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Comprehensive Survey of the DELLA Transcription Factors in Cucumber and Functional Characterization of CsDELLA1 in Regulation of GA-Mediated Growth and Development

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Abstract

DELLAs are known as negative regulators of gibberellin (GA) signaling pathway and control many aspects of plant development. In recent years, DELLA family genes were widely studied in many plant species, but little was known about the biological functions of DELLA genes in cucumber. In this study, genome-wide identification of the DELLA gene family members was performed (CsDELLA1–4), and their phylogenetic relationship, conserved motif, gene structure, cis-regulatory elements, and expression pattern were systematically analyzed. Amongst them, CsDELLA1 encoded a protein-harbored DGLLA, LERLE, and less-conserved TVHYNP motif in its N-terminal DELLA domain, implying the possible role of CsDELLA1 in GA-regulated growth and development. As anticipated, silenced CsDELLA1 by virus-induced gene silencing resulted in increased plant height and early flowering phenotypes. In contrast, overexpression of CsDELLA1 in Arabidopsis resulted in dwarf, late flowering, and inhibited hypocotyl elongation phenotypes, indicating that overexpression of CsDELLA1 inhibited the GA response in Arabidopsis. The transgenic plants also produced more buds and shorter siliques than the wild-type (WT) plants, and displayed a significantly longer primary root length than that of WT under exogenous GA3 treatment. Collectively, these results indicated that the CsDELLA1 might play important roles in regulation of GA-mediated growth and development.

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References

  • Achard P, Genschik P (2009) Releasing the brakes of plant growth: how GAs shutdown DELLA proteins. J Exp Bot 60:1085–1092

    Article  CAS  PubMed  Google Scholar 

  • Bao S, Hua C, Shen L, Yu H (2020) New insights into gibberellin signaling in regulating flowering in Arabidopsis. J Integr Plant Biol 62:118–131

    Article  CAS  PubMed  Google Scholar 

  • Blanco-Touriñán N, Legris M, Minguet EG, Costigliolo-Rojas C, Nohales MA, Iniesto E et al (2020) COP1 destabilizes DELLA proteins in Arabidopsis. Proc Natl Acad Sci U S A 117:13792–13799

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen L, Xiang S, Chen Y, Li D, Yu D (2017) Arabidopsis WRKY45 interacts with the DELLA protein RGL1 to positively regulate age-triggered leaf senescence. Mol Plant 10:1174–1189

    Article  CAS  PubMed  Google Scholar 

  • Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He Y et al (2020a) TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant 13:1194–1202

    Article  CAS  PubMed  Google Scholar 

  • Chen L, Nan H, Kong L, Yue L, Yang H, Zhao Q et al (2020b) Soybean AP1 homologs control flowering time and plant height. J Integr Plant Biol 62:1868–1879

    Article  CAS  PubMed  Google Scholar 

  • Chen Y, Zhang M, Wang X, Shao Y, Hu X, Cheng J et al (2023) Peach DELLA protein PpeDGYLA is not degraded in the presence of active GA and causes dwarfism when overexpressed in poplar and Arabidopsis. Int J Mol Sci 24:6789

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Davière JM, Wild M, Regnault T, Baumberger N, Eisler H, Genschik P et al (2014) Class I TCP–DELLA interactions in inflorescence shoot apex determine plant height. Curr Biol 24:1923–1928

    Article  PubMed  Google Scholar 

  • de Lucas M, Davière JM, Rodríguez-Falcón M, Pontin M, Iglesias-Pedraz JM, Lorrain S et al (2008) A molecular framework for light and gibberellin control of cell elongation. Nature 451:480–484

    Article  PubMed  Google Scholar 

  • Dill A, Jung HS, Sun TP (2001) The DELLA motif is essential for gibberellin-induced degradation of RGA. Proc Natl Acad Sci U S A 98:14162–14167

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dong B, Deng Y, Wang H, Gao R, Stephen GuK, Chen S et al (2017) Gibberellic acid signaling is required to induce flowering of chrysanthemums grown under both short and long days. Int J Mol Sci 18:1259

    Article  PubMed  PubMed Central  Google Scholar 

  • Fang J, Chai Z, Yao W, Chen B, Zhang M (2021a) Interactions between ScNAC23 and ScGAI regulate GA-mediated flowering and senescence in sugarcane. Plant Sci 304:110806

    Article  CAS  PubMed  Google Scholar 

  • Fang L, Wei XY, Liu LZ, Zhou LX, Tian YP, Geng C et al (2021b) A tobacco ringspot virus-based vector system for gene and microRNA function studies in cucurbits. Plant Physiol 186:853–864

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Feng S, Martinez C, Gusmaroli G, Wang Y, Zhou J, Wang F et al (2008) Coordinated regulation of Arabidopsis thaliana development by light and gibberellins. Nature 451:475–479

