A petunia transcription factor, PhOBF1, regulates flower senescence by modulating gibberellin biosynthesis

Xiaotong Ji , Ziwei Xin , Yanping Yuan , Meiling Wang , Xinyi Lu , Jiaqi Li , Yanlong Zhang , Lixin Niu , Cai-Zhong Jiang , Daoyang Sun

Horticulture Research ›› 2023, Vol. 10 ›› Issue (4) : 022

PDF (5130KB)
Horticulture Research ›› 2023, Vol. 10 ›› Issue (4) :022 DOI: 10.1093/hr/uhad022
Article
research-article
A petunia transcription factor, PhOBF1, regulates flower senescence by modulating gibberellin biosynthesis
Author information +
History +
PDF (5130KB)

Abstract

Flower senescence is commonly enhanced by the endogenous hormone ethylene and suppressed by the gibberellins (GAs) in plants. However, the detailed mechanisms for the antagonism of these hormones during flower senescence remain elusive. In this study, we characterized one up-regulated gene PhOBF1, belonging to the basic leucine zipper transcription factor family, in senescing petals of petunia (Petunia hybrida). Exogenous treatments with ethylene and GA3 provoked a dramatic increase in PhOBF1 transcripts. Compared with wild-type plants, PhOBF1-RNAi transgenic petunia plants exhibited shortened flower longevity, while overexpression of PhOBF1 resulted in delayed flower senescence. Transcript abundances of two senescence-related genes PhSAG12 and PhSAG29 were higher in PhOBF1-silenced plants but lower in PhOBF1-overexpressing plants. Silencing and overexpression of PhOBF1 affected expression levels of a few genes involved in the GA biosynthesis and signaling pathways, as well as accumulation levels of bioactive GAs GA1 and GA3. Application of GA3 restored the accelerated petal senescence to normal levels in PhOBF1-RNAi transgenic petunia lines, and reduced ethylene release and transcription of three ethylene biosynthetic genes PhACO1, PhACS1, and PhACS2. Moreover, PhOBF1 was observed to specifically bind to the PhGA20ox3 promoter containing a G-box motif. Transient silencing of PhGA20ox3 in petunia plants through tobacco rattle virus-based virus-induced gene silencing method led to accelerated corolla senescence. Our results suggest that PhOBF1 functions as a negative regulator of ethylene-mediated flower senescence by modulating the GA production.

Cite this article

Download citation ▾
Xiaotong Ji, Ziwei Xin, Yanping Yuan, Meiling Wang, Xinyi Lu, Jiaqi Li, Yanlong Zhang, Lixin Niu, Cai-Zhong Jiang, Daoyang Sun. A petunia transcription factor, PhOBF1, regulates flower senescence by modulating gibberellin biosynthesis. Horticulture Research, 2023, 10 (4) : 022 DOI:10.1093/hr/uhad022

登录浏览全文

4963

注册一个新账户 忘记密码

Acknowledgements

We thank Houhua Li for offering the pHIS2 and pGADT7-Rec vectors. We are grateful to Jiaxin Meng for technique help in dual luciferase assay. We are appreciative of Xiaokun Liu’s kind favor for apparatus operation. This study was funded by the National Natural Science Foundation of China (Grant no. 32271953 and 31801895), Postdoctoral Special Funding Project of China (Grant no. 2019T120958), and the Basic Scientific Research Expense of Northwest A&F University (Grant no. Z1090322159).

Author contributions

D.S. and X.J. conceived and designed the experiments. X.J., Z.X., Y.Y., M.W., X.L., and J.L. conducted the experiments. C.J. provided the materials. M.W., X.L., and J.L. prepared the reagents. X.J., Z.X., Y.Z., L.N., and D.S. analysed the experimental data. X.J. and D.S. wrote the original paper. D.S., C.J., L.N., and Y.Z. revised the manuscript.

Data availability

All data supporting the conclusions of this work are present in the paper or its Supplementary material files.

