Expression Pattern of FT/TFL1 and miR156-Targeted SPL Genes Associated with Developmental Stages in Dendrobium catenatum
Abstract
:1. Introduction
2. Results
2.1. Sequence Analysis of FT/TFL1 and SPL Family Members in D. catenatum
2.2. DcHd3b Is Highly Expressed in Protocorms and Juvenile Plants
2.3. MiR156 Abundance Correlated Well with Protocorm Germination and Differentiation
2.4. DcSPL3 Is the Only Significantly Upregulated Gene among the SPL Family in Adult Plants
3. Discussion
3.1. Is there a Repression of Competence to Flower by TFL1-Like Genes in D. catenatum?
3.2. MiR156/SPL Involvement in Seedling Development and Maturation in D. catenatum
3.3. Is there a Possible Link between the DcHd3b Pathway and the miR156/DcSPL3 Module in Phase Transition in Dendrobium catenatum?
4. Materials and Methods
4.1. Plant Materials and Growth Conditions
4.2. Gene Identification and Phylogenetic Analysis
4.3. RNA Isolation and Quantitative RT-PCR
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Bergonzi, S.; Albani, M.C. Reproductive competence from an annual and a perennial perspective. J. Exp. Bot. 2011, 62, 4415–4422. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hackett, W.P. Juvenility, maturation and rejuvenation in woody plants. Hortic. Rev. 1985, 7, 109–155. [Google Scholar]
- Corbesier, L.; Vincent, C.; Jang, S.; Fornara, F.; Fan, Q.; Searle, I.; Giakountis, A.; Farrona, S.; Gissot, L.; Turnbull, C.; et al. Ft protein movement contributes to long-distance signaling in floral induction of arabidopsis. Science 2007, 316, 1030–1033. [Google Scholar] [CrossRef] [PubMed]
- Tamaki, S.; Matsuo, S.; Wong, H.L.; Yokoi, S.; Shimamoto, K. Hd3a protein is a mobile flowering signal in rice. Science 2007, 316, 1033–1036. [Google Scholar] [CrossRef] [PubMed]
- Kobayashi, Y.; Kaya, H.; Goto, K.; Iwabuchi, M.; Araki, T. A pair of related genes with antagonistic roles in mediating flowering signals. Science 1999, 286, 1960–1962. [Google Scholar] [CrossRef] [PubMed]
- Wickland, D.P.; Hanzawa, Y. The flowering locus t/terminal flower 1 gene family: Functional evolution and molecular mechanisms. Mol. Plant 2015, 8, 983–997. [Google Scholar] [CrossRef] [PubMed]
- Ahn, J.H.; Miller, D.; Winter, V.J.; Banfield, M.J.; Lee, J.H.; Yoo, S.Y.; Henz, S.R.; Brady, R.L.; Weigel, D. A divergent external loop confers antagonistic activity on floral regulators FT and TFL1. EMBO J. 2006, 25, 605–614. [Google Scholar] [CrossRef]
- Wigge, P.A.; Kim, M.C.; Jaeger, K.E.; Busch, W.; Schmid, M.; Lohmann, J.U.; Weigel, D. Integration of spatial and temporal information during floral induction in Arabidopsis. Science 2005, 309, 1056–1059. [Google Scholar] [CrossRef] [PubMed]
- Higuchi, Y. Florigen and anti-florigen: Flowering regulation in horticultural crops. Breed. Sci. 2018, 68, 109–118. [Google Scholar] [CrossRef]
- Liu, Y.Y.; Yang, K.Z.; Wei, X.X.; Wang, X.Q. Revisiting the phosphatidylethanolamine-binding protein (PEBP) gene family reveals cryptic flowering locus t gene homologs in gymnosperms and sheds new light on functional evolution. New Phytol. 2016, 212, 730–744. [Google Scholar] [CrossRef]
- Hedman, H.; Källman, T.; Lagercrantz, U. Early evolution of the MFT-like gene family in plants. Plant Mol. Biol. 2009, 70, 359–369. [Google Scholar] [CrossRef]
- Karlgren, A.; Gyllenstrand, N.; Källman, T.; Sundström, J.F.; Moore, D.; Lascoux, M.; Lagercrantz, U. Evolution of the PEBP gene family in plants: Functional diversification in seed plant evolution. Plant Physiol. 2011, 156, 1967–1977. [Google Scholar] [CrossRef] [PubMed]
