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Expression of ethylene biosynthetic genes during flower senescence and in response to ethephon and silver nitrate treatments in Osmanthus fragrans

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Abstract

Background

Sweet osmanthus (Osmanthus fragrans) is an ornamental evergreen tree species in China, whose flowers are sensitive to ethylene. The synthesis of ethylene is controlled by key enzymes and restriction enzymes, 1-aminocyclopropane-1-carboxylic acid synthase (ACS) and 1-aminocyclopropane-1-carboxylic acid oxidase (ACO), which are encoded by multigene families. However, the key synthase responsible for ethylene regulation in O. fragrans is still unknown.

Objective

This study aims to screen the key ethylene synthase genes of sweet osmanthus flowers in response to ethylene regulation.

Methods

In this study, we used the ACO and ACS sequences of Arabidopsis thaliana to search for homologous genes in the O. fragrans petal transcriptome database. These genes were also analyzed bioinformatically. Finally, the expression levels of O. fragrans were compared before and after senescence, as well as after ethephon and silver nitrate treatments.

Results

The results showed that there are five ACO genes and one ACS gene in O. fragrans transcriptome database, and the phylogenetic tree revealed that the proteins encoded by these genes had high homology to the ACS and ACO proteins in plants. Sequence alignment shows that the OfACO1-5 proteins have the 2OG-Fe(II) oxygenase domain, while OfACS1 contains seven conserved domains, as well as conserved amino acids in transaminases and glutamate residues related to substrate specificity. Expression analysis revealed that the expression levels of OfACS1 and OfACO1-5 were significantly higher at the early senescence stage compared to the full flowering stage. The transcripts of the OfACS1, OfACO2, and OfACO5 genes were upregulated by treatment with ethephon. However, out of these three genes, only OfACO2 was significantly downregulated by treatment with AgNO3.

Conclusion

Our study found that OfACO2 is an important synthase gene in response to ethylene regulation in sweet osmanthus, which would provide valuable data for further investigation into the mechanisms of ethylene-induced senescence in sweet osmanthus flowers.

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References

  • Adams DO, Yang SF (1979) Ethylene biosynthesis: identification of 1-aminocyclopropane-1-carboxylic acid as an intermediate in the conversion of methionine to ethylene. PNAS 76:170–174

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baharudin NF, Osman NI (2023) Plant development, stress responses and secondary metabolism under ethylene regulation. Plant Stress 7:100146

    Article  CAS  Google Scholar 

  • Barry CS, Grierson D, Llop-Tous MI (2000) The regulation of 1-aminocyclopropane-1-carboxylic acid synthase gene expression during the transition from system-1 to system-2 ethylene synthesis in tomato. Plant Physiol 123:979–986

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bidonde S, Ferrer MA, Zegzouti H, Ramassamy S, Latche A, Pech JC, Hamilton AJ, Grierson D, Bouzayen M (1998) Expression and characterization of three tomato 1-aminocyclopropane-1-carboxylate oxidase cDNAs in yeast. Eur J Biochem 253:20–26

    Article  CAS  PubMed  Google Scholar 

  • Binder BM (2020) Ethylene signaling in plants. J Biol Chem 295:7710–7725

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Briesemeister S, Rahnenführer J, Kohlbacher O (2010) YLoc—an interpretable web server for predicting subcellular localization. NAR 38:W497–502

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen H, Zeng X, Yang J, Cai X, Shi Y, Zheng R, Wang Z, Liu J, Yi X, Xiao S et al (2021) Whole-genome resequencing of Osmanthus fragrans provides insights into flower color evolution. Hortic Res 8:98

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng Z, Guangwen Z (2000) Physiological and biochemical changes in flower senescence of Osmanthus fragrans Lour. Acta Horticulturae Sinica 27:356–360

    Google Scholar 

  • Ding W, Ouyang Q, Li Y, Shi T, Li L, Yang X, Ji K, Wang L, Yue Y (2020) Genome-wide investigation of WRKY transcription factors in sweet osmanthus and their potential regulation of aroma synthesis. Tree Physiol 40:557–572

    Article  CAS  PubMed  Google Scholar 

  • Doan A, Ylmaz G, Erkan M, Baktr I (2013) Effects of sucrose and silver nitrate on the vase life of cut Ranunculus asiaticus L. Acta Hort 1002:341–348

