Advances in the study of senescence mechanisms in the genus Paeonia

Abstract

Tree and herbaceous peony are considerably important ornamental plants within the genus Paeonia, and hold substantial horticultural value. This review summarizes the progress in research on the senescence mechanisms of tree and herbaceous peony flowers, focusing on the regulation of gene expression, hormonal interactions, and the influence of environmental factors on senescence. Using high-throughput sequencing technologies, key genes displaying differential expression during senescence have been identified, and these play central roles in hormone signaling and cellular senescence. The interactions among plant hormones, including ethylene, abscisic acid, gibberellins, cytokinins, and auxins, also play key roles in the regulation of senescence. Adjustments in antioxidant levels, as well as water and energy metabolism, are critical factors in the delay of senescence. Environmental factors, including light, temperature, drought, and salt stress, also significantly affect senescence. Additionally, this review proposes future research directions, including the expansion of the molecular regulatory network of senescence in Paeonia, the use of gene editing technologies like CRISPR/Cas9, multiomics studies, and exploratory comparative research on spatial biology senescence mechanisms. These studies aim to deepen our understanding of the molecular mechanisms that underlie senescence in Paeonia and provide a scientific basis for cultivar improvement and postharvest management of these ornamental commodities in the horticultural industry.

Acknowledgments

This work was financially supported by the National Natural Science Foundation of China (32071817). We extend our heartfelt gratitude to Ms. An Chen, Mr. Jianli Wang, Ms. Huanzhi Song, Mr. Xinqi Xu, Ms. Kaiyue Liu, and Ms. Chunyan Wu for their invaluable assistance in the preparation of this manuscript.

Author Contributions

Y.W. and W.Z. developed the structure of the review article. Y.W. and M.S. was responsible for gathering the necessary literature and drafting the initial manuscript. Y.W. and L.C. meticulously assembled this initial draft. Y.W., S.Z., J.A.T., and J.Z. was in charge of organizing the tables, figure, and refining the citations. X.Y., J.A.T., Y.W., and M.S. provided multiple critical revisions and enhancements to the manuscript. All authors contributed to the article and approved the submitted version.

Conflict of interest statement

No potential conflicts of interest were reported by the authors.

Supplementary data

Supplementary data is available at Horticulture Research online.

References

[1] Yu XN. Ornamental Peony. Beijing: China Forestry Publishing House; 2019: (in Chinese)

[2] Li JY. Chinese Tree Peonies and Herbaceous Peonies. China Forestry Publishing House; 1996: (in Chinese)

[3] Tian Y, Wang XNL. Let the "national flower peony" bloom more vigorously and brilliantly. Henan Daily (Nat Sci). 2023;008. (in Chinese)

[4] Wang YX, Yu XN. The glory of herbaceous peony—the revival and opportunities of traditional famous flowers. China Flowers & Horticulture (Nat Sci). 2024;2:36-9 (in Chinese)

[5] Kamenetsky-Goldstein R, Yu X. Cut peony industry: the first 30 years of research and new horizons. Hortic Res. 2022;9:uhac079

[6] Teixeira da Silva JA. The cut flower: postharvest considerations. Online J Biol Sci. 2003;3: 406-42

[7] Sade N, Del Mar R-WM, Umnajkitikorn K. et al. Stress-induced senescence and plant tolerance to abiotic stress. JExp Bot. 2018;69: 845-53

[8] Ay N, Janack B, Humbeck K. Epigenetic control of plant senes-cence and linked processes. JExp Bot. 2014;65: 3875-87

[9] Feng S, Jiang X, Huang Z. et al. DNA methylation remodeled amino acids biosynthesis regulates flower senescence in carna-tion (Dianthus caryophyllus). New Phytol. 2024;241: 1605-20

[10] Feng S, Jiang X, Wang R. et al. Histone H3K4 methyltransferase DcATX1 promotes ethylene induced petal senescence in carna-tion. Plant Physiol. 2023;192: 546-64

[11] Chen WH, Lin PT, Hsu WH. et al. Regulatory network for FOR-EVER YOUNG FLOWER-like genes in regulating Arabidopsis FLOWER senescence and abscission. Commun Biol. 2022;5:662

[12] Cheng SLH, Xu H, Ng JHT. et al. Systemic movement of long non-coding RNA ELENA1 attenuates leaf senescence under nitrogen deficiency. Nat Plants. 2023;9: 1598-606

[13] Holme IB, Ingvardsen CR, Dionisio G. et al. CRISPR/Cas9-mediated mutation of Eil1 transcription factor genes affects exogenous ethylene tolerance and early flower senescence in campanula portenschlagiana. Plant Biotechnol J. 2024;22: 484-96

[14] Guo L, Li Y, Zhang C. et al. Integrated analysis of miRNAome tran-scriptome and degradome reveals miRNA-target modules gov-erning floral florescence development and senescence across early- and late-flowering genotypes in tree peony. Front Plant Sci. 2022;13:1082415

[15] Ji XT, Yuan YP, Bai ZZ. et al. PlZFP mediates the combinatorial interactions of abscisic acid with gibberellin and ethylene during flower senescence in cut herbaceous peony. Postharvest Biol Technol. 2023;195:112130.

