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Genome-wide identification and expression profiling of copper-containing amine oxidase genes in sweet orange (Citrus sinensis)

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Abstract

Copper-containing amine oxidases (CuAOs) play important roles in polyamine catabolism and function in plant development and abiotic stresses response. In this study, eight putative CuAO genes (CsCuAO1–CsCuAO8), distributed on three chromosomes, were identified in sweet orange (Citrus sinensis Osbeck) genome. They were divided into two major groups according to the phylogenetic analysis. The CsCuAOs possess typically conserved 33 amino acid residues and contain either a C-terminal peroxisomal targeting peptide or an N-terminal signal. Transcript levels of the CsCuAOs were detected in leaf, stem cotyledon, and root, but tissue-specific expression pattern was observed. Many putative cis-elements involved in hormone and stress response were predicted in a 1.5-kb promoter region of the CsCuAOs. The CsCuAOs were significantly induced by exogenous polyamines, including putrescine, spermidine, and spermine. ABA and various abiotic stresses (cold, salt, and osmotic shock) down-regulated most of the CsCuAOs, whereas CsCuAO3 and CsCuAO7 were up-regulated. Transient expression assay demonstrate that CsCuAO2 was involved in putrescine catabolism. Taken together, these findings provide valuable knowledge for better understanding of the potential biological functions of CuAO genes in polyamine catabolism of sweet orange.

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Abbreviations

PAs:

Polyamines

PAO:

Polyamine oxidase

CuAO:

Copper-containing amine oxidase

FAD:

Flavin adenine dinucleotide

Put:

Putrescine

Spd:

Spermidine

Spm:

Spermine

ABAL:

4-Aminobutanal

Dap:

1,3-Diaminopropane

GABA:

4-Aminobutyrate

CsCuAO :

Citrus sinensis copper-containing amine oxidase

qPCR:

Real-time quantitative PCR detecting system

PCD:

Programmed cell death

PTSl:

Peroxisomal targeting signals

TPQ:

2,4,5-Trihydroxyphenylalanine quinone cofactor

References

  • Alcázar R, Altabella T, Marco F, Bortolotti C, Reymond M, Koncz C, Carrasco P, Tiburcio AF (2010) Polyamines molecules with regulatory functions in plant abiotic stress tolerance. Planta 231:1237–1249

    Article  PubMed  Google Scholar 

  • Alcázar R, Marco F, Cuevas JC, Patrón M, Ferrando A, Carrasco P, Tiburcio AF, Altabella T (2006) Involvement of polyamines in plant response to abiotic stress. Biotechnol Lett 28:1867–1876

    Article  PubMed  Google Scholar 

  • Angelini R, Cona A, Federico R, Fincato P, Tavladoraki P, Tisi A (2010) Plant amine oxidases ‘on the move’: an update. Plant Physiol Biochem 48:560–564

    Article  CAS  PubMed  Google Scholar 

  • An ZF, Jing W, Liu YL, Zhang WH (2008) Hydrogen peroxide generated by copper amine oxidase is involved in abscisic acid-induced stomatal closure in Vicia faba. J Exp Bot 59:815–825

    Article  CAS  PubMed  Google Scholar 

  • Bethke PC, Jones RL (2001) Cell death of barley aleurone protoplasts is mediated by reactive oxygen species. Plant J 25:19–29

    Article  CAS  PubMed  Google Scholar 

  • Campestrea MP, Bordenavea CD, Origonea AC, Menéndeza AB, Ruiza OA, Rodrígueza AA, Maiale SJ (2011) Polyamine catabolism is involved in response to salt stress in soybean hypocotyls. J Plant Physiol 168:1234–1240

    Article  Google Scholar 

  • Cona A, Rea G, Angelini R, Federico R, Tavladoraki P (2006) Functions of amine oxidases in plant development and defense. Trends Plant Sci 11:80–88

