic acid and polyamines in Arabidopsis 3 Authors: Franco R. Rossi, Andrés Gárriz, María Marina and Fernando L. Pieckenstain# 4 Afiliation: Instituto Tecnológico Chascomús (INTECH), Universidad Nacional de General 5 San Martín (UNSAM)-Consejo Nacional de Investigaciones Científicas y Técnicas 6 (CONICET), Av. Intendente Marino Km 8,2 , CC 164 (7130) Chascomús, Argentina. 7 Franco R. Rossi, [email protected] 8 Andrés Gárriz, [email protected] 9 María Marina, [email protected] 10 Fernando L. Pieckenstain, [email protected] 11 #Corresponding author, Fernando L. Pieckenstain 12 13 Date of submission, October 28th 2020 14 Number of figures, 7 15 Number of supplementary figures, 3 16 Number of supplementary tables, 1 17 Word count (start of the introduction to the end of the acknowledgements, excluding 18 materials and methods): 5090 19 20 Highlight 21 Salicylic acid modulates polyamine biosynthesis and catabolism in Arabidopsis. 22 Regulatory effects of salicylic acid are independent of the master regulator NPR1 and 23 are mediated by the MPK6 kinase. 24 1 bioRxiv preprint doi: https://doi.org/10.1101/2020.10.28.359752; this version posted October 29, 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 The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.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. 2 25 Abstract: 26 Polyamines (PAs) play important roles in plant defense against pathogens, but 27 the regulation of PA metabolism by hormone-mediated defense signaling pathways 28 has not been studied in depth. In this study, the modulation of PA metabolism in 29 Arabidopsis by salicylic acid (SA) was analyzed, by combining the exogenous 30 application of this hormone with the use of PA biosynthesis and SA synthesis/signaling 31 mutants. SA induced notable modifications of polyamine metabolism, mainly 32 consisting in putrescine accumulation both in whole-plant extracts and apoplastic 33 fluids. Put was accumulated at the expense of increased biosynthesis by arginine 34 decarboxylase 2 and decreased oxidation by copper amine oxidase. Enhancement of 35 Put levels by SA was independent of the regulatory protein Non-Expressor of 36 Pathogenesis Related 1 (NPR1) and the signaling kinases MKK4 and MPK3, but 37 depended on MPK6. On its part, plant infection by Pseudomonas syringae pv. tomato 38 DC3000 elicited Put accumulation in a SA-dependent way. The present study 39 demonstrates a clear connection between SA signaling and plant PA metabolism in 40 Arabidopsis and contributes to understand the mechanisms by which SA modulates PA 41 levels during plant-pathogen interactions. 42 43 Keywords: Polyamines, salicylic acid, Putrescine, Arginine decarboxylase, MAPK, NPR1, 44 Plant-pathogen interactions, Apoplast, Pseudomonas syringae 45 46 Abbreviations 47 ADC, arginine decarboxylase; AOs, amine oxidases; AWFs, apoplastic washing 48 fluids; CFUs, colony forming units; Col-0, Columbia-0; CuAO, copper-containing amine 49 oxidase; HPT, hours post-treatment; NPR1, Non-Expressor of Pathogenesis Related 1; 50 ODC, ornithine decarboxylase; PAO, polyamine oxidase; PAs, polyamines; Pst, 51 Pseudomonas syringae pv. tomato strain DC3000; Put, putrescine; SA, salicylic acid; 52 SAMDC, S-adenosylmethionine decarboxylase; Spd, spermidine; SPDS, spermidine 53 synthase; Spm, spermine; SPMS, spermine synthase. 54 2 bioRxiv preprint doi: https://doi.org/10.1101/2020.10.28.359752; this version posted October 29, 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. 3 55 Introduction 56 In nature, plants are continuously challenged by pathogenic microorganisms 57 that pose serious threats to their growth and development. Nevertheless, these 58 biological interactions rarely result in disease because plants have developed, through 59 their evolution, sophisticated defense mechanisms that allow them to avoid the 60 deleterious consequences of infection (Berens et al., 2017). In this trend, after the 61 recognition of the pathogen, plants activate different local and systemic signaling 62 pathways mediated by hormones such as salicylates, jasmonates and ethylene, with 63 the purpose to hinder the propagation of the microorganism to the rest of the plant 64 and/or prepare the plant for future attacks. These responses involve the activation of 65 protein kinases conducing to the expression of defense proteins and the accumulation 66 of different compounds that globally contribute to plant defense. 