[16] Zhou L, Dong L, Jia PY. et al. Expression of ethylene receptor and transcription factor genes, and ethylene response during flower opening in tree peony (Paeonia suffruticosa). Plant Growth Reg. 2010;62: 171-9

[17] Zu MT, Qiu SY, Qian Y. et al. Transcriptome sequencing pro-vides insights into high-temperature-induced leaf senescence in herbaceous peony. Agriculture. 2024;14:547

[18] Locato V, De Gara L. Programmed cell death in plants: an overview. Methods Mol Biol. 2018;1743: 1-8

[19] van Doorn WG, Woltering EJ. Physiology and molecular biology of petal senescence. JExp Bot. 2008;59: 453-80

[20] Xu L, Sun M, Teixeira da Silva JA. et al. Assessment of pro-grammed cell death in aging Paeonia lactiflora petals. Cytologia. 2023;88: 151-9

[21] Tong N, Shu Q, Wang B. et al. Histology, physiology, and tran-scriptomic and metabolomic profiling reveal the developmental dynamics of annual shoots in tree peonies (Paeonia suffruticosa Andr.). Hortic Res. 2023;10:uhad152.

[22] Shi GA, Guo XF, Zhang GH. et al. Changes in physiological indi-cators during the opening and senescence of herbaceous peony flowers. Acta Bot Boreali-Occidentalia Sin (Nat Sci). 2008;3:506-11 (in Chinese)

[23] Hui GJ, Zheng GS, Zhang W. et al. Effects of pre-harvest calcium spray on the physiological and biochemical characteristics of herbaceous peony cut flowers. Acta Bot Boreali-Occidentalia Sin (Nat Sci). 2009;29:1246-51 (in Chinese)

[24] Wang X. Effects of Pre-Harvest Spraying of Calcium and Bud Removal Interactions on the Quality of Cut Peonies(MSc thesis). Beijing: Chi-nese Academy of Forestry Sciences; 2016: (in Chinese)

[25] Zhao D, Luan Y, Shi W. et al. Melatonin enhances stem strength by increasing lignin content and secondary cell wall thickness in herbaceous peony. JExp Bot. 2022;73: 5974-91

[26] Wang YX, Liu XF, Sun M. et al. Melatonin enhances vase life and alters physiological responses in peony (Paeonia lactiflora Pall.) cut flowers. Postharvest Biol Technol. 2024;212:112896.

[27] Apel K, Hirt H. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol. 2004;55: 373-99

[28] LiuD XuS,HuH. et al. Endogenous hydrogen sulfide homeosta-sis is responsible for the alleviation of senescence of postharvest daylily flower via increasing antioxidant capacity and main-tained energy status. J Agric Food Chem. 2017b;65: 718-26

[29] Wang Z, Liu X, Wang J. et al. Effect of flowering stages on the content of active ingredients and antioxidant capability of Bletilla striata flowers. Chem Biodivers. 2023;20:e202200773.

[30] Geng XM, Liu J, Lu JG. et al. Effects of cold storage and different pulsing treatments on postharvest quality of cut OT lily ’Man-tissa’ flowers. J Fac Agric - Kyushu Univ. 2009;54: 41-5

[31] Shi J, Shi G, Tian Z. Effect of exogenous hydrogen peroxide or ascorbic acid on senescence in cut flowers of tree peony (Paeonia suffruticosa Andr.). J Hortic Sci Biotechnol. 2015;90: 689-94

[32] Ma Z, Zhang K, Guo W. et al. Green synthesis of silver nanoparticles using Eucommia ulmoides leaf extract for inhibiting stem end bacteria in cut tree peony flowers. Front Plant Sci. 2023;14:1176359

[33] Zhang Y, Xu YF, Shang WQ. et al. ClO2 treatment delays petal senescence and extends the vase life of Paeonia suffruticosa ’Luoyang Hong’ cut flowers. Sci Hortic. 2024;325:112650.