    Article  CAS  PubMed  Google Scholar 

  • Cuevas JC, Lopez-Cobollo R, Alcázar R, Zarza X, Koncz C, Altabella T, Salinas J, Tiburcio AF, Ferrando A (2008) Putrescine is involved in Arabidopsis freezing tolerance and cold acclimation by regulating abscisic acid levels in response to low temperature. Plant Physiol 148:1094–1105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cuevas JC, Lopez-Cobollo R, Alcazar R, Zarza X, Koncz C, Altabella T, Salinas J, Tiburcio AF, Ferrando A (2009) Putrescine as a signal to modulate the indispensable ABA increase under cold stress. Plant Signal Behav 4:219–220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Di Paolo ML, Lunelli M, Fuxreiter M, Rigo A, Simon I, Scarpa M (2011) Active site residue involvement in monoamine or diamine oxidation catalyzed by pea seedling amine oxidase. FEBS J 278:1232–1243

    Article  CAS  PubMed  Google Scholar 

  • Flores HE, Galston, AW (1982) Analysis of polyamines in higher plants by high performance liquid chromatography. Plant Physiol 69:701–706

  • Fu XZ, Chen CW, Wang Y, Liu JH, Moriguch T (2011) Ectopic expression of MdSPDS1 in sweet orange (Citrus sinensis Osbeck) reduces canker susceptibility: involvement of H2O2 production and transcriptional alteration. BMC Plant Biol 11:55

  • Groppa MD, Benavides MP (2008) Polyamines and abiotic stress: recent advances. Amino Acids 34:35–45

    Article  CAS  PubMed  Google Scholar 

  • Galston AW, Kaur-Sawhney R (1999) Polyamines in plant physiology. Plant Physiol 94:406–410

    Article  Google Scholar 

  • Ghuge SA, Carucci A, Rodrigues-Pousada RA, Tisi A, Franchi S, Tavladoraki P, Angelini R, Cona A (2015) The apoplastic copper amine oxidase1 mediates jasmonic acid-induced protoxylem differentiation in Arabidopsis roots. Plant Physiol 168:690–707

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hussain SS, Ali M, Ahmad M, Siddique KH (2011) Polyamines: natural and engineered abiotic and biotic stress tolerance in plants. Biotechnol Adv 29:300–311

    Article  CAS  PubMed  Google Scholar 

  • Jiménez-Bremont JF, Ruiz OA, Rodriguez-Kessler M (2007) Modulation of spermidine and spermine levels in maize seedlings subjected to long-term salt stress. Plant Physiol Biochem 45:812–821

    Article  PubMed  Google Scholar 

  • Kusano T, Berberich T, Tateda C, Takahashi Y (2008) Polyamines: essential factors for growth and survival. Planta 228:367–381

    Article  CAS  PubMed  Google Scholar 

  • Kinnersley AM, Turano FJ (2000) Gamma aminobutyric acid (GABA) and plant responses to stress. Crit Rev in Plant Sci 19:479–509

    Article  CAS  Google Scholar 

  • Liu JH, Nada K, Honda C, Kitashiba H, Wen XP, Pang XM, Moriguchi T (2006) Polyamine biosynthesis of apple callus under salt stress: importance of the arginine decarboxylase pathway in stress response. J Exp Bot 57:2589–2599

    Article  CAS  PubMed  Google Scholar 

  • Liu JH, Nakajima I, Morguchi T (2011) Effects of salt and osmotic stresses on free polyamine content and expression of polyamine biosynthetic genes in Vitis vinifera. Biol Plantarum 55:340–344

    Article  CAS  Google Scholar 

  • Liu JH, Wang W, Wu H, Gong XQ, Moriguchi T (2015) Polyamines function in stress tolerance: from synthesis to regulation. Front Plant Sci 6:827

    PubMed  PubMed Central  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Medda R, Padiglia A, Floris G (1995) Plant copper-amine oxidases. Phytochem 39:1–9

    Article  CAS  Google Scholar 

  • Miller G, Shulaev V, Mittler R (2008) Reactive oxygen signaling and abiotic stress. Physiol Plantarum 133:481–489

    Article  CAS  Google Scholar 

  • Minocha R, Majumdar R, Minocha SC (2014) Polyamines and abiotic stress in plants: a complex relationship. Front Plant Sci 5:175