- Taoka, K.; Ohki, I.; Tsuji, H.; Furuita, K.; Hayashi, K.; Yanase, T.; Yamaguchi, M.; Nakashima, C.; Purwestri, Y.A.; Tamaki, S.; et al. 14-3-3 proteins act as intracellular receptors for rice Hd3a florigen. Nature 2011, 476, 332–335. [Google Scholar] [CrossRef] [PubMed]
- Melzer, S.; Lens, F.; Gennen, J.; Vanneste, S.; Rohde, A.; Beeckman, T. Flowering-time genes modulate meristem determinacy and growth form in Arabidopsis thaliana. Nat. Genet. 2008, 40, 1489–1492. [Google Scholar] [CrossRef] [PubMed]
- Lee, J.; Oh, M.; Park, H.; Lee, I. SOC1 translocated to the nucleus by interaction with AGL24 directly regulates leafy. Plant J. 2008, 55, 832–843. [Google Scholar] [CrossRef] [PubMed]
- Lohmann, J.U.; Weigel, D. Building beauty: The genetic control of floral patterning. Dev. Cell 2002, 2, 135–142. [Google Scholar] [CrossRef]
- Randoux, M.; Daviere, J.M.; Jeauffre, J.; Thouroude, T.; Pierre, S.; Toualbia, Y.; Perrotte, J.; Reynoird, J.P.; Jammes, M.J.; Hibrand-Saint Oyant, L.; et al. Roksn, a floral repressor, forms protein complexes with RoFD and RoFT to regulate vegetative and reproductive development in rose. New Phytol. 2014, 202, 161–173. [Google Scholar] [CrossRef]
- Qin, Z.; Bai, Y.; Muhammad, S.; Wu, X.; Deng, P.; Wu, J.; An, H.; Wu, L. Divergent roles of FT-like 9 in flowering transition under different day lengths in brachypodium distachyon. Nat. Commun. 2019, 10, 812. [Google Scholar] [CrossRef]
- Pin, P.A.; Benlloch, R.; Bonnet, D.; Wremerth-Weich, E.; Kraft, T.; Gielen, J.J.; Nilsson, O. An antagonistic pair of FT homologs mediates the control of flowering time in sugar beet. Science 2010, 330, 1397–1400. [Google Scholar] [CrossRef]
- Jung, J.H.; Ju, Y.; Seo, P.J.; Lee, J.H.; Park, C.M. The SOC1-SPl module integrates photoperiod and gibberellic acid signals to control flowering time in Arabidopsis. Plant J. Cell Mol. Biol. 2012, 69, 577–588. [Google Scholar] [CrossRef]
- Yamaguchi, A.; Wu, M.-F.; Yang, L.; Wu, G.; Poethig, R.S.; Wagner, D. The microRNA-regulated SBP-box transcription factor SPL3 is a direct upstream activator of LEAFY, FRUITFULL, and APETALA1. Dev. Cell 2009, 17, 268–278. [Google Scholar] [CrossRef] [PubMed]
- Wang, J.W.; Czech, B.; Weigel, D. Mir156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 2009, 138, 738–749. [Google Scholar] [CrossRef] [PubMed]
- Cui, J.; You, C.; Chen, X. The evolution of micrornas in plants. Curr. Opin. Plant Biol. 2017, 35, 61–67. [Google Scholar] [CrossRef] [PubMed]
- Taylor, R.S.; Tarver, J.E.; Hiscock, S.J.; Donoghue, P.C.J. Evolutionary history of plant micrornas. Trends Plant Sci. 2014, 19, 175–182. [Google Scholar] [CrossRef] [PubMed]
- Rubio-Somoza, I.; Weigel, D. Microrna networks and developmental plasticity in plants. Trends Plant Sci. 2011, 16, 258–264. [Google Scholar] [CrossRef] [PubMed]
- Ha, M.; Kim, V.N. Regulation of microrna biogenesis. Nat. Rev. Mol. Cell Biol. 2014, 15, 509. [Google Scholar] [CrossRef] [PubMed]
- He, J.; Xu, M.; Willmann, M.R.; McCormick, K.; Hu, T.; Yang, L.; Starker, C.G.; Voytas, D.F.; Meyers, B.C.; Poethig, R.S. Threshold-dependent repression of SPL gene expression by mir156/mir157 controls vegetative phase change in Arabidopsis thaliana. PLoS Genet. 2018, 14, e1007337. [Google Scholar] [CrossRef]
- Wu, G.; Park, M.Y.; Conway, S.R.; Wang, J.W.; Weigel, D.; Poethig, R.S. The sequential action of mir156 and mir172 regulates developmental timing in Arabidopsis. Cell 2009, 138, 750–759. [Google Scholar] [CrossRef]
- Wu, G.; Poethig, R.S. Temporal regulation of shoot development in Arabidopsis thaliana by mir156 and its target SPL3. Development 2006, 133, 3539–3547. [Google Scholar] [CrossRef]
