Gibberellin biosynthesis is required for CPPU-induced parthenocarpy in melon

Yue Liu , Yang Li , Huixin Guo , Bingsheng Lv , Jing Feng , Huihui Wang , Zhonghua Zhang , Sen Chai

Horticulture Research ›› 2023, Vol. 10 ›› Issue (6) : 084

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Horticulture Research ›› 2023, Vol. 10 ›› Issue (6) :084 DOI: 10.1093/hr/uhad084
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Gibberellin biosynthesis is required for CPPU-induced parthenocarpy in melon
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Abstract

Spraying N-(2-chloro-4-pyridyl)- N'-phenylurea (CPPU), an exogenous cytokinin (CK) growth regulator, is the conventional method for inducing fruit set during melon (Cucumis melo L.) production; however, the mechanism by which CPPU induces fruit set is unclear. Through histological and morphological observations, fruit size was comparable between CPPU-induced fruits and normal pollinated fruits because CPPU-induced fruits had higher cell density but smaller cell size compared with normal pollinated fruits. CPPU promotes the accumulation of gibberellin (GA) and auxin and decreases the level of abscisic acid (ABA) during fruit set. Moreover, application of the GA inhibitor paclobutrazol (PAC) partially inhibits CPPU-induced fruit set. Transcriptome analysis revealed that CPPU-induced fruit set specifically induced the GA-related pathway, in which the key synthase encoding gibberellin 20-oxidase 1 (CmGA20ox1) was specifically upregulated. Further study indicated that the two-component response regulator 2 (CmRR2) of the cytokinin signaling pathway, which is highly expressed at fruit setting, positively regulates the expression of CmGA20ox1. Collectively, our study determined that CPPU-induced melon fruit set is dependent on GA biosynthesis, providing a theoretical basis for the creation of parthenocarpic melon germplasm.

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Yue Liu, Yang Li, Huixin Guo, Bingsheng Lv, Jing Feng, Huihui Wang, Zhonghua Zhang, Sen Chai. Gibberellin biosynthesis is required for CPPU-induced parthenocarpy in melon. Horticulture Research, 2023, 10 (6) : 084 DOI:10.1093/hr/uhad084

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Acknowledgements

We thank Professor Huaisong Wang for providing ivf05 seeds. We also thank Biorun Bioscience Co., Ltd (Wuhan) for Dr Jin Jie’s contributions to the genetic transformation system of melon. This work was supported by the National Natural Science Foundation of China (32225044 to Z.Z., 32130093 to Z.Z., 32102404 to S.C., 32002064 to Y.L.), This work was also supported by the Taishan Scholar Foundation of the People’s Government of Shandong Province and the Natural Science Foundation of Shandong Province (ZR2020QC157).

Author contributions

Z.Z., S.C., and Y. Liu. designed the research. S.C., H.G., Y. Li., J.F., and H.W. performed the experiments and S.C. and Y. Liu. analyzed the data. B.L. revised the manuscript. Z.Z., S.C. and Y. Liu. wrote the manuscript. All authors participated in the research and approved the final manuscript.

Data availability

Relevant data can be found within the paper and its supporting materials. All data of this study are available from the corresponding author upon reasonable request.

Conflict of interest

All authors declare no conflict of interest.

References

[1]

Zhao G, Lian Q, Zhang Z et al. A comprehensive genome variation map of melon identifies multiple domestication events and loci influencing agronomic traits. Nat Genet. 2019; 51: 1607-15.

[2]

Hayata Y, Niimi Y, Inoue K et al. CPPU and BA, with and without pollination, affect set, growth, and quality of muskmelon fruit. HortScience. 2000; 35: 868-70.

[3]

Fenn MA, Giovannoni JJ . Phytohormones in fruit development and maturation. Plant J. 2021; 105: 446-58.

[4]

McAtee P, Karim S, Schaffer R et al. A dynamic interplay between phytohormones is required for fruit development, maturation, and ripening. Front Plant Sci. 2013; 4: 79.

[5]

Ruan YL, Patrick JW, Bouzayen M et al. Molecular regulation of seed and fruit set. Trends Plant Sci. 2012; 17: 656-65.

[6]

Joldersma D, Liu Z . The making of virgin fruit: the molecular and genetic basis of parthenocarpy. J Exp Bot. 2018; 69: 955-62.

