Abstract
Grape (Vitis vinifera L.), a commercial fruit crop, is profoundly sensitive to gibberellic acid (GA), however exogenous application can significantly induce seedless grape berries. Nevertheless, the underlying molecular mechanism of grape leafy cotyledon 1 (LEC1) on seedless induction remains intangible. Herein, the morphological changes of ‘Wink’ grape cultivar during berry development in response to GA treatments were recorded. To better comprehend the function of VvLEC1 in grape seedless berry induced by GA, the gene and protein sequence were determined by bioinformatics methods, of which motif elements analysis intimates the potential function in seed development. The expression level of VvLEC1 which was repressed by GA treatment, determined by RT PCR, exhibited highest up-regulation at four weeks after flowering in the seed. Furthermore, VvLEC1, a member of the nuclear factor Y subunit B (NF-YB-type) transcription factor, interacts with five proteins which belong to the NF-YC-type transcription factor by the prediction of protein interaction network, thus indicating their collective effects on the development of grape seed. Our research findings elucidate a novel molecular insight into the role of VvLEC1 responsive to GA in accentuating grapevine seed development, which is crucial for the molecular breeding of high-quality seedless grapes.
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Abbreviations
- LEC1:
-
Leafy cotyledon 1
- GA:
-
Gibberellin acid
- NF-YC:
-
Nuclear factor Y subunit C
- qRT-PCR:
-
Quantitative real time polymerase chain reaction
- WAF:
-
Weeks after full bloom
- cDNA:
-
Coding DNA
- ORF:
-
Open reading frame
- SA:
-
Salicylic acid
- ABA:
-
Abscisic acid
- CBF:
-
CCAAT binding factor
References
Abu-Zahra TR (2010) Berry size of Thompson seedless as influenced by the application of gibberellic acid and can girdling. Pak J Bot 42:1755–1760
Agnieszka L, Gaj MD (2011) LEAFY COTYLEDON1, FUSCA3 expression and auxin treatment in relation to somatic embryogenesis induction in Arabidopsis. Plant Growth Regul 65(1):157–167
Cagliari A, Turchetto-Zolet AC, Korbes AP, Maraschin FS, Margis R et al (2014) New insights on the evolution of Leafy cotyledon1 (LEC1) type genes in vascular plants. Genomics 103:380–387
Champa WAH, Gill MIS, Mahajan BVC, Bedi S (2015) Exogenous treatment of spermine to maintain quality and extend postharvest life of table grapes (Vitis vinifera L.) cv. Flame Seedless under low temperature storage. LWT-Food Sci Technol 60:412–419
Cheng C, Xu X, Singer SD, Li J, Zhang H et al (2013) Effect of GA3 treatment on seed development and seed related gene expression in grape. PLoS ONE 8:e80044
Cheng CX, Jiao C, Singer SD, Gao M, Xu X et al (2015) Gibberellin-induced changes in the transcriptome of grapevine (Vitislabrusca × V. vinifera) cv. Kyoho flowers. BMC Genom 16:128
Coombe BG (1995) Growth stages of the grapevine: adoption of a system for identifying grapevine growth stages. Aust J Grape Wine Res 1:104–110
Depuydt S, Hardtke CS (2011) Hormone signaling crosstalk in plant growth regulation. Curr Biol 21:R365–R373
Dorn A, Bollekens J, Staub A, Benoist C, Mathis D (1987) A multiplicity of CCAAT box-binding proteins. Cell 50:863
Fambrini M, Durante C, Cionini G, Geri C, Giorgetti L et al (2006) Characterization of LEAFY COTYLEDON-LIKE gene in Hwlianthusannuus and relationship with zygotic and somatic embryoaenesis. Dev Genes Evol 216:253–264
Gaj MD, Zhang S, Harada JJ, Lemaux PG (2005) Leafy cotyledon genes are essential for induction of somatic embryogenesis of Arabidopsis. Planta 222:977–988