[34] Song J, Li Y, Hu J. et al. Pre- and/or postharvest silicon application prolongs the vase life and enhances the quality of cut peony (Paeonia lactiflora Pall.) flowers. Plan Theory. 2021;10:1742

[35] Song J, Yang J, Jeong BR. Synergistic effects of silicon and preservative on promoting postharvest performance of cut flowers of peony (Paeonia lactiflora Pall.). Int J Mol Sci. 2022;23: 13211

[36] Zhao D, Cheng M, Tang W. et al. Nano-silver modifies the vase life of cut herbaceous peony (Paeonia lactiflora Pall.) flowers. Protoplasma. 2018;255: 1001-13

[37] Li PY, Zhang WM, Tao J. et al. Herbaceous peony polyphenols extend the vase life of cut flowers. Agriculture. 2023b;13:122

[38] Guo YZ, Qiu YJ, Hu H. et al. Petal morphology is correlated with floral longevity in Paeonia suffruticosa. Agriculture. 2024;13:1372

[39] Bresson J, Bieker S, Riester L. et al. A guideline for leaf senescence analyses: from quantification to physiological and molecular investigations. JExp Bot. 2018;69: 769-86

[40] Taiz L, Zeiger E. Plant Physiology. 5th ed. Sunderland, MA: Sinauer Associates; 2010:

[41] Domínguez F, Cejudo FJ. Chloroplast dismantling in leaf senes-cence. JExp Bot. 2021;72: 5905-18

[42] Shi GA. Physiological and Biochemical Mechanisms of Peony Flowering and Senescence(PhD dissertation). Huazhong: Huazhong Agricul-tural University; 2010: (in Chinese)

[43] Han CJ, Wang Q, Zhang HB. et al. Light shading improves the yield and quality of seed in oil-seed peony (Paeonia ostii Feng Dan). J Integrative Agric. 2018;17: 1631-40

[44] Han C, Yu M, Wang Q. et al. Leaf structure and seed histochem-istry analyses provided structural insights into the improved yield and quality of tree peony seed under light shading con-ditions. Sci Rep. 2020;10:4328

[45] Zhao D, Luan Y, Shi W. et al. A Paeonia ostii caffeoyl-CoA O-methyltransferase confers drought stress tolerance by promoting lignin synthesis and ROS scavenging. Plant Sci. 2021;303:110765.

[46] Xie A, Lv M, Zhang D. et al. Effects of slight shading in summer on the leaf senescence and endogenous hormone and polyamine contents in herbaceous peony. Sci Rep. 2023;13:18714

[47] Wang Z, Shi GA, Ma XQ. et al. Ethylene metabolism and phys-iological mechanisms during the flowering and senescence of herbaceous peony ’Tao Hua Fei Xue’. Acta Hortic Sin (Nat Sci). 2014a;41:2268-74 (in Chinese)

[48] Han L. Study on the Mechanism of Low Temperature and Polyamines Affecting Postharvest Aging of Cut Peonies(MSc Thesis). Shandong: Shandong Agricultural University; 2016: (in Chinese)

[49] Rabiza- ´Swider J, Skutnik E, Je˛drzejuk A. et al. Postharvest treatments improve quality of cut peony flowers. Agronomy. 2020;10:1583

[50] Xue JQ, Tang Y, Wang SL. et al. Assessment of vase quality and transcriptional regulation of sucrose transporter and inver-tase genes in cut peony (Paeonia lactiflora ’Yang Fei Chu Yu’) treated by exogenous sucrose. Postharvest Biol Technol. 2018;143: 92-101

[51] Sun J, Guo HX, Tao J. Effects of harvest stage, storage, and preservation technology on postharvest ornamental value of cut peony (Paeonia lactiflora) flowers. Agriculture. 2022;12: 230

[52] Zhang C, Liu M, Fu JX. et al. Exogenous sugars involve-ment in senescence and ethylene production of tree peony ’Luoyang Hong’ cut flowers. Korean J Hortic Sci Technol. 2013;30: 718-24

[53] Wang W. Physiological Roles of ABA, H2O2, and Ethylene in the Senescence of Herbaceous Peony Cut Flowers. (MSc thesis). Henan: Henan University of Science and Technology; 2013: (in Chinese).