Conflict of interest

The authors declare that they have no conflict of interest.

References

[1]

Yang, Takenaga S, Ohno S et al. Ethylene-sensitive abscission layer formation and petal senescence in cut dahlia inflorescences. Hortic J. 2021; 90: 460-8.

[2]

Guiboileau A, Sormani R, Meyer C et al. Senescence and death of plant organs: nutrient recycling and developmental regulation. C R Biol. 2010; 333: 382-91.

[3]

Chen Y, Zhang J, Li Q et al. Effects of nitrogen application on postsilking root senescence and yield of maize. Agron J. 2015; 107: 835-42.

[4]

Schneider HM, Postma JA, Wojciechowski T et al. Root cortical senescence improves growth under suboptimal availability of N, P, and K. Plant Physiol. 2017; 174: 2333-47.

[5]

Liang C, Wang Y, Zhu Y et al. OsNAP connects abscisic acid and leaf senescence by fine-tuning abscisic acid biosynthesis and directly targeting senescence-associated genes in rice. Proc Natl Acad Sci U S A. 2014; 111: 10013-8.

[6]

Yu G, Xie Z, Lei S et al. The NAC factor LpNAL delays leaf senescence by repressing two chlorophyll catabolic genes in perennial ryegrass. Plant Physiol. 2022; 189: 595-610.

[7]

Isobe K, Kurose T, Sasaki Y et al. Effects of early sowing cultivation on yield and occurrence of delayed stem senescence in several soybean cultivars in South Kanto. Jpn J Crop Sci. 2014; 83: 195-202.

[8]

Jiang G, Yan H, Wu F et al. Litchi fruit LcNAC1 is a target of LcMYC2 and regulator of fruit senescence through its interaction with LcWRKY1. Plant Cell Physiol. 2017; 58: 1075-89.

[9]

Kuang JF, Chen JY, Luo M et al. Histone deacetylase HD2 interacts with ERF1 and is involved in longan fruit senescence. J Exp Bot. 2012; 63: 441-54.

[10]

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.

[11]

Wu L, Ma N, Jia Y et al. An ethylene-induced regulatory module delays flower senescence by regulating cytokinin content. Plant Physiol. 2017; 173: 853-62.

[12]

Lerslerwong L, Ketsa S, van Doorn WG . Protein degradation and peptidase activity during petal senescence in Dendrobium cv. Khao Sanan . Postharvest Biol Technol. 2009; 52: 84-90.

[13]

Chang X, Donnelly L, Sun D et al. A petunia homeodomainleucine zipper protein, PhHD-zip, plays an important role in flower senescence. PLoS One. 2014; 9: e88320.

[14]

Müller R, Stummann BM, Andersen AS et al. Involvement of ABA in postharvest life of miniature potted roses. Plant Growth Regul. 1999; 29: 143-50.

[15]

Kumar M, Singh V, Arora A et al. The role of abscisic acid (ABA) in ethylene insensitive gladiolus (Gladiolus grandiflora Hort.) flower senescence . Acta Physiol Plant. 2014; 36: 151-9.

[16]

Porat R, Borochov A, Halevy A . Enhancement of petunia and dendrobium flower senescence by jasmonic acid methyl ester is via the promotion of ethylene production. Plant Growth Regul. 1993; 13: 297-301.

[17]

Macnish A, Jiang CZ, Chieng S et al. Gibberellin/sucrose pulsing improves the performance of Iris. FloraCulture Int. 2010; 20: 38.

[18]

P, Zhang C, Liu J et al. RhHB1 mediates the antagonism of gibberellins to ABA and ethylene during rose (Rosa hybrida) petal senescence . Plant J. 2014; 78: 578-90.

[19]

Hossain AS . Development of longevity of allamanda flower as affected by gibberellic acid and aluminium salt. Res J Environ Sci. 2015; 9: 178-85.