    Article  PubMed  PubMed Central  Google Scholar 

  • Moore RC, Purugganan MD (2003) The early stages of duplicate gene evolution. Proc Nat Acad Sci USA 100:15682–15687

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moschou PN, Sanmartin M, Andriopoulou AH, Rojo E, Sanchez-Serrano JJ, Roubelakis-Angelakis KA (2008) Bridging the gap between plant and mammalian polyamine catabolism: a novel peroxisomal polyamine oxidase responsible for a full back-conversion pathway in Arabidopsis. Plant Physiol 147:1845–1857

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moschou PN, Wu J, Cona A, Tavladoraki P, Angelini R, Roubelakis-Angelakis KA (2012) The polyamines and their catabolic products are significant players in turnover of nitrogenous molecules in plants. J Exp Bot 63:5003–5015

    Article  CAS  PubMed  Google Scholar 

  • Møller SG, McPherson MJ (1998) Developmental expression and biochemical analysis of the Arabidopsis Atao1 gene encoding an H2O2-generating diamine oxidase. Plant J 13:781–791

    Article  PubMed  Google Scholar 

  • Murashige T, Tucker DPH (1969) Growth factor requirements of citrus tissue culture. Proc First Intl Citrus Symp 3:1155–1161

    CAS  Google Scholar 

  • Naconsie M, Kato K, Shoji T, Hashimoto T (2014) Molecular evolution of N-methylputrescine oxidase in tobacco. Plant Cell Physiol 55:436–444

    Article  CAS  PubMed  Google Scholar 

  • Neill S, Desikan R, Hancock J (2002) Hydrogen peroxide signaling. Curr Opin Plant Biol 5:388–395

    Article  CAS  PubMed  Google Scholar 

  • Planas-Portell J, Gallart M, Tiburcio AF, Altabella T (2013) Copper-containing amine oxidases contribute to terminal polyamine oxidation in peroxisomes and apoplast of Arabidopsis thaliana. BMC Plant Biol 13:109

    Article  PubMed  PubMed Central  Google Scholar 

  • Pietrangeli P, Federico R, Mondovì B, Morpurgo L (2007) Substrate specificity of copper-containing plant amine oxidases. J Inorg Biochem 101:997–1004

    Article  CAS  PubMed  Google Scholar 

  • Rodríguez-Kessler M, Alpuche-Solís AG, Ruiz OA, Jiménez-Bremont JF (2006) Effect of salt stress on the regulation of maize (Zea mays L.) genes involved in polyamine biosynthesis. Plant Growth Regul 48:175–185

    Article  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Seiler N (2004) Catabolism of polyamines. Amino Acids 26:217–233

    CAS  PubMed  Google Scholar 

  • Shelp BJ, Bozzo GG, Trobacher CP, Zarei A, Deyman KL, Brikis CJ (2012a) Hypothesis/review: contribution of putrescine to ɤ-aminobutyrate (GABA) production in response to abiotic stress. Plant Sci 193(194):130–135

    Article  PubMed  Google Scholar 

  • Shelp BJ, Bozzo GG, Trobacher CP, Chiu G, Bajwa VS (2012b) Strategies and tools for studying the metabolism and function of ɤ-aminobutyrate in plants. Botany 90:651–668

    Article  CAS  Google Scholar 

  • Shi H, Chan Z (2014) Improvement of plant abiotic stress tolerance through modulation of the polyamine pathway. J Intg Plant Biol 56:114–121

    Article  CAS  Google Scholar 

  • Swamy PM, Smith B (1999) Role of abscisic acid in plant stress tolerance. Curr Sci 76:1220–1227

    CAS  Google Scholar 

  • Tavladoraki P, Rossi MN, Saccuti G, Perez-Amador MA, Polticelli F, Angelini R, Federico R (2006) Heterologous expression and biochemical characterization of a polyamine oxidase from Arabidopsis involved in polyamine back conversion. Plant Physiol 141:1519–1532

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tipping AJ, McPherson MJ (1995) Cloning and molecular analysis of the pea seeding copper amine oxidase. J Biol Chem 270:16939–16946

    Article  CAS  PubMed  Google Scholar 

  • Tiburcio AF, Altabella T, Bitrián M, Alcázar R (2014) The roles of polyamines during the lifespan of plants: from development to stress. Planta 24:1–18

