Transcriptomic Identification of Floral Transition and Development-Associated Genes in Styrax japonicus
Abstract
:1. Introduction
2. Materials and Methods
3. Results
3.1. Differential Gene Expression during Floral Development
3.2. GO and KEGG Annotation of DEGs
3.3. Differential Expression of Transcription Factors and Protein Kinases
3.4. Transcriptome Analysis of Phytohormone Pathway Genes during Flower Development
3.5. RT-qPCR Validation of Selected Flowering-Related Genes
4. Discussion
4.1. Transcription Factors Associated with Floral Development
4.2. Time-Associated Gene Expression during S. japonicus Flowering
4.3. Identification of Hormone Unigenes Related to Flowering Stage
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Wang, X.Y.; Yu, S.; Liu, M.; Yang, Q.-S.; Chen, X.-Y. Twenty-three microsatellite loci for Styrax confusus and Styrax japonicus (Styracaceae). Conserv. Genet. Resour. 2010, 2, 51–54. [Google Scholar] [CrossRef]
- Li, W.; Zhang, C.P.; Jiang, X.Q.; Liu, Q.C.; Liu, Q.H.; Wang, K. De Novo Transcriptomic Analysis and Development of EST–SSRs for Styrax japonicus. Forests 2018, 9, 748. [Google Scholar] [CrossRef] [Green Version]
- Arabidopsis Genome Initiative. Analysis of the genome sequence of the flowering plant. Nature 2000, 408, 796–815. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ramsey, J.; Schemske, D.W. Pathways, Mechanisms, and Rates of Polyploid Formation in Flowering Plants. Annu. Rev. Ecol. Syst. 1998, 29, 467–501. [Google Scholar] [CrossRef] [Green Version]
- Zhang, X.; Zhang, J.; Jie, Z.; Zhao, J.; Ren, X. Function of protein ubiquitination and SUMOylation in regulating flowering time of plants: A review. J. Zhejiang Univ. 2015, 41, 371–384. [Google Scholar]
- Mizoguchi, T. Distinct Roles of GIGANTEA in Promoting Flowering and Regulating Circadian Rhythms in Arabidopsis. Plant Cell 2005, 17, 2255–2270. [Google Scholar] [CrossRef] [Green Version]
- Imaizumi, T.; Tran, H.G.; Swartz, T.E.; Briggs, W.R.; Kay, S.A. FKF1 is essential for photoperiodic-specific light signalling in Arabidopsis. Nature 2003, 426, 302–306. [Google Scholar] [CrossRef]
- Morris, K.; Jackson, S.P. DAY NEUTRAL FLOWERING does not act through GIGANTEA and FKF1 to regulate CONSTANS expression and flowering time. Plant Signal. Behav. 2010, 5, 1105–1107. [Google Scholar] [CrossRef] [Green Version]
- Han, P.; García-Ponce, B.; Fonseca-Salazar, G.; Alvarez-Buylla, E.R.; Yu, H. AGAMOUS-LIKE 17, a novel flowering promoter, acts in a FT-independent photoperiod pathway. Plant J. 2008, 55, 253. [Google Scholar] [CrossRef]
- Kim, D.H.; Doyle, M.R.; Sung, S.; Amasino, R.M. Vernalization: Winter and the Timing of Flowering in Plants. Annu. Rev. Cell Dev. Biol. 2009, 25, 277–299. [Google Scholar] [CrossRef] [Green Version]
- Mutasa-Gottgens, E.; Qi, A.; Mathews, A.; Thomas, S.; Phillips, A.; Hedden, P. Modification of gibberellin signalling (metabolism & signal transduction) in sugar beet: Analysis of potential targets for crop improvement. Transgenic Res. 2009, 18, 301–308. [Google Scholar] [PubMed]
- Foley, M.E.; Anderson, J.V.; Horvath, D.P. The effects of temperature, photoperiod, and vernalization on regrowth and flowering competence in Euphorbia esula (Euphorbiaceae) crown buds. Botany 2009, 87, 986–992. [Google Scholar] [CrossRef] [Green Version]
- An, L.; Jin, L.; Yang, C.; Li, T. Effect and Functional Mechanism of Exogenous Gibberellin on Flowering of Peach. Sci. Agric. Sin. 2009, 42, 605–611. [Google Scholar]