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fuentes S, Ljung K, Sorefan K, Alvey E, Harberd NP, Østergaard L (2012) Fruit growth in Arabidopsis occurs via DELLA-dependent and DELLA-independent gibberellin responses. Plant Cell 24:3982–3996

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gallego-Bartolomé J, Minguet EG, Marín JA, Prat S, Blázquez MA, Alabadí D (2010) Transcriptional diversification and functional conservation between DELLA proteins in Arabidopsis. Mol Biol Evol 27:1247–1256

    Article  PubMed  Google Scholar 

  • Gebretsadik K, Qiu X, Dong S, Miao H, Bo K (2021) Molecular research progress and improvement approach of fruit quality traits in cucumber. Theor Appl Genet 134:3535–3552

    Article  PubMed  Google Scholar 

  • Gómez MD, Fuster-Almunia C, Ocaña-Cuesta J, Alonso JM, Pérez-Amador MA (2019) RGL2 controls flower development, ovule number and fertility in Arabidopsis. Plant Sci 281:82–92

    Article  PubMed  Google Scholar 

  • Gómez MD, Barro-Trastoy D, Fuster-Almunia C, Tornero P, Alonso JM, Perez-Amador MA (2020) Gibberellin-mediated RGA-LIKE1 degradation regulates embryo sac development in Arabidopsis. J Exp Bot 71:7059–7072

    Article  PubMed  PubMed Central  Google Scholar 

  • Gomi K, Sasaki A, Itoh H, Ueguchi-Tanaka M, Ashikari M, Kitano H et al (2004) GID2, an F-box subunit of the SCF E3 complex, specifically interacts with phosphorylated SLR1 protein and regulates the gibberellin-dependent degradation of SLR1 in rice. Plant J 37:626–634

    Article  CAS  PubMed  Google Scholar 

  • Guo Y, Wu H, Li X, Li Q, Zhao X, Duan X et al (2017) Identification and expression of GRAS family genes in maize (Zea mays L.). PLoS ONE 12:e0185418-19

    Article  PubMed  PubMed Central  Google Scholar 

  • Hedden P, Sponsel V (2015) A century of gibberellin research. J Plant Growth Regul 34:740–760

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hernández-García J, Briones-Moreno A, Dumas R, Blázquez MA (2019) Origin of gibberellin-dependent transcriptional regulation by molecular exploitation of a transactivation domain in DELLA proteins. Mol Biol Evol 36:908–918

    Article  PubMed  Google Scholar 

  • Hernández-García J, Briones-Moreno A, Blázquez MA (2021) Origin and evolution of gibberellin signaling and metabolism in plants. Semin Cell Dev Biol 109:46–54

    Article  PubMed  Google Scholar 

  • Hou X, Hu WW, Shen L, Lee LY, Tao Z, Han JH et al (2008) Global identification of DELLA target genes during Arabidopsis flower development. Plant Physiol 147:1126–1142

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu J, Israeli A, Ori N, Sun TP (2018) The interaction between DELLA and ARF/IAA mediates crosstalk between gibberellin and auxin signaling to control fruit initiation in tomato. Plant Cell 30:1710–1728

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang D, Wang S, Zhang B, Shang-Guan K, Shi Y, Zhang D et al (2015) A gibberellin-mediated DELLA-NAC signaling cascade regulates cellulose synthesis in rice. Plant Cell 27:1681–1696

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jasinski S, Tattersall A, Piazza P, Hay A, Martinez-Garcia JF, Schmitz G et al (2008) PROCERA encodes a DELLA protein that mediates control of dissected leaf form in tomato. Plant J 56:603–612

    Article  CAS  PubMed  Google Scholar 

  • Jiang C, Gao F, Li T, Chen T, Zheng X, Lian X et al (2022) Genome-wide analysis of the GRAS transcription factor gene family in peach (Prunus persica) and ectopic expression of PpeDELLA1 and PpeDELLA2 in Arabidopsis result in dwarf phenotypes. Sci Hortic 298:111003

    Article  CAS  Google Scholar 

  • Lawit SJ, Wych HM, Xu D, Kundu S, Tomes DT (2010) Maize DELLA proteins dwarf plant8 and dwarf plant9 as modulators of plant development. Plant Cell Physiol 51:1854–1868

    Article  CAS  PubMed  Google Scholar 

  • Lee BD, Yim Y, Cañibano E, Kim SH, García-León M, Rubio V et al (2022) CONSTITUTIVE PHOTOMORPHOGENIC 1 promotes seed germination by destabilizing RGA-LIKE 2 in Arabidopsis. Plant Physiol 189:1662–1676