[54] van Doorn WG. Is petal senescence due to sugar starvation? Plant Physiol. 2004;134: 35-42

[55] Skutnik E, Rabiza-Swider J, Jedrzejuk A. et al. The effect of the long-term cold storage and preservatives on senescence of cut herbaceous peony flowers. Agriculture. 2020;10:1631

[56] Zhang C, Wang Y, Fu J. et al. Transcriptomic analysis of cut tree peony with glucose supply using the RNA-Seq technique. Plant Cell Rep. 2014;33: 111-29

[57] Xue JQ, Tang Y, Wang SL. et al. Evaluation of dry and wet storage on vase quality of cut peony based on the regulation of starch and sucrose metabolism. Postharvest Biol Technol. 2019; 155:11-9

[58] Ma N, Ma C, Liu Y. et al. Petal senescence: a hormone view. JExp Bot. 2018;69: 719-32

[59] Sun X, Qin M, Yu Q. et al. Molecular understanding of postharvest flower opening and senescence. Mol Hortic. 2021;1:7

[60] Wang YJ, Zhang C, Jia PY. et al. Isolation and expression analysis of three EIN3-like genes in tree peony (Paeonia suffruticosa). Plant Cell Tissue Organ Cult. 2013b;112: 181-90

[61] Wang YJ, Zhang C, Wang XQ. et al. Involvement of glucose in the regulation of ethylene biosynthesis and sensitivity in cut Paeonia suffruticosa flowers. Sci Hortic. 2014b;169: 44-50

[62] Wu F, Zhang C, Wang XQ. et al. Ethylene-influenced develop-ment of tree peony cut flowers and characterization of genes involved in ethylene biosynthesis and perception. Postharvest Biol Technol. 2017;125: 150-60

[63] Ji X, Wang M, Xu Z. et al. PlMYB308 regulates flower senescence by modulating ethylene biosynthesis in herbaceous peony. Front Plant Sci. 2022;13:872442.

[64] Chen K, Li GJ, Bressan RA. et al. Abscisic acid dynamics, signaling, and functions in plants. J Integr Plant Biol. 2020;62: 25-54

[65] Yuan YC, Zhou NN, Bai SS. et al. Evolutionary and integrative analysis of the gibberellin 20-oxidase, 3-oxidase, and 2-oxidase gene family in Paeonia ostii: insight into their roles in flower senescence. Agriculture. 2024;14:590

[66] Chandler JW. Auxin response factors. Plant Cell Environ. 2016;39: 1014-28

[67] SunY, ChenJ, YuanY. et al. Auxin efflux carrier PsPIN4 identified through genome-wide analysis as vital factor of petal abscission. Front Plant Sci. 2024a;15:1380417

[68] Zhao DQ, Zhang XY, Wang R. et al. Herbaceous peony tryptophan decarboxylase confers drought and salt stresses tolerance. Env Exp Bot. 2019;162: 345-56

[69] Cao JK. Cloning and Functional Analysis of the PlARF2 Gene in Herba-ceous Peony(MSc thesis). Henan: Henan Agricultural University; 2023: (in Chinese)

[70] Zhou L, Zhang C, Fu JX. et al. Molecular characterization and expression of ethylene biosynthetic genes during cut flower development in tree peony (Paeonia suffruticosa) in response to ethylene and functional analysis of PsACS1 in Arabidopsis thaliana. J Plant Growth Regul. 2013;32: 362-375

[71] Liu CY, Liu ZQ, Yuan YC. et al. Comprehensive analyses of the proteome and ubiquitome revealed mechanism of high temper-ature accelerating petal abscission in tree peony. Hortic Plant J. 2024;10: 205-22

[72] Tang Y, Zhang XX, Wang SL. et al. Effects of different cold storage methods on the vase quality of cut peonies. Northern Horticulture (Nat Sci). 2018;21:148-54 (in Chinese)

[73] Sun XH, Niu LX, Zhang MF. et al. Application of carbon-based nutrient fertilizer improved soil fertility and seed yield of Paeonia ostii ’Feng Dan’. IndCropProd. 2024b;212:118348.

[74] Joshi K, Jugran AK, Bhatt I. Agrotechniques development for Paeonia emodi Royle: evaluation of soil composition, biomass, and secondary metabolites. J Soil Sci Plant Nutr. 2023;23: 3290-301

[75] Hunter DA, Ferrante A, Vernieri P. et al. Role of abscisic acid in perianth senescence of daffodil (Narcissus pseudonarcissus "Dutch master"). Physiol Plant. 2004;121: 313-21

[76] do Nascimento Simões A, Diniz NB, da Silva Vieira MR, et al. Impact of GA3 and spermine on postharvest quality of anthurium cut flowers (Anthurium andraeanum) cv. Arizona. Sci Hortic. 2018;241: 178-86