- Liu, K.; Feng, S.; Pan, Y.; Zhong, J.; Chen, Y.; Yuan, C.; Li, H. Transcriptome Analysis and Identification of Genes Associated with Floral Transition and Flower Development in Sugar Apple (Annona squamosa L.). Front. Plant Sci. 2016, 7, 1695. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, D.; Ren, L.; Yue, J.H.; Wang, L.; Shen, X.H. GA4 and IAA were involved in the morphogenesis and development of flowers in Agapanthus praecox ssp. orientalis. J. Plant Physiol. 2014, 171, 966–976. [Google Scholar] [CrossRef] [PubMed]
- Bohlenius, H. CO/FT Regulatory Module Controls Timing of Flowering and Seasonal Growth Cessation in Trees. Science 2007, 312, 1040–1043. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cheng, X.F. Overexpression of COL9, a CONSTANS-LIKE gene, delays flowering by reducing expression of CO and FT in Arabidopsis thaliana. Plant J. 2010, 43, 758–768. [Google Scholar] [CrossRef]
- Li, J.X.; Hou, X.J.; Zhu, J.; Zhou, J.J.; Huang, H.B.; Yue, J.Q.; Gao, J.Y.; Du, Y.X.; Hu, C.X.; Hu, C.G.; et al. Identification of Genes Associated with Lemon Floral Transition and Flower Development during Floral Inductive Water Deficits: A Hypothetical Model. Front. Plant Sci. 2017, 8, 1013. [Google Scholar] [CrossRef] [Green Version]
- Mao, Y.; Liu, W.; Chen, X.; Xu, Y.; Lu, W.; Hou, J.; Ni, J.; Wang, Y.; Wu, L. Flower Development and Sex Determination between Male and Female Flowers in Vernicia fordii. Front. Plant Sci. 2017, 8, 1291. [Google Scholar] [CrossRef] [Green Version]
- Liu, H.; Fu, J.; Du, H.; Hu, J.; Wuyun, T. De novo sequencing of Eucommia ulmoides flower bud transcriptomes for identification of genes related to floral development. Genom. Data 2016, 9, 105–110. [Google Scholar] [CrossRef] [Green Version]
- Grabherr, M.G.; Haas, B.J.; Yassour, M.; Levin, J.Z.; Thompson, D.A.; Amit, I.; Adiconis, X.; Fan, L.; Raychowdhury, R.; Zeng, Q. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotechnol. 2011, 29, 644–652. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Langdon, B.W. Performance of genetic programming optimised Bowtie2 on genome comparison and analytic testing (GCAT) benchmarks. Biodata Min. 2015, 8, 1. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wainer, H.; Sireci, S.G.; Thissen, D. Differential Testlet Functioning: Definitions and Detection. J. Educ. Meas. 1991, 28, 197–219. [Google Scholar] [CrossRef]
- Trapnell, C.; Williams, B.A.; Pertea, G.; Mortazavi, A.; Kwan, G.; van Baren, M.J.; Salzberg, S.L.; Wold, B.J.; Pachter, L. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 2010, 28, 511–515. [Google Scholar] [CrossRef] [Green Version]
- Livak, K.; Schmittgen, T. Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−△△Ct Method. Methods 2000, 25, 402–408. [Google Scholar] [CrossRef]
- Mao, X.; Tao, C.; Olyarchuk, J.G.; Wei, L. Automated genome annotation and pathway identification using the KEGG Orthology (KO) as a controlled vocabulary. Bioinformatics 2005, 21, 3787–3793. [Google Scholar] [CrossRef]
- Kato, R.; Fujii, T. Increase in the Activities of Protein Kinases under a Flower-Inducing Condition in Lemna paucicostata. Plant Cell Physiol. 1988, 29, 85–88. [Google Scholar]
- Lease, K.A.; Lau, N.Y.; Schuster, R.A.; Torii, K.U.; Walker, J.C. Receptor serine/threonine protein kinases in signalling: Analysis of the erecta receptor-like kinase of Arabidopsis thaliana. New Phytol. 2001, 151, 133–143. [Google Scholar] [CrossRef]
- Vimolmangkang, S.; Han, Y.; Wei, G.; Korban, S.S. An apple MYB transcription factor, MdMYB3, is involved in regulation of anthocyanin biosynthesis and flower development. BMC Plant Biol. 2013, 13, 176. [Google Scholar] [CrossRef] [Green Version]
