The chromosome-level genome of Gypsophila paniculata reveals the molecular mechanism of floral development and ethylene insensitivity

Fan Li , Yuan Gao , Chunlian Jin , Xiaohui Wen , Huaiting Geng , Ying Cheng , Haoyue Qu , Xing Liu , Shan Feng , Fan Zhang , Jiwei Ruan , Chunmei Yang , Liangsheng Zhang , Jihua Wang

Horticulture Research ›› 2022, Vol. 9 ›› Issue (1) : uhac176

PDF (2469KB)
Horticulture Research ›› 2022, Vol. 9 ›› Issue (1) :uhac176 DOI: 10.1093/hr/uhac176
Article
research-article
The chromosome-level genome of Gypsophila paniculata reveals the molecular mechanism of floral development and ethylene insensitivity
Author information +
History +
PDF (2469KB)

Abstract

Gypsophila paniculata, belonging to the Caryophyllaceae of the Caryophyllales, is one of the most famous worldwide cut flowers. It is commonly used as dried flowers, whereas the underlying mechanism of flower senescence has not yet been addressed. Here, we present a chromosome-scale genome assembly for G. paniculata with a total size of 749.58 Mb. Whole-genome duplication signatures unveil two major duplication events in its evolutionary history: an ancient one occurring before the divergence of Caryophyllaceae and a more recent one shared with Dianthus caryophyllus. The integrative analyses combining genomic and transcriptomic data reveal the mechanisms regulating floral development and ethylene response of G. paniculata. The reduction of AGAMOUS expression probably caused by sequence polymorphism and the mutation in miR172 binding site of PETALOSA are associated with the double flower formation in G. paniculata. The low expression of ETHYLENE RESPONSE SENSOR (ERS) and the reduction of downstream ETHYLENE RESPONSE FACTOR (ERF) gene copy number collectively lead to the ethylene insensitivity of G. paniculata, affecting flower senescence and making it capable of making dried flowers. This study provides a cornerstone for understanding the underlying principles governing floral development and flower senescence, which could accelerate the molecular breeding of the Caryophyllaceae species.

Cite this article

Download citation ▾
Fan Li, Yuan Gao, Chunlian Jin, Xiaohui Wen, Huaiting Geng, Ying Cheng, Haoyue Qu, Xing Liu, Shan Feng, Fan Zhang, Jiwei Ruan, Chunmei Yang, Liangsheng Zhang, Jihua Wang. The chromosome-level genome of Gypsophila paniculata reveals the molecular mechanism of floral development and ethylene insensitivity. Horticulture Research, 2022, 9 (1) : uhac176 DOI:10.1093/hr/uhac176

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Lu D, Nicholas JT . Gypsophila linnaeus . In: Wu Z, Raven PH (eds.), Flora of China, Chapter 6. Beijing/St. Louis: Science Press/Missouri Botanical Garden, 2001, 108-13.

[2]

Li F, Wang G, Yu R et al. Effects of seasonal variation and gibberellic acid treatment on the growth and development of Gypsophila paniculata . HortScience. 2019; 54: 1370-4.

[3]

Wani MA, Nazki IT, Din A et al. Sustainable Agriculture Reviews. In: Lichtfouse E (ed.), Floriculture Sustainability Initiative: The Dawn of New Era, Chapter 27. Cham: Springer International Publishing, 2018, 91-127.

[4]

Jin C, Sun D, Wei C et al. Gas chromatography-mass spectrometry analysis of natural products in Gypsophila paniculata . HortScience. 2021; 56: 1195-8.

[5]

Li F, Jin C, Zhang L et al. Hyper-recombinant plants: an emerging field for plant breeding. Crit Rev Plant Sci. 2021; 40: 446-58.

[6]

Li F, Mo X, Wu L et al. A novel double-flowered cultivar of Gypsophila paniculata mutagenized by 60Co γ-ray. HortScience. 2020; 55: 1531-2.

[7]

Wang SM, Piao XC, Park SY et al. Improved micropropagation of Gypsophila paniculata with bioreactor and factors affecting ex vitro rooting in microponic system. In Vitro Cell. Dev Biol Plant. 2013; 49: 70-8.

[8]

Zvi MMB, Zuker A, Ovadis M et al. Agrobacterium-mediated transformation of gypsophila (Gypsophila paniculata L.) . Mol Breed. 2008; 22: 543-53.

[9]

Wang Q, Zhang X, Lin S et al. Mapping a double flower phenotype-associated gene DcAP2L in Dianthus chinensis . J Exp Bot. 2020; 71: 1915-27.

[10]

François L, Verdenaud M, Fu X et al. A miR172 target-deficient AP2-like gene correlates with the double flower phenotype in roses. Sci Rep. 2018; 8: 12912.

[11]

Li S, Cheng Y, Sun D et al. Identification and expression of TOP3α in Gerbera hybrida . Hortic Plant J. 2021; 7: 167-73.