    Google Scholar 

  • Hayashi T, Teruya T, Chaleckis R, Morigasaki S, Yanagida M (2018) S-adenosylmethionine synthetase is required for cell growth, maintenance of G0 phase, and termination of quiescence in fission yeast. Iscience 5:38–51

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Houben M, Van de Poel B (2019) 1-Aminocyclopropane-1-carboxylic acid oxidase (ACO): the enzyme that makes the plant hormone ethylene. Front Plant Sci 10:695

    Article  PubMed  PubMed Central  Google Scholar 

  • Husain T, Fatima A, Suhel M, Singh S, Sharma A, Prasad SM, Singh VP (2020) A brief appraisal of ethylene signaling under abiotic stress in plants. Plant Signal Behav 15:1782051

    Article  PubMed  PubMed Central  Google Scholar 

  • Imsabai W, Ketsa S, van Doorn WG (2010) Role of ethylene in the lack of floral opening and in petal blackening of cut lotus (Nelumbo nucifera) flowers. Postharvest Biol Tec 58:57–64

    Article  CAS  Google Scholar 

  • Iqbal N, Khan NA, Ferrante A, Trivellini A, Francini A, Khan M (2017) Ethylene role in plant growth, development and senescence: interaction with other phytohormones. Front Plant Sci 8:475

    Article  PubMed  PubMed Central  Google Scholar 

  • Jian G, Dong, Woo T, Kim W, Yip K (1991) Cloning of a cDNA encoding 1-aminocyclopropane-1-carboxylate synthase and expression of its mRNA in ripening apple fruit. Planta 185:38–45

    Article  CAS  PubMed  Google Scholar 

  • John P (1991) How plant molecular biologists revealed a surprising relationship between two enzymes, which took an enzyme out of a membrane where it was not located, and put it into the soluble phase where it could be studied. Plant Mol Biol 9:192–194

    Article  Google Scholar 

  • Kanojia A, Xu X, Dijkwel PP (2023) Ethylene as a plant aging modulator, 6th edn. Academic Press, Cambridge, pp 73–87

    Google Scholar 

  • Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lacey RF, Binder BM (2014) How plants sense ethylene gas — the ethylene receptors. J Inorg Biochem 133:58–62

    Article  CAS  PubMed  Google Scholar 

  • Lee HY, Chen YC, Kieber JJ, Yoon GM (2017) Regulation of the turnover of ACC synthases by phytohormones and heterodimerization in Arabidopsis. Plant J 91:491–504

    Article  CAS  PubMed  Google Scholar 

  • Liu CY, Lu RH, Li J, Zhao AC, Wang XL, Diane U, Wang XH, Wang CH, Yu YS, Han SM et al (2014) Characterization and expression profiles of MaACS and MaACO genes from mulberry (Morus alba L). J Zhejiang Univ Sci B 15:611–623

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma N, Cai L, Lu W, Tan H, Gao J (2005) Exogenous ethylene influences flower opening of cut roses (Rosa hybrida) by regulating the genes encoding ethylene biosynthesis enzymes. Sci China C Life Sci 48:434–444

    Article  CAS  PubMed  Google Scholar 

  • Marić S, Lukić M, Flachowsky H (2014) Allelic polymorphism and inheritance of MdACS1 and MdACO1 genes in apple (Malus × domestica Borkh). Plant Breeding 133:108–114

    Article  Google Scholar 

  • Mirica LM, Klinman JP (2008) The nature of O2 activation by the ethylene-forming enzyme 1-aminocyclopropane-1-carboxylic acid oxidase. Proc Natl Acad Sci U S A 105:1814–1819

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Momonoi K, Shoji K, Yoshida K (2007) Cloning and characterization of ACC oxidase genes from tulip. Plant Biotechnol 24:241–246

    Article  CAS  Google Scholar 

  • Moon J, Park YJ, Son SH, Roh J, Youn JH, Kim SY, Kim SK (2020) Brassinosteroids signaling via BZR1 down-regulates expression of ACC oxidase 4 to control growth of Arabidopsis thaliana seedlings. Plant Signal Behav 15:1734333

    Article  PubMed  PubMed Central  Google Scholar 

  • Nair SA, Singh V, Sharma T (2003) Effect of chemical preservatives on enhancing vase-life of gerbera flowers. J Trop Agric 41:56–58

    CAS  Google Scholar 

  • Norikoshi R, Niki T, Ichimura K (2022) Differential regulation of two 1-aminocyclopropane-1-carboxylate oxidase (ACO) genes, including the additionally cloned DcACO2, during senescence in carnation flowers. Postharvest Biol Tec 183:111752