- Browse, M.J. MyB108 Acts Together with MyB24 to Regulate Jasmonate-Mediated Stamen Maturation in Arabidopsis. Plant Physiol. 2009, 149, 851–862. [Google Scholar]
- Takos, A.M.; Jaffe, F.W.; Jacob, S.R.; Bogs, J.; Robinson, S.P.; Walker, A.R. Light-Induced Expression of a MYB Gene Regulates Anthocyanin Biosynthesis in Red Apples. Plant Physiol. 2006, 142, 1216–1232. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liu, Q.; Zhanchao, W.; Xuemei, X.; Haizhen, Z.; Chenghao, L.; Manoj, P. Genome-Wide Analysis of C2H2 Zinc-Finger Family Transcription Factors and Their Responses to Abiotic Stresses in Poplar (Populus trichocarpa). PLoS ONE 2015, 10, e0134753. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liu, Q.N.; Liu, Y.; Xin, Z.-Z.; Zhang, D.-Z.; Ge, B.-M.; Yang, R.-P.; Wang, Z.-F.; Yang, L.; Tang, B.-P.; Zhou, C.-L. Genome-wide identification and characterization of the WRKY gene family in potato (Solanum tuberosum). Biochem. Syst. Ecol. 2017, 71, 212–218. [Google Scholar] [CrossRef]
- Yu, Y.; Liu, Z.; Wang, L.; Kim, S.G.; Xiang, F. WRKY71 accelerates flowering via the direct activation of FLOWERING LOCUS T and LEAFY in Arabidopsis thaliana. Plant J. 2015, 85, 96–106. [Google Scholar] [CrossRef] [Green Version]
- Halliday, K.J.; Praekelt, U.M.; Salter, M.G.; Whitelam, G.C. Functions and Actions of Arabidopsis Phytochromes; Springer: Boston, MA, USA, 2001. [Google Scholar]
- Imaizumi, T. Arabidopsis circadian clock and photoperiodism: Time to think about location. Curr. Opin. Plant Biol. 2010, 13, 83–89. [Google Scholar] [CrossRef] [Green Version]
- Tiyayon, P.; Hegele, M.; Wünsche, J.N.; Pongsriwat, K.; Samach, A. Studies on the molecular basis of flowering in longan (Dimocarpus longan). Acta Hortic. 2011, 903, 979–985. [Google Scholar] [CrossRef]
- Zhu, L.; Doyle, T.J.; Kim, K.H. Retinoic Acid Modulates the Subcellular Localization of Small Ubiquitin-Related Modifier-2/3 (SUMO-2/3) in the Testis. J. Androl. 2010, 31, 406–418. [Google Scholar] [CrossRef]
- Murakami-Kojima, M. The APRR3 Component of the Clock-Associated APRR1/TOC1 Quintet is Phosphorylated by a Novel Protein Kinase Belonging to the WNK Family, the Gene for which is also Transcribed Rhythmically in Arabidopsis thaliana. Plant Cell Physiol. 2002, 43, 675–683. [Google Scholar] [CrossRef] [Green Version]
- Marquardt, S.; Boss, P.; Hadfield, J.; Dean, C. Additional targets of the Arabidopsis autonomous pathway members, FCA and FY. J. Exp. Bot. 2006, 57, 3379–3386. [Google Scholar] [CrossRef]
- Hong, J.K.; Kim, J.A.; Lee, S.I.; Suh, E.J.; Chang, A.; Koo, B.S.; Lee, Y.-H. Flowering Time Genes and Application in Crops. Korean J. Breed. Sci. 2013, 45, 303–310. [Google Scholar] [CrossRef] [Green Version]
- Domagalska, M.A.; Schomburg, F.M.; Amasino, R.M.; Vierstra, R.D.; Nagy, F.; Davis, S.J. Attenuation of brassinosteroid signaling enhances FLC expression and delays flowering. Development 2007, 134, 2841–2850. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hou, J.; Yan, L.; Harsh, R.; Zou, X.; Jing, W.; Dai, S.; Xiao, Q.; Cong, L.; Fan, L.; Liu, B. A Tourist -like MITE insertion in the upstream region of the BnFLC.A10 gene is associated with vernalization requirement in rapeseed (Brassica napus L). BMC Plant Biol. 2012, 12, 238. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Alabadí, D.; Blázquez, M.A. Molecular interactions between light and hormone signaling to control plant growth. Plant Mol. Biol. 2009, 69, 409–417. [Google Scholar] [CrossRef] [PubMed]