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lei W, Li Y, Yao X, Qiao K, Wei L, Liu B et al (2020) NAP is involved in GA-mediated chlorophyll degradation and leaf senescence by interacting with DELLAs in Arabidopsis. Plant Cell Rep 39:75–87

    Article  CAS  PubMed  Google Scholar 

  • Li K, Yu R, Fan LM, Wei N, Chen H, Deng XW (2016) DELLA-mediated PIF degradation contributes to coordination of light and gibberellin signalling in Arabidopsis. Nat Commun 7:11868

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li Q, Li H, Huang W, Xu Y, Zhou Q, Wang S et al (2019) A chromosome-scale genome assembly of cucumber (Cucumis sativus L.). Gigascience 8:giz072

    Article  PubMed  PubMed Central  Google Scholar 

  • Li C, Dong S, Beckles DM, Miao H, Sun J, Liu X et al (2022) The qLTG1.1 candidate gene CsGAI regulates low temperature seed germination in cucumber. Theor Appl Genet 135:2593–2607

    Article  CAS  PubMed  Google Scholar 

  • Li B, Zhao YT, Yue ZC, Lei JL, Hu QZ, Tao P (2023) Identification of DELLA gene family in head cabbage and analysis of mRNA transport in the heterograft. Yi Chuan 45:156–164

    PubMed  Google Scholar 

  • Liao Z, Yu H, Duan J, Yuan K, Yu C, Meng X et al (2019) SLR1 inhibits MOC1 degradation to coordinate tiller number and plant height in rice. Nat Commun 10:2738

    Article  PubMed  PubMed Central  Google Scholar 

  • Liao L, Hu Z, Liu S, Yang Y, Zhou Y (2021) Characterization of germin-like proteins (GLPs) and their expression in response to abiotic and biotic stresses in cucumber. Horticulturae 7:412

    Article  Google Scholar 

  • Lim S, Park J, Lee N, Jeong J, Toh S, Watanabe A et al (2013) ABA-insensitive3, ABA-insensitive5, and DELLAs Interact to activate the expression of SOMNUS and other high-temperature-inducible genes in imbibed seeds in Arabidopsis. Plant Cell 25:4863–4878

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu B, Sun Y, Xue J, Jia X, Li R (2018) Genome-wide characterization and expression analysis of GRAS gene family in pepper (Capsicum annuum L.). PeerJ 6:e4796

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu Y, Wang P, Yan S, Liu X, Lu L, Chen X et al (2020) Molecular cloning and functional characterization of the DELLA gene family in Liriodendron hybrids. Forests 11:1363

    Article  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 

  • Luo W, Zhao Z, Chen H, Ao W, Lu L, Liu J et al (2023) Genome-wide characterization and expression of DELLA genes in Cucurbita moschata reveal their potential roles under development and abiotic stress. Front Plant Sci 14:1137126

    Article  PubMed  PubMed Central  Google Scholar 

  • Martí C, Orzáez D, Ellul P, Moreno V, Carbonell J, Granell A (2007) Silencing of DELLA induces facultative parthenocarpy in tomato fruits. Plant J 52:865–876

    Article  PubMed  Google Scholar 

  • Niu X, Chen S, Li J, Liu Y, Ji W, Li H (2019) Genome-wide identification of GRAS genes in Brachypodium distachyon and functional characterization of BdSLR1 and BdSLRL1. BMC Genomics 20:635

    Article  PubMed  PubMed Central  Google Scholar 

  • Phokas A, Coates JC (2021) Evolution of DELLA function and signaling in land plants. Evol Dev 23:137–154

    Article  PubMed  PubMed Central  Google Scholar 

  • Plackett ARG, Ferguson AC, Powers SJ, Wanchoo-Kohli A, Phillips AL, Wilson ZA et al (2014) DELLA activity is required for successful pollen development in the Columbia ecotype of Arabidopsis. New Phytol 201:825–836

    Article  CAS  PubMed  Google Scholar 

  • Sarwar R, Jiang T, Ding P, Gao Y, Tan X, Zhu K (2021) Genome-wide analysis and functional characterization of the DELLA gene family associated with stress tolerance in B. napus. BMC Plant Biol 21:286

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shan F, Zhang R, Zhang J, Wang C, Lyu X, Xin T et al (2021) Study on the regulatory effects of GA3 on soybean internode elongation. Plants 10:1737

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shohat H, Illouz-Eliaz N, Kanno Y, Seo M, Weiss D (2020) The tomato DELLA protein PROCERA promotes abscisic acid responses in guard cells by upregulating an abscisic acid transporter. Plant Physiol 184:518–528

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shohat H, Cheriker H, Cohen A, Weiss D (2023) Tomato ABA-IMPORTING TRANSPORTER 1.1 inhibits seed germination under high salinity conditions. Plant Physiol 191:1404–1415