- Hou, H.M.; Yan, X.X.; Sha, T.; Yan, Q.; Wang, X.P. The SBP-box gene VpSBP11 from Chinese wild vitis is involved in floral transition and affects leaf development. Int. J. Mol. Sci. 2017, 18, 1493. [Google Scholar] [CrossRef]
- Xu, M.; Hu, T.; Zhao, J.; Park, M.Y.; Earley, K.W.; Wu, G.; Yang, L.; Poethig, R.S. Developmental functions of mir156-regulated squamosa promoter binding protein-like (SPL) genes in Arabidopsis thaliana. PLoS Genet. 2016, 12, e1006263. [Google Scholar] [CrossRef] [PubMed]
- Jung, J.H.; Lee, H.J.; Ryu, J.Y.; Park, C.M. SPL3/4/5 integrate developmental aging and photoperiodic signals into the FT-FD module in Arabidopsis flowering. Mol. Plant 2016, 9, 1647–1659. [Google Scholar] [CrossRef] [PubMed]
- Aukerman, M.J.; Sakai, H. Regulation of flowering time and floral organ identity by a microRNA and its apetala2-like target genes. Plant Cell 2003, 15, 2730–2741. [Google Scholar] [CrossRef] [PubMed]
- Hyun, Y.; Richter, R.; Vincent, C.; Martinez-Gallegos, R.; Porri, A.; Coupland, G. Multi-layered regulation of SPL15 and cooperation with soc1 integrate endogenous flowering pathways at the Arabidopsis shoot meristem. Dev. Cell 2016, 37, 254–266. [Google Scholar] [CrossRef] [PubMed]
- Yamaguchi, N.; Winter, C.M.; Wu, M.F.; Kanno, Y.; Yamaguchi, A.; Seo, M.; Wagner, D. Gibberellin acts positively then negatively to control onset of flower formation in Arabidopsis. Science 2014, 344, 638–641. [Google Scholar] [CrossRef] [PubMed]
- Xu, H.; Liu, Q.; Yao, T.; Fu, X. Shedding light on integrative GA signaling. Curr. Opin. Plant Biol. 2014, 21, 89–95. [Google Scholar] [CrossRef] [PubMed]
- Yu, S.; Galvao, V.C.; Zhang, Y.C.; Horrer, D.; Zhang, T.Q.; Hao, Y.H.; Feng, Y.Q.; Wang, S.; Schmid, M.; Wang, J.W. Gibberellin regulates the Arabidopsis floral transition through mir156-targeted squamosa promoter binding-like transcription factors. Plant Cell 2012, 24, 3320–3332. [Google Scholar] [CrossRef]
- da Silva, J.A.T.; Aceto, S.; Liu, W.; Yu, H.; Kanno, A. Genetic control of flower development, color and senescence of Dendrobium orchids. Sci. Hortic-Amst. 2014, 175, 74–86. [Google Scholar] [CrossRef]
- Wang, Y.; Liu, L.; Song, S.; Li, Y.; Shen, L.; Yu, H. DOFT and DOFTIP1 affect reproductive development in the orchid Dendrobium chao praya smile. J. Exp. Bot. 2017, 68, 5759–5772. [Google Scholar] [CrossRef]
- Hou, C.J.; Yang, C.H. Functional analysis of FT and TFL1 orthologs from orchid (oncidium gower ramsey) that regulate the vegetative to reproductive transition. Plant Cell Physiol. 2009, 50, 1544–1557. [Google Scholar] [CrossRef]
- Wang, H.-M.; Tong, C.-G.; Jang, S. Current progress in orchid flowering/flower development research. Plant Signal Behav. 2017, 12, e1322245. [Google Scholar] [CrossRef] [Green Version]
- Zhang, G.Q.; Xu, Q.; Bian, C.; Tsai, W.C.; Yeh, C.M.; Liu, K.W.; Yoshida, K.; Zhang, L.S.; Chang, S.B.; Chen, F.; et al. The Dendrobium catenatum lindl. Genome sequence provides insights into polysaccharide synthase, floral development and adaptive evolution. Sci. Rep. 2016, 6, 19029. [Google Scholar] [CrossRef] [PubMed]
- Ho, W.W.; Weigel, D. Structural features determining flower-promoting activity of Arabidopsis flowering locus T. Plant Cell 2014, 26, 552–564. [Google Scholar] [CrossRef] [PubMed]
- Preston, J.C.; Hileman, L.C. Functional evolution in the plant squamosa-promoter binding protein-like (SPL) gene family. Front. Plant Sci. 2013, 4, 80. [Google Scholar] [CrossRef] [PubMed]