[12]

Krizek BA, Fletcher JC . Molecular mechanisms of flower development: an armchair guide. Nat Rev Genet. 2005; 6: 688-98.

[13]

Zhang L, Chen F, Zhang X et al. The water lily genome and the early evolution of flowering plants. Nature. 2020; 577: 79-84.

[14]

Dubois A, Raymond O, Maene M et al. Tinkering with the C-function: a molecular frame for the selection of double flowers in cultivated roses. PLoS One. 2010; 5: e9288.

[15]

Shibuya T, Murakawa Y, Nishidate K et al. Characterization of flowering-related genes and flowering response in relation to blue light in Gypsophila paniculata . J Hortic. 2017; 86: 94-104.

[16]

Morgan E, Funnell K . Ornamental Crops. In: Van Huylenbroeck J (ed.), Limonium, Chapter 21. Cham: Springer International Publishing, 2018, 513-27.

[17]

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. Physiol Veg. 2020; 151: 103-12.

[18]

Liu Y, Tang M, Liu M et al. The molecular regulation of ethylene in fruit ripening. Small Methods. 2020; 4: 1900485.

[19]

Ma N, Ma C, Liu Y et al. Petal senescence: a hormone view. J Exp Bot. 2018; 69: 719-32.

[20]

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.

[21]

Zhang S, Zhao Q, Zeng D et al. RhMYB108, an R2R3-MYB transcription factor, is involved in ethylene-and JA-induced petal senescence in rose plants . Hortic. Res. 2019; 6: 131-1.

[22]

Jing W, Zhao Q, Zhang S et al. RhWRKY33 positively regulates onset of floral senescence by responding to wounding-and ethylene-signaling in rose plants. Front Plant Sci. 2021; 12: 726797-7.

[23]

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

[24]

Van Doorn WG, Reid MS . Role of ethylene in flower senescence of Gypsophila paniculata L. Postharvest Biol Technol. 1992; 1: 265-72.

[25]

Hoeberichts FA, de Jong AJ, Woltering EJ . Apoptotic-like cell death marks the early stages of gypsophila (Gypsophila paniculata) petal senescence . Postharvest Biol Technol. 2005; 35: 229-36.

[26]

Doorn WGV . Effect of ethylene on flower abscission: a survey. Ann Bot. 2002; 89: 689-93.

[27]

Doorn WV, Stead A . Abscission of flowers and floral parts. J Exp Bot. 1997; 48: 821-37.

[28]

Chen F, Su L, Hu S et al. A chromosome-level genome assembly of rugged rose (Rosa rugosa) provides insights into its evolution, ecology, and floral characteristics . Horticulture Research. 2021; 8: 141.

[29]

Versteeg R, van Schaik BDC, van Batenburg MF et al. The human transcriptome map reveals extremes in gene density, intron length, GC content, and repeat pattern for domains of highly and weakly expressed genes. Genome Res. 2003; 13: 1998-2004.

[30]

Yang Z, Rannala B . Bayesian estimation of species divergence times under a molecular clock using multiple fossil calibrations with soft bounds. Mol Biol Evol. 2006; 23: 212-26.

[31]

Gao W, Lu L, Qiu W et al. OsPAP26 encodes a major purple acid phosphatase and regulates phosphate remobilization in rice. Plant Cell Physiol. 2017; 58: 885-92.

[32]

Kan C, Zhang Y, Wang HL et al. Transcription factor NAC075 delays leaf senescence by deterring reactive oxygen species accumulation in Arabidopsis . Front Plant Sci. 2021; 12: 164.

[33]

Lin Z, Ho CW, Grierson D . AtTRP1 encodes a novel TPR protein that interacts with the ethylene receptor ERS1 and modulates development in Arabidopsis . J Exp Bot. 2009; 60: 3697-714.

[34]

Chen F, Song Y, Li X et al. Genome sequences of horticultural plants: past, present, and future. Hortic Res. 2019; 6: 1-23.

[35]

Parcy F, Bomblies K, Weigel D . Interaction of LEAFY, AGAMOUS and TERMINAL FLOWER1 in maintaining floral meristem identity in Arabidopsis . Development. 2002; 129: 2519-27.

[36]

Aida R, Komano M, Saito M et al. Chrysanthemum flower shape modification by suppression of chrysanthemum- AGAMOUS gene . Plant Biotechnol. 2008; 25: 55-9.

[37]

Liu Z, Zhang D, Liu D et al. Exon skipping of AGAMOUS homolog PrseAG in developing double flowers of Prunus lanesiana (Rosaceae) . Plant Cell Rep. 2013; 32: 227-37.

[38]

Dreni L, Kater MM . MADS reloaded: evolution of the AGAMOUS subfamily genes. New Phytol. 2014; 201: 717-32.

[39]

Chunlian J, Huaiting G, Suping Q et al. AGAMOUS correlates with the semi-double flower trait in carnation . Ornam Plant Res. 2022; 2: 1-6.