[20]

Tahir I, Nisar S, Dar R . Gibberellin and cytokinins modulate flower senescence and longevity in Nicotiana plumbaginifolia. Acta Hortic. 2019; 1263: 469-76.

[21]

Adil AM, Ahmed EE, Al-Chalabi AT et al. Effect of planting time and corms treatment with gibberellic acid on growth, flowering, and vase life of ‘Corona’. J Hortic Res. 2021; 29: 23-30.

[22]

Kumar N, Srivastava GC, Dixit K . Hormonal regulation of flower senescence in roses (Rosa hybrida L.). Plant Growth Regul. 2008; 55: 65-71.

[23]

Trivellini A, Ferrante A, Vernieri P et al. Effects of abscisic acid on ethylene biosynthesis and perception in Hibiscusa rosasinensis L. flower development . J Exp Bot. 2011; 62: 5437-52.

[24]

Onoue T, Mikami M, Yoshioka T et al. Characteristics of the inhibitory action of 1, 1-dimethyl-4-(phenylsulfonyl) semicarbazide (DPSS) on ethylene production in carnation (Dianthus caryophyllus L.) flowers . Plant Growth Regul. 2000; 30: 201-7.

[25]

Kim J, Chang C, Tucker ML . To grow old: regulatory role of ethylene and jasmonic acid in senescence. Front Plant Sci. 2015; 6: 20.

[26]

Chen C, Hussain N, Wang Y et al. An ethylene-inhibited NFYC transcription factor RhNF-YC9 regulates petal expansion in rose. Hortic Plant J. 2020; 6: 419-27.

[27]

Riechmann JL, Heard J, Martin G et al. Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science. 2000; 290: 2105-10.

[28]

Ma J, Hanssen M, Lundgren K et al. The sucrose-regulated Arabidopsis transcription factor bZIP11 reprograms metabolism and regulates trehalose metabolism. New Phytol. 2011; 191: 733-45.

[29]

Weiste C, Dröge-Laser W . The Arabidopsis transcription factor bZIP11 activates auxin-mediated transcription by recruiting the histone acetylation machinery. Nat Commun. 2014; 5: 3883.

[30]

Yang SH, Berberich T, Sano H et al. Specific association of transcripts of tbzF and tbz17, tobacco genes encoding basic region leucine zipper-type transcriptional activators, with guard cells of senescing leaves and/or flowers . Plant Physiol. 2001; 127: 23-32.

[31]

Thalor SK, Berberich T, Lee SS et al. Deregulation of sucrosecontrolled translation of a bZIP-type transcription factor results in sucrose accumulation in leaves. PLoS One. 2012; 7: e33111.

[32]

Han X, Mao L, Lu W et al. Positive regulation of the transcription of AchnKCS by a bZIP transcription factor in response to ABAstimulated suberization of kiwifruit . J Agric Food Chem. 2019; 67: 7390-8.

[33]

Du Y, Liu L, Peng Y et al. UNBRANCHED3 expression and inflorescence development is mediated by UNBRANCHED2 and the distal enhancer, KRN4, in maize . PLoS Genet. 2020; 16: e1008764.

[34]

Reid MS, Chen JC, Jiang CZ . Virus-induced gene silencing for functional characterization of genes in petunia. In: Gerats T, Strommer J, eds. Petunia. Springer: Berlin Heidelberg, 2009, 381-94.

[35]

Wang H, Chang X, Lin J et al. Transcriptome profiling reveals regulatory mechanisms underlying corolla senescence in petunia. Hortic Res. 2018; 5: 16.

[36]

Wang H, Stier G, Lin J et al. Transcriptome changes associated with delayed flower senescence on transgenic petunia by inducing expression of etr1-1, a mutant ethylene receptor . PLoS One. 2013; 8: e65800.

[37]

Yin J, Chang X, Kasuga T et al. A basic helix-loop-helix transcription factor, PhFBH4, regulates flower senescence by modulating ethylene biosynthesis pathway in petunia . Hortic Res. 2015; 2: 15059.