- Gallego-Bartolome, J.; Minguet, E.G.; Grau-Enguix, F.; Abbas, M.; Locascio, A.; Thomas, S.G.; Alabadi, D.; Blazquez, M.A. Molecular mechanism for the interaction between gibberellin and brassinosteroid signaling pathways in Arabidopsis. Proc. Natl. Acad. Sci. USA 2012, 109, 13446–13451. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhao, L.; Kim, Y.J.; Dinh, T.T.; Chen, X. miR172 regulates stem cell fate and defines the inner boundary of APETALA3 and PISTILLATA expression domain in Arabidopsis floral meristems. Plant J. 2007, 51, 840–849. [Google Scholar] [CrossRef] [Green Version]
- Krizek, B.A. Aintegumenta and Aintegumenta-Like6 regulate auxin-mediated flower development in Arabidopsis. BMC Res. Notes 2011, 4, 176. [Google Scholar] [CrossRef] [Green Version]
- Aloni, R.; Aloni, E.; Langhans, M.; Ullrich, C.I. Role of auxin in regulating Arabidopsis flower development. Planta 2005, 223, 315–328. [Google Scholar] [CrossRef]
- Luca, C.; Simona, M.; Dola, S.R.; Stefano, B.; Irma, R.-V.; Anicet, D.F.; Klaus, P.; Rüdiger, S.; Lucia, C.; Markus, G. Maternal Control of PIN1 Is Required for Female Gametophyte Development in Arabidopsis. PLoS ONE 2013, 8, e66148. [Google Scholar]
- Ottenschläger. Gravity Regulated Differential Auxin Transport in Arabidopsis Roots and the Search for Interaction Partners of AtPIN1. Ph.D. Thesis, University of Cologne, Cologne, Germany, 2002.
- Naor, V.; Kigel, J.; Ziv, M. effect of Gibberellin and cytokinin on floral development in Zantedeschia spp. in vivo and in vitro. Acta Hortic. 2005, 673, 255–263. [Google Scholar] [CrossRef]
- Sheerin, D.J.; Buchanan, J.; Kirk, C.; Harvey, D.; Spagnuolo, J. Inter- and intra-molecular interactions of Arabidopsis thalianaDELLA protein RGL1. Biochem. J. 2011, 435, 629–639. [Google Scholar] [CrossRef] [Green Version]
- Su, W.R.; Huang, K.-L.; Shen, R.-S.; Chen, W.-S. Abscisic acid affects floral initiation in Polianthes tuberosa. J. Plant Physiol. 2002, 159, 557–559. [Google Scholar] [CrossRef]
- D’Aloia, M.; Bonhomme, D.; Bouché, F.; Tamseddak, K.; Périlleux, C. Cytokinin promotes flowering of Arabidopsis via transcriptional activation of the FT paralogue TSF. Plant J. 2011, 65, 972–979. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pearce, S.; Huttly, A.K.; Prosser, I.M.; Li, Y.D.; Phillips, A.L. Heterologous expression and transcript analysis of gibberellin biosynthetic genes of grasses reveals novel functionality in the GA3ox family. BMC Plant Biol. 2015, 15, 130. [Google Scholar] [CrossRef] [PubMed] [Green Version]
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Li, W.; Xu, Z.; Zhang, C.; Jiang, X.; Wang, K. Transcriptomic Identification of Floral Transition and Development-Associated Genes in Styrax japonicus. Forests 2020, 11, 10. https://doi.org/10.3390/f11010010
Li W, Xu Z, Zhang C, Jiang X, Wang K. Transcriptomic Identification of Floral Transition and Development-Associated Genes in Styrax japonicus. Forests. 2020; 11(1):10. https://doi.org/10.3390/f11010010
Chicago/Turabian StyleLi, Wei, Zhengzhao Xu, Cuiping Zhang, Xinqiang Jiang, and Kuiling Wang. 2020. "Transcriptomic Identification of Floral Transition and Development-Associated Genes in Styrax japonicus" Forests 11, no. 1: 10. https://doi.org/10.3390/f11010010
APA StyleLi, W., Xu, Z., Zhang, C., Jiang, X., & Wang, K. (2020). Transcriptomic Identification of Floral Transition and Development-Associated Genes in Styrax japonicus. Forests, 11(1), 10. https://doi.org/10.3390/f11010010