[7]

Sharif R, Su L, Chen X et al. Hormonal interactions underlying parthenocarpic fruit formation in horticultural crops. Hortic Res. 2022; 9: uhab24.

[8]

Yoshioka Y, Shimomura K, Sugiyama M . Exploring an East Asian melon (Cucumis melo L.) collection for parthenocarpic ability . Genet Resour Crop Evol. 2018; 65: 91-101.

[9]

Cheng J, Chen HW, Ding XC et al. Transcriptome analysis of the influence of CPPU application for fruit set on melon volatile content. J Integr Agric. 2021; 20: 3199-208.

[10]

Luo F, Li Q, Yu L et al. High concentrations of CPPU promotes cucurbitacin B accumulation in melon (Cucumis melo var. makuwa Makino) fruit by inducing transcription factor CmBt. Plant Physiol Biochem. 2020; 154: 770-81.

[11]

Li J, Wu Z, Cui L et al. Transcriptome comparison of global distinctive features between pollination and parthenocarpic fruit set reveals transcriptional phytohormone crosstalk in cucumber (Cucumis sativus L.). Plant Cell Physiol. 2014; 55: 1325-42.

[12]

Su L, Rahat S, Ren N et al. Cytokinin and auxin modulate cucumber parthenocarpy fruit development. Sci Hortic. 2021; 282: 110026.

[13]

Rotino GL, Perri E, Zottini M et al. Genetic engineering of parthenocarpic plants. Nat Biotechnol. 1997; 15: 1398-401.

[14]

Cong L, Yue R, Wang H et al. 2,4-D-induced parthenocarpy in pear is mediated by enhancement of GA4 biosynthesis. Physiol Plant. 2019; 166: 812-20.

[15]

Wang H, Jones B, Li Z et al. The tomato aux/IAA transcription factor IAA9 is involved in fruit development and leaf morphogenesis . Plant Cell. 2005; 17: 2676-92.

[16]

Serrani JC, Sanjuan R, Ruiz-Rivero O et al. Gibberellin regulation of fruit set and growth in tomato. Plant Physiol. 2007; 145: 246-57.

[17]

Garcia-Hurtado N, Carrera E, Ruiz-Rivero O et al. The characterization of transgenic tomato overexpressing gibberellin 20-oxidase reveals induction of parthenocarpic fruit growth, higher yield, and alteration of the gibberellin biosynthetic pathway . J Exp Bot. 2012; 63: 5803-13.

[18]

Martinez-Bello L, Moritz T, Lopez-Diaz I . Silencing C19-GA 2-oxidases induces parthenocarpic development and inhibits lateral branching in tomato plants. J Exp Bot. 2015; 66: 5897-910.

[19]

Serrani JC, Ruiz-Rivero O, Fos M et al. Auxin-induced fruit-set in tomato is mediated in part by gibberellins. Plant J. 2008; 56: 922-34.

[20]

Hu J, Israeli A, Ori N et al. The interaction between DELLA and ARF/IAA mediates crosstalk between gibberellin and auxin signaling to control fruit initiation in tomato . Plant Cell. 2018; 30: 1710-28.

[21]

Wu L, Lan J, Xiang X et al. Transcriptome sequencing and endogenous phytohormone analysis reveal new insights in CPPU controlling fruit development in kiwifruit (Actinidia chinensis). PLoS One. 2020; 15: e0240355.

[22]

Cong L, Wu T, Liu H et al. CPPU may induce gibberellin-independent parthenocarpy associated with PbRR9 in ’Dangshansu’ pear . Hortic Res. 2020; 7: 68.

[23]

Kieber JJ, Schaller GE . Cytokinin signaling in plant development. Development. 2018; 145: dev149344.

[24]

To JP, Kieber JJ . Cytokinin signaling: two-components and more. Trends Plant Sci. 2008; 13: 85-92.

[25]

Ding J, Chen B, Xia X et al. Cytokinin-induced parthenocarpic fruit development in tomato is partly dependent on enhanced gibberellin and auxin biosynthesis. PLoS One. 2013; 8: e70080.

[26]

Lu L, Liang J, Zhu X et al. Auxin- and cytokinin-induced berries set in grapevine partly rely on enhanced gibberellin biosynthesis. Tree Genet Genomes. 2016; 12: 41.