[38]

Sun D, Li S, Niu L et al. PhOBF1, a petunia ocs element binding factor, plays an important role in antiviral RNA silencing . J Exp Bot. 2017; 68: 915-30.

[39]

Ehlert A, Weltmeier F, Wang X et al. Two-hybrid protein-protein interaction analysis in Arabidopsis protoplasts: establishment of a heterodimerization map of group C and group S bZIP transcription factors. Plant J. 2006; 46: 890-900.

[40]

Hanson J, Hanssen M, Wiese A et al. The sucrose regulated transcription factor bZIP11 affects amino acid metabolism by regulating the expression of ASPARAGINE SYNTHETASE1 and PROLINE DEHYDROGENASE2. Plant J. 2008; 53: 935-49.

[41]

Srikanth A, Schmid M . Regulation of flowering time: all roads lead to Rome. Cell Mol Life Sci. 2011; 68: 2013-37.

[42]

Zhang H, Zhou C . Signal transduction in leaf senescence. Plant Mol Biol. 2013; 82: 539-45.

[43]

Nijhawan A, Jain M, Tyagi AK et al. Genomic survey and gene expression analysis of the basic leucine zipper transcription factor family in rice. Plant Physiol. 2008; 146: 333-50.

[44]

Wigge PA, Kim MC, Jaeger KE et al. Integration of spatial and temporal information during floral induction in Arabidopsis. Science. 2005; 309: 1056-9.

[45]

Abe M, Kobayashi Y, Yamamoto S et al. FD, a bZIP protein mediating signals from the floral pathway integrator FT at the shoot apex. Science. 2005; 309: 1052-6.

[46]

Chuang CF, Running MP, Williams RW et al. The PERIANTHIA gene encodes a bZIP protein involved in the determination of floral organ number in Arabidopsis thaliana. Genes Dev. 1999; 13: 334-44.

[47]

Cai F, Shao C, Zhang Y et al. Two FD homologs from London plane (Platanus acerifolia) are associated with floral initiation and flower morphology . Plant Sci. 2021; 310: 110971.

[48]

Dar RA, Nisar S, Tahir I . Ethylene: a key player in ethylene sensitive flower senescence: a review. Sci Hortic. 2021; 290: 110491.

[49]

Maxson J, Woodson W . Transcriptional regulation of senescence-related genes in carnation flowers. In: Kanellis AK, Chang C, Kende H, Grierson D, eds. Biology and Biotechnology of the Plant Hormone Ethylene. Springer: Dordrecht, 1997, 155-62.

[50]

Reid MS, Jiang CZ . Postharvest biology and technology of cut flowers and potted plants. Hortic Rev. 2012; 40: 3-56.

[51]

Tan Y, Liu J, Huang F et al. PhGRL2 protein, interacting with PhACO1, is involved in flower senescence in the petunia. Mol Plant. 2014; 7: 1384- 7.

[52]

Verma V, Ravindran P, Kumar PP . Plant hormone-mediated regulation of stress responses. BMC Plant Biol. 2016; 16: 86.

[53]

Love AJ, Laval V, Geri C et al. Components of Arabidopsis defense-and ethylene-signaling pathways regulate susceptibility to Cauliflower mosaic virus by restricting long-distance movement. Mol Plant-Microbe Interact. 2007; 20: 659-70.

[54]

Zhu S, Gao F, Cao X et al. The rice dwarf virus P2 protein interacts with ent-kaurene oxidases in vivo, leading to reduced biosynthesis of gibberellins and rice dwarf symptoms. Plant Physiol. 2005; 139: 1935-45.

[55]

Dong T, Zheng T, Fu W et al. The effect of ethylene on the color change and resistance to Botrytis cinerea infection in ‘Kyoho’grape fruits . Foods. 2020; 9: 892-7.

[56]

Ren H, Wu Y, Ahmed T et al. Response of resistant and susceptible bayberry cultivars to infection of twig blight pathogen by histological observation and gibberellin related genes expression. Pathogens. 2021; 10: 402-16.