[77] Cheng C, Yu Q, Wang Y. et al. Ethylene-regulated asymmetric growth of the petal base promotes flower opening in rose (Rosa hybrida). Plant Cell. 2021;33: 1229-51

[78] Lu J, Zhang G, Ma C. et al. The F-box protein RhSAF destabi-lizes the gibberellic acid receptor RhGID1 to mediate ethylene-induced petal senescence in rose. Plant Cell. 2024;36: 1736-54

[79] Ma N, Xue J, Li Y. et al. Rh-PIP2;1, a rose aquaporin gene, is involved in ethylene-regulated petal expansion. Plant Physiol. 2008;148: 894-907

[80] Eisinger W. Role of cytokinins in carnation flower senescence. Plant Physiol. 1997;59: 707-9

[81] Macnish AJ, Jiang CZ, Reid MS. Treatment with thidiazuron improves opening and vase life of iris flowers. Postharvest Biol Technol. 2010;56: 77-84

[82] Nagano S, Mori N, Tomari Y. et al. Effect of differences in light source environment on transcriptome of leaf lettuce (Lactuca sativa L.) to optimize cultivation conditions. PLoS One. 2022;17: e0265994.

[83] Shi J, Huang T, Zhang Y. et al. The effect of BVOCs pro-duced by Lysinibacillus fusiformis and LED irradiation on pigment metabolism in stored broccoli. Food Chem. 2023;420:136068.

[84] Guan Y, Ding L, Jiang J. et al. Overexpression of the CmJAZ1-like gene delays flowering in Chrysanthemum morifolium. Hortic Res. 2021;8:87

[85] He S, Zhi F, Min Y. et al. 2023. The MYB59 transcription factor negatively regulates salicylic acid- and jasmonic acid-mediated leaf senescence. Plant Physiol. 2023;192:488-503

[86] Jiang L, Liu K, Zhang T. et al. The RhWRKY33a-RhPLATZ9 reg-ulatory module delays petal senescence by suppressing rapid reactive oxygen species accumulation in rose flowers. Plant J. 2023;114: 1425-42

[87] Luo J, Chen S, Cao S. et al. Rose (Rosa hybrida) ethylene responsive factor 3 promotes rose flower senescence via direct activation of the abscisic acid synthesis-related 9-CIS-EPOXYCAROTENOID DIOXYGENASE gene. Plant Cell Physiol. 2021;62: 1030-43

[88] Xu H, Luo D, Zhang F. DcWRKY75 promotes ethylene induced petal senescence in carnation (Dianthus caryophyllus L.). Plant J. 2021;108: 1473-92

[89] Liu CY, Li FZ, Gai SP. et al. Screening and identification of genes associated with flower senescence in tree peony (Paeonia x suf-fruticosa Andrews) using suppression subtractive hybridization. J Hortic Sci Biotechnol. 2017a;92: 146-54

[90] Xu J, Kang BC, Naing AH. et al. CRISPR/Cas9-mediated editing of 1-aminocyclopropane-1-carboxylate oxidase1 enhances petunia flower longevity. Plant Biotechnol J. 2020;18: 287-97

[91] Gautam T, Dutta M, Jaiswal V. et al. Emerging roles of SWEET sugar transporters in plant development and abiotic stress responses. Cells. 2022;11:1303

[92] Huo J, Huang D, Zhang J. et al. Comparative proteomic analysis during the involvement of nitric oxide in hydrogen gas-improved postharvest freshness in cut lilies. Int J Mol Sci. 2018;19:3955

[93] Zhao H, Zhong S, Sang L. et al. PaACL silencing accelerates flower senescence and changes the proteome to maintain metabolic homeostasis in Petunia hybrida. JExp Bot. 2020;71: 4858-76

[94] Corydon TJ, Schulz H, Richter P. et al. Current knowledge about the impact of microgravity on gene regulation. Cells. 2023;12:1043

[95] Cui X, Zheng J, Zheng J. et al. Study of autophagy in plant senescence. Methods Mol Biol. 2018;1744: 299-306

[96] Wang Y, Yu B, Zhao J. et al. Autophagy contributes to leaf starch degradation. Plant Cell. 2013a;25: 1383-99

[97] Li Y, Shu P, Xiang L. et al. CRISPR/Cas9-mediated SlATG5 muta-genesis reduces the resistance of tomato fruit to Botrytis cinerea. Food Secur. 2023a;12:2750

[98] Parmesan C, Hanley ME. Plants and climate change: complexi-ties and surprises. Ann Bot. 2015;116: 849-64