    Article  CAS  PubMed  Google Scholar 

  • Sun TP (2010) Gibberellin-GID1-DELLA: a pivotal regulatory module for plant growth and development. Plant Physiol 154:567–570

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van De Velde K, Ruelens P, Geuten K, Rohde A, Van Der Straeten D (2017) Exploiting DELLA signaling in cereals. Trends Plant Sci 22:880–893

    Article  PubMed  Google Scholar 

  • Wang P, Zhang Q, Chen Y, Zhao Y, Ren F, Shi H et al (2020) Comprehensive identification and analysis of DELLA genes throughout the plant kingdom. BMC Plant Biol 20:372

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang M, Yang S, Sun L, Feng Z, Gao Y, Zhai X et al (2022) A CBL4-CIPK6 module confers salt tolerance in cucumber. Veg Res 2:1–10

    Google Scholar 

  • Xue H, Gao X, He P, Xiao G (2022) Origin, evolution, and molecular function of DELLA proteins in plants. Crop J 10:287–299

    Article  Google Scholar 

  • Yu S, Galvão VC, Zhang YC, Horrer D, Zhang TQ, Hao YH et al (2012) Gibberellin regulates the Arabidopsis floral transition through miR156-targeted SQUAMOSA promoter binding-like transcription factors. Plant Cell 24:3320–3332

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zeng D, Si C, Teixeira da Silva JA, Shi H, Chen J, Huang L et al (2023) Uncovering the involvement of DoDELLA1-interacting proteins in development by characterizing the DoDELLA gene family in Dendrobium officinale. BMC Plant Biol 23:93

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Y, Liu B, Yang S, An J, Chen C, Zhang X et al (2014) A cucumber DELLA homolog CsGAIP may inhibit staminate development through transcriptional repression of B class floral homeotic genes. PLoS ONE 9:e91804

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang Y, Zhao G, Li Y, Mo N, Zhang J, Liang Y (2017) Transcriptomic analysis implies that GA regulates sex expression via ethylene-dependent and ethylene-independent pathways in cucumber (Cucumis sativus L.). Front Plant Sci 8:10

    PubMed  PubMed Central  Google Scholar 

  • Zhang H, Wang H, Zhu Q, Gao Y, Wang H, Zhao L et al (2018) Transcriptome characterization of moso bamboo (Phyllostachys edulis) seedlings in response to exogenous gibberellin applications. BMC Plant Biol 18:125

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang Z, Chen L, Yu J (2023) Maize WRKY28 interacts with the DELLA protein D8 to affect skotomorphogenesis and participates in the regulation of shade avoidance and plant architecture. J Exp Bot 74:3122–3141

    Article  CAS  PubMed  Google Scholar 

  • Zhao J, Bo K, Pan Y, Li Y, Yu D, Li C et al (2023) Phytochrome-interacting factor PIF3 integrates phytochrome B and UVB signaling pathways to regulate gibberellin- and auxin-dependent growth in cucumber hypocotyls. J Exp Bot 74:4520–4539

    Article  CAS  PubMed  Google Scholar 

  • Zhou Y, Hu L, Ye S, Jiang L, Liu S (2019) Overexpression of an APETALA1-like gene from cucumber (Cucumis sativus L.) induces earlier flowering and abnormal leaf development in transgenic Arabidopsis. Can J Plant Sci 99:210–220

    Article  CAS  Google Scholar 

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Acknowledgements

This work was supported by the Academic and Technical Leader Plan of Jiangxi Provincial Main Disciplines (20204BCJ22023), the National Natural Science Foundation of China (32160709), and the earmarked fund for Innovation team of Jiangxi Agricultural University (JXAUCXTD009).

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  1. Yong Zhou and Jingju Chen have contributed equally to this study.

Authors and Affiliations

  1. College of Bioscience and Bioengineering, Jiangxi Agricultural University, Nanchang Economic and Technological Development District, Nanchang, 330045, Jiangxi, China

    Yong Zhou, Jingju Chen, Yaqi Hu, Lingdi Xiao, Zhaoyang Hu, Yuelong Zhou & Shiqiang Liu

  2. Key Laboratory of Crop Physiology, Ecology and Genetic Breeding, Ministry of Education, Jiangxi Agricultural University, Nanchang, 330045, China

    Yong Zhou

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JC, YH, and LX completed the experiments; YZ, ZH, and YLZ analyzed the data; YZ wrote the manuscript; SL designed of experimental work, reviewed and edited the manuscript.

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Correspondence to Shiqiang Liu.

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Zhou, Y., Chen, J., Hu, Y. et al. Comprehensive Survey of the DELLA Transcription Factors in Cucumber and Functional Characterization of CsDELLA1 in Regulation of GA-Mediated Growth and Development. J Plant Growth Regul (2024). https://doi.org/10.1007/s00344-024-11308-9

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