[57]

Lange T, Krämer C, Pimenta Lange MJ . The class III gibberellin 2-oxidases AtGA2ox9 and AtGA2ox10 contribute to cold stress tolerance and fertility. Plant Physiol. 2020; 184: 478-86.

[58]

Zhang Z, Huang R . Enhanced tolerance to freezing in tobacco and tomato overexpressing transcription factor TERF2/ LeERF2 is modulated by ethylene biosynthesis . Plant Mol Biol. 2010; 73: 241-9.

[59]

Alghabari F, Ihsan MZ, Khaliq A et al. Gibberellin-sensitive Rht alleles confer tolerance to heat and drought stresses in wheat at booting stage . J Cereal Sci. 2016; 70: 72-8.

[60]

Arraes FBM, Beneventi MA, Lisei ME et al. Implications of ethylene biosynthesis and signaling in soybean drought stress tolerance. BMC Plant Biol. 2015; 15: 213.

[61]

Shi G, Guo X, Zhang G et al. Physiological changes during florescence and flower senescence of Chinese peony. Acta Bot Sin. 2008; 28: 506-11.

[62]

Scarpeci TE, Frea VS, Zanor MI et al. Overexpression of AtERF019 delays plant growth and senescence, and improves drought tolerance in Arabidopsis . J Exp Bot. 2017; 68: 673-85.

[63]

Zhang Y, Wu Z, Feng M et al. The circadian-controlled PIF8BBX28 module regulates petal senescence in rose flowers by governing mitochondrial ROS homeostasis at night. Plant Cell. 2021; 33: 2716-35.

[64]

Fukazawa J, Nakata M, Ito T et al. The transcription factor RSG regulates negative feedback of NtGA20ox1 encoding GA 20oxidase . Plant J. 2010; 62: 1035-45.

[65]

Coomey JH, MacKinnon KJM, McCahill IW et al. Touch-triggered bZIP translocation regulates elongation and secondary wall biosynthesis. bioRxiv. 2022;preprint: not peer reviewed.

[66]

Saks Y, Van Staden J . The role of gibberellic acid in the senescence of carnation flowers. J Plant Physiol. 1992; 139: 484-8.

[67]

Steffens B, Sauter M . Epidermal cell death in rice is regulated by ethylene, gibberellin, and abscisic acid. Plant Physiol. 2005; 139: 713-21.

[68]

Ziauka J, Kuusiene S . Plant hormone gibberellin induces decline of viability in isolated larch shoot buds. Balt For. 2009; 15: 13-22.

[69]

Liao PC, Lin TP, Lan WC et al. Duplication of the class I cytosolic small heat shock protein gene and potential functional divergence revealed by sequence variations flanking the α-crystallin domain in the genus Rhododendron (Ericaceae). Ann Bot. 2010; 105: 57-69.

[70]

Zhou H, Liao L, Xu S et al. Two amino acid changes in the R3 repeat cause functional divergence of two clustered MYB10 genes in peach . Plant Mol Biol. 2018; 98: 169-83.

[71]

Pun UK, Ichimura K . Role of sugars in senescence and biosynthesis of ethylene in cut flowers. Jpn Agric Res Q. 2003; 37: 219-24.

[72]

Zhang L, Becker DF . Connecting proline metabolism and signaling pathways in plant senescence. Front Plant Sci. 2015; 6: 552.

[73]

De Jong AT . Effect of flanking bases on the DNA specificity of EmBP-1. Biochemistry. 2013; 52: 786-94.

[74]

Carles C, Bies-Etheve N, Aspart L et al. Regulation of Arabidopsis thaliana Em genes: role of ABI5 . Plant J. 2002; 30: 373-83.

[75]

Alonso R, Oñate-Sánchez L, Weltmeier F et al. A pivotal role of the basic leucine zipper transcription factor bZIP53 in the regulation of Arabidopsis seed maturation gene expression based on heterodimerization and protein complex formation. Plant Cell. 2009; 21: 1747-61.