[27]

Royo C, Carbonell-Bejerano P, Torres-Pérez R et al. Developmental, transcriptome, and genetic alterations associated with parthenocarpy in the grapevine seedless somatic variant Corinto bianco. J Exp Bot. 2016; 67: 259-73.

[28]

Ding L, Yan S, Jiang L et al. HANABA TARANU regulates the shoot apical meristem and leaf development in cucumber (Cucumis sativus L.). J Exp Bot. 2015; 66: 7075-87.

[29]

Luo W, Li Y, Sun Y et al. Comparative RNA-seq analysis reveals candidate genes associated with fruit set in pumpkin. Sci Hortic. 2021; 288: 110255.

[30]

Claeys H, De Bodt S, Inze D . Gibberellins and DELLAs: central nodes in growth regulatory networks. Trends Plant Sci. 2014; 19: 231-9.

[31]

Lv B, Yan Z, Tian H et al. Local auxin biosynthesis mediates plant growth and development. Trends Plant Sci. 2019; 24: 6-9.

[32]

Zhao Y, Chan Z, Gao J et al. ABA receptor PYL9 promotes drought resistance and leaf senescence . Proc Natl Acad Sci USA. 2016; 113: 1949-54.

[33]

Ferreira FJ, Kieber JJ . Cytokinin signaling. Curr Opin Plant Biol. 2005; 8: 518-25.

[34]

Matsuo S, Kikuchi K, Fukuda M et al. Roles and regulation of cytokinins in tomato fruit development. J Exp Bot. 2012; 63: 5569-79.

[35]

Greenboim-Wainberg Y, Maymon I, Borochov R et al. Cross talk between gibberellin and cytokinin: the Arabidopsis GA response inhibitor SPINDLY plays a positive role in cytokinin signaling . Plant Cell. 2005; 17: 92-102.

[36]

Hu, Li D, Liu X et al. Engineering non-transgenic gynoecious cucumber using an improved transformation protocol and optimized CRISPR/Cas9 system. Mol Plant. 2017; 10: 1575-8.

[37]

Xin T, Zhang Z, Li S et al. Genetic regulation of ethylene dosage for cucumber fruit elongation. Plant Cell. 2019; 31: 1063-76.

[38]

Kim D, Langmead B, Salzberg SL . HISAT: a fast spliced aligner with low memory requirements. Nat Methods. 2015; 12: 357-60.

[39]

Pertea M, Pertea GM, Antonescu CM et al. StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat Biotechnol. 2015; 33: 290-5.

[40]

Love MI, Huber W, Anders S . Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014; 15: 550.

[41]

Yu G, Wang LG, Han Y et al. clusterProfiler: an R package for comparing biological themes among gene clusters. OMICS. 2012; 16: 284-7.

[42]

Xu Y, Zhang H, Zhong Y et al. Comparative genomics analysis of bHLH genes in cucurbits identifies a novel gene regulating cucurbitacin biosynthesis . Hortic Res. 2022; 9: uhac038.

[43]

Xin T, Tian H, Ma Y et al. Targeted creating new mutants with compact plant architecture using CRISPR/Cas9 genome editing by an optimized genetic transformation procedure in cucurbit plants. Hortic Res. 2022; 9: uhab086.

[44]

Napoli C, Lemieux C, Jorgensen R . Introduction of a chimeric chalcone synthase gene into petunia results in reversible cosuppression of homologous genes in trans. Plant Cell. 1990; 2: 279-89.

[45]

Zhang X, Zhou Y, Ding L et al. Transcription repressor HANABA TARANU controls flower development by integrating the actions of multiple hormones, floral organ specification genes, and GATA3 family genes in Arabidopsis. Plant Cell. 2013; 25: 83-101.

[46]

Zhu M, Tao L, Zhang J et al. The type-B response regulators ARR10, ARR12, and ARR18 specify the central cell in Arabidopsis. Plant Cell. 2022; 34: 4714-37.

[47]

Kodama Y, Shumway M, Leinonen R . The sequence read archive: explosive growth of sequencing data. Nucleic Acids Res. 2011; 40: D54-6.

[48]

Liu Y, Tian T, Zhang K et al. PCSD: a plant chromatin state database. Nucleic Acids Res. 2018; 46: D1157-67.

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