    Article  CAS  Google Scholar 

  • Park CH, Roh J, Youn JH, Son SH, Kim SK (2018) Arabidopsis ACC oxidase 1 coordinated by multiple signals mediates ethylene biosynthesis and is involved in root development. Mol Cells 41:923–932

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pattyn J, Vaughan-Hirsch J, Van de Poel B (2021) The regulation of ethylene biosynthesis: a complex multilevel control circuitry. New Phytol 229:770–782

    Article  CAS  PubMed  Google Scholar 

  • Poel B, Straeten D (2014) 1-Aminocyclopropane-1-carboxylic acid (ACC) in plants: more than just theprecursor of ethylene. Front Plant Sci 5:640

    PubMed  PubMed Central  Google Scholar 

  • Polko JK, Kieber JJ (2019) 1-Aminocyclopropane 1-carboxylic acid and its emerging role as an ethylene-independent growth regulator. Front Plant Sci 10:1602

    Article  PubMed  PubMed Central  Google Scholar 

  • Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C, Pang N, Forslund K, Ceric G, Clements J (2004) The pfam protein families database. Nucleic Acids Res 32:D138–D141

    Article  Google Scholar 

  • Reid MS, Fujino DW, Hoffman NE, Whitehead CS (1984) 1-Aminocyclopropane-l-carboxylic acid (ACC)—the transmitted stimulus in pollinated flowers? J Plant Growth Regul 3:189–196

    Article  CAS  Google Scholar 

  • Rottmann WH, Peter GF, Oeller PW, Keller JA, Shen NF, Nagy BP, Taylor LP, Campbell AD, Theologis A (1991) 1-Aminocyclopropane-1-carboxylate synthase in tomato is encoded by a multigene family whose transcription is induced during fruit and floral senescence. J Mol Biol 222:937–961

    Article  CAS  PubMed  Google Scholar 

  • Ruduś I, Sasiak M, Kępczyński J (2012) Regulation of ethylene biosynthesis at the level of 1-aminocyclopropane-1-carboxylate oxidase (ACO) gene. Acta Physiol Plant 35:295–307

    Article  Google Scholar 

  • Sato T, Theologis A (1989) Cloning the mRNA encoding 1-aminocyclopropane-1-carboxylate synthase, the key enzyme for ethylene biosynthesis in plants. PNAS 86:6621–6625

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sebastià CH, Hardin SC, Clouse SD, Kieber JJ, Huber SC (2004) Identification of a new motif for CDPK phosphorylation in vitro that suggests ACC synthase may be a CDPK substrate. Arch Biochem Biophys 428:81–91

    Article  Google Scholar 

  • Shi LS, Liu JP (2016) Molecular cloning and expression analysis of an 1-aminocyclopropane-1-carboxylate synthase gene from Oncidium Gower Ramsey. Biochem Bioph Res Co 469:203–209

    Article  CAS  Google Scholar 

  • Shibuya K, Yoshioka T, Hashiba T, Sato S (2000) Role of the gynoecium in natural senescence of carnation (Dianthus caryophyllus L.) flowers. J Exp Bot 51:2067–2073

    Article  CAS  PubMed  Google Scholar 

  • Tanase K, Otsu S, Satoh S, Onozaki T (2013) Expression and Regulation of Senescence-related Genes in Carnation Flowers with Low Ethylene Production during Senescence. J Jpn Soc Hort Sci 82(2):179–187

    Article  CAS  Google Scholar 

  • Tang X, Gomes AMTR, Woodson BWR (1994) Pistil-specific and ethylene-regulated expression of 1-aminocyclopropane-1-carboxylate oxidase genes in petunia flowers. Plant Cell 6:1227–1239

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tatsuki M (2001) Phosphorylation of tomato 1-aminocyclopropane-1-carboxylic acid synthase, LE-ACS2, at the C-terminal region. J Biol Chem 276:28051–28057

    Article  CAS  PubMed  Google Scholar 

  • Thanomchit K, Imsabai W, Burns P, McAtee PA, Schaffer RJ, Allan AC, Ketsa S (2022) Differential expression of ethylene biosynthetic and receptor genes in pollination-induced senescence of Dendrobium florets. Plant Physiol Bioch 188:38–46

    Article  CAS  Google Scholar 

  • Wang KL, Li H, Ecker JR (2002) Ethylene biosynthesis and signaling networks. Plant Cell 14:S131–S151