[76]

Mendes A, Kelly AA, van Erp H et al. bZIP67 regulates the omega3 fatty acid content of Arabidopsis seed oil by activating fatty acid desaturase3. Plant Cell. 2013; 25: 3104-16.

[77]

Nawkar GM, Kang CH, Maibam P et al. HY5, a positive regulator of light signaling, negatively controls the unfolded protein response in Arabidopsis. Proc Natl Acad Sci U S A. 2017; 114: 2084-9.

[78]

Dixit SK, Gupta A, Senthil-Kumar M . Current understanding of regulation of GBF3 under abiotic and biotic stresses and its potential role in combined stress tolerance. In: Akula R, Singh GS, eds. Metabolic Adaptations in Plants during Abiotic Stress. CRC Press: Boca Raton, 2018, 289-94.

[79]

Fujita Y, Yoshida T, Yamaguchi-Shinozaki K . Pivotal role of the AREB/ABF-SnRK2 pathway in ABRE-mediated transcription in response to osmotic stress in plants. Physiol Plant. 2013; 147: 15-27.

[80]

Kaminaka H, Näke C, Epple P et al. bZIP10-LSD1 antagonism modulates basal defense and cell death in Arabidopsis following infection. EMBO J. 2006; 25: 4400-11.

[81]

Ji X, Liu G, Liu Y et al. The bZIP protein from Tamarix hispida, ThbZIP1, is ACGT elements binding factor that enhances abiotic stress signaling in transgenic Arabidopsis . BMC Plant Biol. 2013; 13: 151.

[82]

Shibuya K, Yoshioka T, Hashiba T et al. Role of the gynoecium in natural senescence of carnation (Dianthus caryophyllus L.) flowers . J Exp Bot. 2000; 51: 2067-73.

[83]

Aalifar M, Aliniaeifard S, Arab M et al. Blue light postpones senescence of carnation flowers through regulation of ethylene and abscisic acid pathway-related genes. Plant Physiol Biochem. 2020; 151: 103-12.

[84]

Jones ML, Stead AD, Clark DG . Petunia flower senescence. In: Gerats T, Strommer J, eds. Petunia. Springer: Berlin Heidelberg, 2009, 301-24.

[85]

Prior MJ, Selvanayagam J, Kim JG et al. Arabidopsis bZIP11 is a susceptibility factor during Pseudomonas syringae infection . Mol Plant-Microbe Interact. 2021; 34: 439-47.

[86]

Liang YC, Reid MS, Jiang CZ . Controlling plant architecture by manipulation of gibberellic acid signalling in petunia. Hortic Res. 2014; 1: 14061.

[87]

Livak KJ, Schmittgen TD . Analysis of relative gene expression data using real-time quantitative PCR and the 2 −ΔΔCT method . Methods. 2001; 25: 402-8.

[88]

Gou J, Strauss SH, Tsai CJ et al. Gibberellins regulate lateral root formation in Populus through interactions with auxin and other hormones . Plant Cell. 2010; 22: 623-39.

[89]

Yin D, Sun D, Han Z et al. PhERF2, an ethylene-responsive element binding factor, plays an essential role in waterlogging tolerance of petunia . Hortic Res. 2019; 6: 83.

[90]

Sun D, Zhang X, Zhang Q et al. Comparative transcriptome profiling uncovers a Lilium regale NAC transcription factor, LrNAC35, contributing to defence response against cucumber mosaic virus and tobacco mosaic virus . Mol Plant Pathol. 2019; 20: 1662-81.

[91]

Chen JC, Jiang CZ, Gookin T et al. Chalcone synthase as a reporter in virus-induced gene silencing studies of flower senescence. Plant Mol Biol. 2004; 55: 521-30.

PDF (5130KB)

70

Accesses

0

Citation

Detail

Sections
Recommended

/