- Meng, Y.; Yu, D.; Xue, J.; Lu, J.; Feng, S.; Shen, C.; Wang, H. A transcriptome-wide, organ-specific regulatory map of Dendrobium officinale, an important traditional Chinese orchid herb. Sci. Rep. 2016, 6, 18864. [Google Scholar] [CrossRef] [PubMed]
- Hyun, Y.; Richter, R.; Coupland, G. Competence to flower: Age-controlled sensitivity to environmental cues. Plant Physiol. 2017, 173, 36–46. [Google Scholar] [CrossRef] [PubMed]
- Mouhu, K.; Kurokura, T.; Koskela, E.A.; Albert, V.A.; Elomaa, P.; Hytonen, T. The fragaria vesca homolog of suppressor of overexpression of constans1 represses flowering and promotes vegetative growth. Plant Cell 2013, 25, 3296–3310. [Google Scholar] [CrossRef] [PubMed]
- Gandikota, M.; Birkenbihl, R.P.; Hohmann, S.; Cardon, G.H.; Saedler, H.; Huijser, P. The miRNA156/157 recognition element in the 3′ UTR of the Arabidopsis SBP box gene SPL3 prevents early flowering by translational inhibition in seedlings. Plant J. Cell Mol. Biol. 2007, 49, 683–693. [Google Scholar] [CrossRef] [PubMed]
- Xie, K.; Wu, C.; Xiong, L. Genomic organization, differential expression, and interaction of squamosa promoter-binding-like transcription factors and microrna156 in rice. Plant Physiol. 2006, 142, 280–293. [Google Scholar] [CrossRef]
- Yu, N.; Cai, W.J.; Wang, S.; Shan, C.M.; Wang, L.J.; Chen, X.Y. Temporal control of trichome distribution by microrna156-targeted SPL genes in Arabidopsis thaliana. Plant Cell 2010, 22, 2322–2335. [Google Scholar] [CrossRef]
- Wang, J.W.; Park, M.Y.; Wang, L.J.; Koo, Y.; Chen, X.Y.; Weigel, D.; Poethig, R.S. Mirna control of vegetative phase change in trees. PLoS Genet. 2011, 7, e1002012. [Google Scholar] [CrossRef] [PubMed]
- Bergonzi, S.; Albani, M.C.; Ver Loren van Themaat, E.; Nordstrom, K.J.; Wang, R.; Schneeberger, K.; Moerland, P.D.; Coupland, G. Mechanisms of age-dependent response to winter temperature in perennial flowering of Arabis alpina. Science 2013, 340, 1094–1097. [Google Scholar] [CrossRef] [PubMed]
- Zhang, G.Q.; Liu, K.W.; Li, Z.; Lohaus, R.; Hsiao, Y.Y.; Niu, S.C.; Wang, J.Y.; Lin, Y.C.; Xu, Q.; Chen, L.J.; et al. The apostasia genome and the evolution of orchids. Nature 2017, 549, 379–383. [Google Scholar] [CrossRef] [PubMed]
- Cai, J.; Liu, X.; Vanneste, K.; Proost, S.; Tsai, W.C.; Liu, K.W.; Chen, L.J.; He, Y.; Xu, Q.; Bian, C.; et al. The genome sequence of the orchid Phalaenopsis equestris. Nat. Genet. 2015, 47, 65–72. [Google Scholar] [CrossRef] [PubMed]
- Varkonyi-Gasic, E. Stem-loop QRT-PCR for the detection of plant micrornas. Methods Mol. Biol. 2017, 1456, 163–175. [Google Scholar]
- Schmittgen, T.D.; Livak, K.J. Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc. 2008, 3, 1101–1108. [Google Scholar] [CrossRef] [PubMed]
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Zheng, J.; Ma, Y.; Zhang, M.; Lyu, M.; Yuan, Y.; Wu, B. Expression Pattern of FT/TFL1 and miR156-Targeted SPL Genes Associated with Developmental Stages in Dendrobium catenatum. Int. J. Mol. Sci. 2019, 20, 2725. https://doi.org/10.3390/ijms20112725
Zheng J, Ma Y, Zhang M, Lyu M, Yuan Y, Wu B. Expression Pattern of FT/TFL1 and miR156-Targeted SPL Genes Associated with Developmental Stages in Dendrobium catenatum. International Journal of Molecular Sciences. 2019; 20(11):2725. https://doi.org/10.3390/ijms20112725
Chicago/Turabian StyleZheng, Jie, Yuru Ma, Mengyao Zhang, Meiling Lyu, Yuan Yuan, and Binghua Wu. 2019. "Expression Pattern of FT/TFL1 and miR156-Targeted SPL Genes Associated with Developmental Stages in Dendrobium catenatum" International Journal of Molecular Sciences 20, no. 11: 2725. https://doi.org/10.3390/ijms20112725