    Article  Google Scholar 

  • Urano K, Yoshiba Y, Nanjo T, Igarashi Y, Seki M, Sekiguchi F, Yamaguchi-Shinozaki K, Shinozaki K (2003) Characterization of Arabidopsis genes involved in biosynthesis of polyamines in abiotic stress responses and developmental stages. Plant Cell Environ 26:1917–1926

    Article  CAS  Google Scholar 

  • Voinnet O, Rivas S, Mestre P, Baulcombe D (2003) An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J 33:949–956

    Article  CAS  PubMed  Google Scholar 

  • Wang W, Liu JH (2015) Genome-wide identification and expression analysis of the polyamine oxidase gene family in sweet orange (Citrus sinensis). Gene 555:421–429

    Article  CAS  PubMed  Google Scholar 

  • Wang J, Sun PP, Chen CL, Wang Y, Fu XZ, Liu JH (2011) An arginine decarboxylase gene PtADC from Poncirus trifoliata confers abiotic stress tolerance and promotes primary root growth in Arabidopsis. J Exp Bot 62:2899–2914

  • Wimalasekera R, Villar C, Beguma T, Scherer GF (2011) Cooper amine oxidase1 (CuAO1) of Arabidopsis thaliana contributes to abscisic acid and polyamine-induced nitric oxide biosynthesis and abscisic acid signal transduction. Mol Plant 4:663–678

    Article  CAS  PubMed  Google Scholar 

  • Xu Q, Chen LL, Ruan XA, Chen DJ, Zhu AD, Chen CL, Bertrand D, Jiao WB, Hao BH, Lyon MP et al (2013) The draft genome of sweet orange (Citrus sinensis). Nat Genet 45:59–66

    Article  CAS  PubMed  Google Scholar 

  • Yan J, Tsuichihara N, Etoh T, Iwai S (2007) Reactive oxygen species and nitric oxide are involved in ABA inhibition of stomatal opening. Plant Cell Environ 30:1320–1325

    Article  CAS  PubMed  Google Scholar 

  • Yan JW, Yuan FR, Long GY, Qin L, Deng ZN (2012) Selection of reference genes for quantitative real-time RT-PCR analysis in citrus. Mol Biol Rep 39:1831–1838

    Article  CAS  PubMed  Google Scholar 

  • Zarei A, Trobacher CP, Cooke AR, Meyers AJ, Hall JC, Shelp BJ (2015) Apple fruit copper amine oxidase isoforms: peroxisomal MdAO1 prefers diamines as substrates whereas extracellular MdAO2 exclusively utilizes monoamines. Plant Cell Physiol 56:137–147

    Article  CAS  PubMed  Google Scholar 

  • Zhang QH, Wang M, Hu JB, Wang W, Fu XZ, Liu JH (2015) PtrABF of Poncirus trifoliata functions in dehydration tolerance by reducing stomatal density and maintaining reactive oxygen species homeostasis. J Exp Bot 66:5911–5927

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (31320103908) and the Ministry of Agriculture.

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Authors and Affiliations

  1. Key Laboratory of Horticultural Plant Biology, College of Horticulture and Forestry Sciences, Huazhong Agricultural University, Wuhan, 430070, China

    Wei Wang, Hao Wu & Ji-Hong Liu

  2. College of Horticulture, Henan Agricultural University, Zhengzhou, 450002, China

    Wei Wang

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  1. Wei Wang
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  2. Hao Wu
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Correspondence to Ji-Hong Liu.

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The authors declare that they have no competing interests.

Data archiving statement

All identified amino acid of CuAO gene sequences were deposited into the NCBI database (http://www.ncbi.nlm.nih.gov/). The accession numbers are listed in Supplemental Table 2.

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Communicated by C. Dardick

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Wang, W., Wu, H. & Liu, JH. Genome-wide identification and expression profiling of copper-containing amine oxidase genes in sweet orange (Citrus sinensis). Tree Genetics & Genomes 13, 31 (2017). https://doi.org/10.1007/s11295-017-1102-7

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