Jaillon O, Aury JM, Noel B, Policriti A, Clepet C et al (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449:463–467
Jia HF, Jiu ST, Zhang C, Wang C, Tariq P et al (2016) Abscisic acid and sucrose regulate tomato and strawberry fruit ripening through the abscisic acid-stress-ripening transcription factor. Plant Biotechnol J 14:2045–2065
Kwong RW, Bui AQ, Lee H, Kwong LW, Fischer RL et al (2003) LEAFY COTYLEDON1-LIKE defines a class of regulators essential for embryo development. Plant Cell 15:5–18
Letovsky S, Kasif S (2003) Predicting protein function from protein/protein interaction data: a probabilistic approach. Bioinformatics 19:i197
Li XY, Mantovani R, Hooft Van Huijsduijnen R et al (1992) Evolutionary variation of the CCAAT-binding transcription factor NF-Y. Nucleic Acids Res 20:1087–1091
Li A, **a H, Wang X, Li C, Zhao C, Bi Y et al (2009) Cloning and expression analysis of peanut (Arachis hypogaea L.) LEC1. Acta Bot. Boreal Occident Sin 29:1730–1735
Lotan T, Ohto M, Matsudaira Yee K et al (1998) Arabidopsis LEAFY COTYLEDON1 is sufficient to induce embryo development in vegetative cells. Cell 93:1195–1205
Maity SN, Crombrugghe BD (1998) Role of the CCAAT-binding protein CBF/NF-Y in transcription. Trends Biochem Sci 23:174
Meinke DW (1992) A homoeotic mutant of Arabidopsis thaliana with leafy cotyledons. Science 258:1647–1650
Meinke DW, Franzmann LH, Nickle TC et al (1994) Leafy cotyledon mutants of Arabidopsis. Plant Cell 6:1049–1064
Murcia G, Pontin M, Piccoli P (2018) Role of ABA and Gibberellin A3 on gene expression pattern of sugar transporters and invertases in Vitis vinifera cv. Malbec during berry ripening. Plant Growth Regul 84:275–283
Parcy F, Valon C, Kohara A (1997) The ABSCISIC ACID-INSENSITIVE3, FUSCA3, and LEAFY COTYLEDON1 loci act in concert to control multiple aspects of Arabidopsis seed development. Plant Cell 9:1265–1277
Ramakers C, Ruijter JM, Deprez RH et al (2003) Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci Lett 339:62–66
Ren GH, Bilkish N, Zhu XD et al (2014) Cloning, expression, and characterization of miR058 and its target PPO during the development of grapevine berry stone. Gene 548:166–173
Riechmann JL, Ratcliffe OJ (2000) A genomic perspective on plant transcription factors. Curr Opin Plant Biol 3:423–434
Rodyoung A, Masuda Y, Tomiyama H, Saito K et al (2016) Effects of light emitting diode irradiation at night on abscisic acid metabolism and anthocyanin synthesis in grapes in different growing seasons. Plant Growth Regul 79:39–46
Schwechheimer C, Willige BC (2009) Shedding light on gibberellic acid signalling. Curr Opin Plant Biol 12(1):57–62
Singh DP, Jermakow AW, Swain SM (2002) Gibberellins are required for seed development and pollen tube growth in Arabidopsis. Plant Cell 14:3133–3147
Stephenson TJ, Mcintyre CL, Collet C et al (2007) Genome-wide identification and expression analysis of the NF-Y family of transcription factors in Triticum aestivum. Plant Mol Biol 65:77–92
Tamura K, Peterson D, Peterson N, Stecher G, Nei M et al (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739
Upadhyay A, Maske S, Jogaiah S, Kadoo N, Gupta V (2018) GA3, application in grapes (Vitis vinifera, L.) modulates different sets of genes at cluster emergence, full bloom, and berry stage as revealed by RNA sequence-based transcriptome analysis. Funct Integr Genom 18:439–455
Velasco R, Zharkikh A, Troggio M, Cartwright D, Cestaro A et al (2007) A high quality draft consensus sequence of the genome of a heterozygous grapevine variety. PLoS ONE 2:e1326