[40]

Liang Y, Li F, Gao Q et al. The genome of Eustoma grandiflorum reveals the whole-genome triplication event contributing to ornamental traits in cultivated lisianthus. Plant Biotechnol J. 2022.

[41]

Gattolin S, Cirilli M, Chessa S et al. Mutations in orthologous PETALOSA TOE-type genes cause a dominant double-flower phenotype in phylogenetically distant eudicots. J Exp Bot. 2020; 71: 2585-95.

[42]

Yu Y, Wang H, Liu J et al. Transcriptional regulation of two RTE-like genes of carnation during flower senescence and upon ethylene exposure, wounding treatment and sucrose supply. Plant Biol. 2011; 13: 719-24.

[43]

Naing AH, Soe MT, Kyu SY et al. Nano-silver controls transcriptional regulation of ethylene-and senescence-associated genes during senescence in cut carnations. Sci Hortic. 2021; 287: 110280.

[44]

Shibuya K, Nagata M, Tanikawa N et al. Comparison of mRNA levels of three ethylene receptors in senescing flowers of carnation (Dianthus caryophyllus L.) . J Exp Bot. 2002; 53: 399-406.

[45]

Yagi M, Kosugi S, Hirakawa H et al. Sequence analysis of the genome of carnation (Dianthus caryophyllus L.) . DNA Res. 2014; 21: 231-41.

[46]

Dervinis C, Clark DG, Barrett JE et al. Effect of pollination and exogenous ethylene on accumulation of ETR1 homologue transcripts during flower petal abscission in geranium (pelargonium × hortorum L.H. bailey). Plant Mol Biol. 2000; 42: 847-56.

[47]

Kuroda S, Hakata M, Hirose Y et al. Ethylene production and enhanced transcription of an ethylene receptor gene, ERS1, in delphinium during abscission of florets. Plant Physiol Biochem. 2003; 41: 812-20.

[48]

Tanase K, Ichimura K . Expression of ethylene receptors dl-ERS1-3 and dl-ERS2, and ethylene response during flower senescence in delphinium . J Plant Physiol. 2006; 163: 1159-66.

[49]

Arumuganathan K, Earle ED . Estimation of nuclear DNA content of plants by flow cytometry. Plant Mol Biol Report. 1991; 9: 229-41.

[50]

Xiao CL, Chen Y, Xie SQ et al. MECAT: fast mapping, error correction, and de novo assembly for single-molecule sequencing reads. Nat Methods. 2017; 14: 1072-4.

[51]

Li H, Durbin R . Fast and accurate short read alignment with burrows-wheeler transform. Bioinformatics. 2009; 25: 1754-60.

[52]

Zhang X, Zhang S, Zhao Q et al. Assembly of allele-aware, chromosomal-scale autopolyploid genomes based on hi-C data. Nature Plants. 2019; 5: 833-45.

[53]

Vasimuddin M, Misra S, Li H et al. Efficient architecture-aware acceleration of BWA-MEM for multicore systems. In: 2019 IEEE Parallel and Distributed Processing Symposium (IPDPS).IEEE, 2019; 314-24.

[54]

Li H, Handsaker B, Wysoker A et al. The sequence alignment/map format and SAMtools. Bioinformatics. 2009; 25: 2078-9.

[55]

Simão FA, Waterhouse RM, Ioannidis P et al. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics. 2015; 31: 3210-2.

[56]

Huerta-Cepas J, Forslund K, Coelho LP et al. Fast genome-wide functional annotation through orthology assignment by eggNOG-mapper. Mol Biol Evol. 2017; 34: 2115-22.

[57]

Finn RD, Clements J, Eddy SR . HMMER web server: interactive sequence similarity searching. Nucleic Acids Res. 2011; 39: W29-37.

[58]

Tang H, Bowers JE, Wang X et al. Synteny and collinearity in plant genomes. Science. 2008; 320: 486-8.

[59]

Sievers F, Higgins DG . Clustal omega for making accurate alignments of many protein sequences. Protein Sci. 2018; 27: 135-45.

[60]

Yang Z . PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol. 2007; 24: 1586-91.

[61]

Han MV, Thomas GWC, Lugo-Martinez J et al. Estimating gene gain and loss rates in the presence of error in genome assembly and annotation using CAFE 3. Mol Biol Evol. 2013; 30: 1987-97.

[62]

Katoh K, Standley DM . MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013; 30: 772-80.

[63]

Edgar RC . MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004; 32: 1792-7.

[64]

Langfelder P, Horvath S . WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics. 2008; 9: 559-9.

[65]

Li F, Cheng Y, Ma L et al. Identification of reference genes provides functional insights into meiotic recombination suppressors in Gerbera hybrida . Hortic Plant J. 2022; 8: 123-32.

PDF (2469KB)

0

Accesses

0

Citation

Detail

Sections
Recommended

/