67 Salicylic acid (SA) is a plant defense hormone that plays critical roles in plant 68 immunity. Signaling cascades mediated by this hormone are required for the activation 69 of key processes involved in plant defense. Thus, SA accumulation is associated with 70 the hypersensitive response, a type of programmed cell death usually induced during 71 effector-triggered immunity (Radojičić et al., 2018). In addition, SA participates in the 72 establishment of the systemic acquired resistance, a set of defense responses 73 triggered in uninfected distal tissues that helps plants to defend themselves against 74 further infections by a broad spectrum of pathogens. In Arabidopsis, downstream SA 75 signaling is mainly coordinated via the transcriptional regulator NPR1, whose 76 degradation is controlled by its paralogues NPR3/NPR4 in a SA concentration- 77 dependent manner (Fu et al., 2012; Moreau et al., 2012), and specific MAPK (also 78 named MPK) proteins that exert positive (AtMPK3 and AtMPK6) and negative 79 (AtMPK4) effects on defense gene expression (Colcombet and Hirt, 2008). Additionally, 80 SA was shown to activate defense responses by an NPR1-independent pathway 81 (Uquillas et al., 2004; Herrera-Vásquez et al., 2015; Singh et al., 2018). 82 PAs, mainly the diamine putrescine (Put), the triamine spermidine (Spd) and 83 the tetraamine spermine (Spm), are natural aliphatic polycations essential for 84 prokaryotic and eukaryotic cells. As PAs are positively charged at physiological pH, they 85 interact with anionic molecules such as proteins, nucleic acids and phospholipids. As a 3 bioRxiv preprint doi: https://doi.org/10.1101/2020.10.28.359752; this version posted October 29, 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. 4 86 consequence, they modulate protein–protein (Thomas et al., 1999; Garufi et al., 2007) 87 and DNA–protein interactions (Shah et al., 1999; D’Agostino et al., 2005), as well as 88 RNA structure (Igarashi and Kashiwagi, 2010). In this way, PAs regulate many 89 fundamental cellular processes such as cell division, differentiation and proliferation, 90 cell death, DNA and protein synthesis, gene expression, and stress responses (Seiler 91 and Raul, 2005; Kusano et al., 2008; Igarashi and Kashiwagi, 2010; Romero et al., 92 2018). In plants, different routes are involved in the synthesis of Put. Thus, this PA may 93 be obtained after the decarboxylation of ornithine by ornithine decarboxylase (ODC). 94 On the other hand, arginine can be converted into agmatine by the enzyme arginine 95 decarboxylase (ADC), which is later metabolized to Put in two additional reactions 96 catalyzed by agmatine iminohydrolase and N-carbamoylputrescine amidohydrolase. A 97 novel route for Put production from arginine was recently described to operate in 98 Arabidopsis and soybean. This pathway is located in chloroplasts and involves 99 arginases that also deploy agmatinase activity (Patel et al., 2017). The synthesis of the 100 higher PAs Spd and Spm requires decarboxylated S-adenosylmethionine generated by 101 the action of S-adenosylmethionine decarboxylase (SAMDC). Decarboxylated S- 102 adenosylmethionine functions as an aminopropyl donor in the reactions catalyzed by 103 spermidine synthase (SPDS) and spermine synthase (SPMS), which in two consecutive 104 reactions add aminopropyl moieties to convert Put into Spd, and Spd into Spm, 105 respectively. Interestingly, Arabidopsis has lost the ODC gene and thus depends 106 exclusively on the arginine routes for Put synthesis (Hanfrey et al., 2001; Fuell et al., 107 2010). As a consequence, modulation of ADC activity in this species is of key 108 importance for the regulation of PA levels. Arabidopsis possess two ADC genes 109 (AtADC1 and 2), which are differentially regulated during ontogenesis (Hummel et al., 110 2004) and in response to distinct environmental stimuli (Alcazar et al., 2012; Rossi et 111 al., 2015). Simultaneous knockout of both AtADC genes leads to a lethal phenotype, 112 thus confirming that Arabidopsis strongly depends on ADC for Put biosynthesis (Urano 113 et al., 2005). In addition to de novo biosynthesis, PA levels are also regulated by 114 catabolic pathways. PAs are oxidatively deaminated by amine oxidases (AOs), which 115 can be classified into FAD- dependent (PAOs) and copper-containing (CuAO) enzymes. 116 PAOs catalyze the oxidative deamination of Spm, Spd and/or their acetylated 117 derivatives at the secondary amino group, whereas CuAOs catalyze the oxidation of 4 bioRxiv preprint doi: https://doi.org/10.1101/2020.10.28.359752; this version posted October 29, 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.
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