Venkateswarlu K (2003) Interaction protein for cytohesin exchange factors 1 (IPCEF1) binds cytohesin 2 and modifies its activity. J Biol Chem 278(44):43460–43469
Vicient CM, Bies-Etheve N, Delseny M (2000) Changes in gene expression in the leafy cotyledon1 (lec1) and fusca3 (fus3) mutants of Arabidopsis thaliana L. J Exp Bot 51:995–1003
Wang C, Han J, Liu C, Kibet KN, Kayesh E et al (2012) Identification of microRNAs from Amur grape (Vitis amurensis Rupr.) by deep sequencing and analysis of microRNA variations with bioinformatics. BMC Genom 13:122
Wang C, Leng XP, Zhang YY, Kayesh E, Zhang Y et al (2014) Transcriptome-wide analysis of dynamic variations in regulation modes of grapevine microRNAs on their target genes during grapevine development. Plant Mol Biol 84:269–285
Wang M, Sun X, Wang C, Cui L, Chen L et al (2017) Characterization of miR061 and its target genes in grapevine responding to exogenous gibberellic acid. Funct Integr Genom 17:537–549
West MAL, Yee KM, Danao J, Zimmerman JL, Fischer RL et al (1994) LEAFY COTYLEDON1 is an essential regulator of late embryogenesis and cotyledon identity in Arabidopsis. Plant Cell 6:1731–1745
Yamamoto A, Kagaya Y, Toyoshima R, Kagaya M, Takeda S et al (2009) Arabidopsis NF-YB subunits LEC1 and LEC1-LIKE activate transcription by interacting with seed-specific ABRE-binding factors. Plant J 58:843
Yang S, Wang Y, Yin H, Guo H, Gao M et al (2015) Identification and characterization of NF-YB family genes in tungtree. Mol Genet Genom 290:2187–2198
Yazawa K, Takahata K, Kamada H (2004) Isolation of the gene encoding carrot leafy cotyledon 1 and expression analysis during somatic and zygotic embryogenesis. Plant Physiol Biochem 42:215–223
Zhang S, Wong L, Weng L, Lemaux P (2002) Similarity of expression patterns of knotted and ZmLEC1 during somatic and zygotic embryogenesis in maize. Planta 215:191–194
Zhang W, Abdelrahman M, Jiu S, Guan L et al (2019) (2019) VvmiR160s/VvARFs interaction and their spatio-temporal expression/cleavage products during GA-induced grape parthenocarpy. BMC Plant Biol 19:111
Acknowledgements
This work was supported by a grant from the Central University basic scientific research business fee independent innovation major project (NATURAL SCIENCE) (KYTZ201602), and Key Laboratory of Fruit Breeding Technology, Ministry of Agriculture of China, Zhengzhou, Henan, 450009, P.R. China.
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CW and CL conceived the study and carried out the molecular mechanism analysis. MC and WW cloned and identify the precise sequence of VvLEC1. MC, FG, XF and LG conducted the expression analysis of VvLEC1 in grape berry development stages. TZ, XZ and HJ performed the promoter element analysis of VvLEC1. WW and CW preliminarily validate the activity of VvLEC1 promoters in response to GA. JF predict the interacting proteins of VvLEC1. MC drew the tables and figures. MC and CW drafted the manuscript. CW, JF and CL revised the manuscript. All authors read and approved the final manuscript.
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Mengjie Cui and Wenran Wang are co-first authors.
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Cui, M., Wang, W., Guo, F. et al. Characterization and temporal–spatial expression analysis of LEC1 gene in the development of seedless berries in grape induced by gibberellin. Plant Growth Regul 90, 585–596 (2020). https://doi.org/10.1007/s10725-020-00582-8
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DOI: https://doi.org/10.1007/s10725-020-00582-8