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wei H, Xue Y, Chen P, Yang Y (2021) Genome-wide identification and functional investigation of 1-aminocyclopropane-1-carboxylic acid oxidase (ACO) genes in cotton. Plants 10:1699

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu L, Liu J, Huang W, Wang Y, Chen Q, Lu B (2022) Exploration of Osmanthus fragrans Lour.‘s composition, nutraceutical functions and applications. Food Chem 377:131853

    Article  CAS  PubMed  Google Scholar 

  • Xiaoyan T, Cuiping Y, Jin H, Bingyu Y, Xiaoxiao G, Yufen Z, Yingwen P, Jinping L (2015) Cloning and expression analysis of OnACO2 gene from Oncidium Gower Ramsey. Mol Plant Breed 13:1602–1610

    Google Scholar 

  • Yang H (1984) Ethylene biosynthesis and its regulation in higher plants. Annu Rev Plant Phys 35:89–155

    Article  Google Scholar 

  • Yin J, Chang X, Kasuga T, Bui M, Reid MS, Jiang CZ (2015) A basic helix-loop-helix transcription factor, PhFBH4, regulates flower senescence by modulating ethylene biosynthesis pathway in petunia. Hortic Res 2:15059

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang C, Wang Y, Fu J, Bao Z, Zhao H (2016) Transcriptomic analysis and carotenogenic gene expression related to petal coloration in Osmanthus fragrans ‘Yanhong Gui.’ Trees 30:1207–1223

    Article  CAS  Google Scholar 

  • Zhao D, Tao J, Zhou C, Wang S (2014) Expression, cloning and characterization of ACC synthase and ACC oxidase genes in Paeonia lactiflora. Int J Agric Biol 16:777–782

    CAS  Google Scholar 

  • Zhou Y, Wang CY, Cheng ZW (2008) Effects of exogenous ethylene and ethylene inhibitor on longevity and peatal senescence of sweet osmanthus. Acta Hort 768:487–493

    Article  CAS  Google Scholar 

  • Zhou L, Jia PY, Liu J, Wang WR, Dong L (2009) Effect of ethylene on cut flowers of tree peony ‘Luoyang Hong’ opening and senescence process and endogenous ethylene biosynthesis. Acta Hortic Sin 36:239–244

    CAS  Google Scholar 

  • Zou J-j, Zhou Y, Cai X, Wang C-y (2014) Increase in DNA fragmentation and the role of ethylene and reactive oxygen species in petal senescence of Osmanthus fragrans. Postharvest Biol Tec 93:97–105

    Article  CAS  Google Scholar 

  • Zou J, Cai X, Wang C (2017) The spatial and temporal distribution of programmed cell death (PCD) during petal senescence of Osmanthus fragrans. Acta Hortic 1185:315–324

    Article  Google Scholar 

  • Zou J-J, Cai X, Yang J, Zeng X, Liu D-X, Huang S, Chen X, Yang Q-Y, Wang C, Chen H (2023) DNA hypomethylation mediates flower opening and senescence in sweet osmanthus through auxin and ethylene responsive pathways. Postharvest Biol Tec 198:112250

    Article  CAS  Google Scholar 

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Funding

This work was supported by Zhejiang Provincial Natural Science Foundation of China (Grant Nos. LY19C160002), and the Open Fund of Zhejiang Provincial Key Laboratory of Germplasm Innovation and Utilization for Garden Plants.

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Authors and Affiliations

  1. Zhejiang Provincial Key Laboratory of Germplasm Innovation and Utilization for Garden Plants, College of Landscape and Architecture, Zhejiang Agriculture and Forestry University, Hangzhou, 311300, Zhejiang, China

    Hui Qiu, Yiwen Chen, Jianxin Fu & Chao Zhang

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  1. Hui Qiu
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  2. Yiwen Chen
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  3. Jianxin Fu
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  4. Chao Zhang
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Contributions

CZ and JF conceived the project and designed the experiments. HQ and YC collected datasets and performed the bioinformatics analysis and expression analysis. HQ, CZ and JF wrote and revised the manuscript. All authors read and approved the final manuscript.

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Correspondence to Jianxin Fu or Chao Zhang.

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Qiu, H., Chen, Y., Fu, J. et al. Expression of ethylene biosynthetic genes during flower senescence and in response to ethephon and silver nitrate treatments in Osmanthus fragrans. Genes Genom 46, 399–408 (2024). https://doi.org/10.1007/s13258-023-01489-0

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