Morphological Characterization of Flower Buds Development and Related Gene Expression Profiling at Bud Break Stage in Heterodichogamous Cyclocarya paliurus (Batal.) lljinskaja
Tóm tắt
Cyclocarya paliurus (Batal.) Iljinskaja, a unique species growing in southern China, is a multi-function tree species with medicinal, healthcare, material, and ornamental values. So far, sexual reproduction is the main method for extensive cultivation of C. paliurus plantations, but this is limited by low seed plumpness resulted from the character of heterodichogamy. Phenological observations have revealed the asynchronism of flower development in this species. However, its molecular mechanism remains largely unknown. To reveal molecular mechanism of heterodichogamy in C. paliurus, transcriptome of female (F) and male (M) buds from two mating types (protandry, PA; protogyny, PG) at bud break stage were sequenced using Illumina Hiseq 4000 platform. The expression patterns of both 32 genes related to flowering and 58 differentially expressed transcription factors (DETFs) selected from 6 families were divided four groups (PG-F, PG-M, PA-F, and PA-M) into two categories: first flowers (PG-F and PA-M) and later flowers (PA-F and PG-M). The results indicated that genes related to plant hormones (IAA, ABA, and GA) synthesis and response, glucose metabolism, and transcription factors (especially in MIKC family) played significant roles in regulating asynchronism of male and female flowers in the same mating type. The expression of DETFs showed two patterns. One contained DETFs up-regulated in first flowers in comparison to later flowers, and the other was the reverse. Nine genes related to flowering were selected for qRT-PCR to confirm the accuracy of RNA-seq, and generally, the RPKM values of these genes were consistent with the result of qRT-PCR. The results of this work could improve our understanding in asynchronism of floral development within one mating type in C. paliurus at transcriptional level, as well as lay a foundation for further study in heterodichogamous plants.
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Tài liệu tham khảo
Kikuchi, 2009, Analysis of the disassortative mating pattern in a heterodichogamous plant, Acer mono Maxim. using microsatellite markers, Plant Ecol., 204, 43, 10.1007/s11258-008-9564-1
Liu, 2016, Molecular mechanism of controlling flower formation by photoperiod inducement in plants, J. Nanjing For. Univ., 40, 147
Fukuhara, 2014, Inflorescence dimorphism, heterodichogamy and thrips pollination in Platycarya strobilacea (Juglandaceae), Ann. Bot., 113, 467, 10.1093/aob/mct278
Yin, 2013, Growth and triterpenic acid accumulation of Cyclocarya paliurus cell suspension cultures, Biotechnol. Bioprocess Eng., 18, 606, 10.1007/s12257-012-0751-5
Yang, 2018, Pentacyclic triterpenoids from Cyclocarya paliurus and their antioxidant activities in FFA-induced HepG2 steatosis cells, Phytochemistry, 151, 119, 10.1016/j.phytochem.2018.03.010
Ning, 2019, Identification of α-glucosidase inhibitors from: Cyclocarya paliurus tea leaves using UF-UPLC-Q/TOF-MS/MS and molecular docking, Food Funct., 10, 1893, 10.1039/C8FO01845F
Xie, 2018, Protective effect of flavonoids from Cyclocarya paliurus leaves against carbon tetrachloride-induced acute liver injury in mice, Food Chem. Toxicol., 119, 392, 10.1016/j.fct.2018.01.016
Li, X.C., Fu, X.X., Shang, X.L., Yang, W.X., and Fang, S.Z. (2017). Natural population structure and genetic differentiation for heterodicogamous plant: Cyclocarya paliurus (Batal.) Iljinskaja (Juglandaceae). Tree Genet. Genomes, 13.
Mao, 2016, Flowering biological characteristics and mating system in immature plantations of heterodichogamous Cyclocarya paliurus, J. Nanjing For. Univ., 40, 47
Mao, X., Fu, X.X., Huang, P., Chen, X.L., and Qu, Y.Q. (2019). Heterodichogamy, pollen viability, and seed set in a population of polyploidy Cyclocarya paliurus (Batal) Iljinskaja (Juglandaceae). Forests, 10.
Fu, 2010, Observation on flowering habits and anatomy of stamen development in Cyclocarya paliurus, J. Nanjing For. Univ., 34, 67
Fu, 2011, Observation of morphological and anatomical characters on staminate and pistillate flower differentiation in Cyclocarya paliurus, J. Nanjing For. Univ., 35, 17
Sun, Y.Y., Wang, G.D., Li, Y.X., Jiang, L., Yang, Y.X., and Guan, S.X. (2016). De novo transcriptome sequencing and comparative analysis to discover genes related to floral development in Cymbidium faberi Rolfe. SpringerPlus, 5.
Fornara, F., De Montaigu, A., and Coupland, G. (2010). SnapShot: Control of Flowering in Arabidopsis. Cell, 141.
King, 2006, Regulation of flowering in the long-day grass Lolium temulentum by gibberellins and the FLOWERING LOCUS T gene, Plant Physiol., 141, 498, 10.1104/pp.106.076760
Wang, 2008, Application of Arabidopsis AGAMOUS second intron for the engineered ablation of flower development in transgenic tobacco, Plant Cell Rep., 27, 251, 10.1007/s00299-007-0450-4
Zhang, 2008, Overexpression of the cucumber LEAFY homolog CFL and hormone treatments alter flower development in gloxinia (Sinningia speciosa), Plant Mol. Biol., 67, 419, 10.1007/s11103-008-9330-8
2016, Hormonal control of the development of the gynoecium, Curr. Opin. Plant Biol., 29, 104, 10.1016/j.pbi.2015.12.006
Bowman, 2012, The ABC model of flower development: Then and now, Development, 139, 4095, 10.1242/dev.083972
Gomez, 2015, Anther and pollen development: A conserved developmental pathway, J. Integr. Plant Biol., 57, 876, 10.1111/jipb.12425
Pajoro, 2014, The (r)evolution of gene regulatory networks controlling Arabidopsis plant reproduction: A two decades history, J. Exp. Bot., 65, 4731, 10.1093/jxb/eru233
Vito, 1985, Pistillate flower differentiation in English walnut (Juglans regia L.): A development basis for heterodichogamy, Scientia Horticulturae, 26, 333, 10.1016/0304-4238(85)90017-2
Bai, 2007, Mating patterns and pollen dispersal in a heterodichogamous tree, Juglans mandshurica (Juglandaceae), New Phytol., 176, 699, 10.1111/j.1469-8137.2007.02202.x
Polito, 1997, The relationship between phenology of pistillate flower organogenesis and mode of heterodichogamy in Juglans regia L. (Juglandaceae), Sex. Plant Reprod., 10, 36, 10.1007/s004970050065
Huang, 2018, Dynamic changes of nutrients during flora development in heterodichogamous Cyclocarya paliurus, J. Nanjing For. Univ., 42, 1
Zhang, 2019, Cyclocarya paliurus triterpenic acids fraction attenuates kidney injury via AMPK-mTOR-regulated autophagy pathway in diabetic rats, Phytomedicine, 64, 153060, 10.1016/j.phymed.2019.153060
Yang, 2019, Effects of Cyclocarya paliurus polysaccharide on lipid metabolism-related genes DNA methylation in rats, Int. J. Biol. Macromol., 123, 343, 10.1016/j.ijbiomac.2018.11.110
Xuan, 2019, Cyclocarioside O-Q, three novel seco-dammarane triterpenoid glycosides from the leaves of Cyclocarya paliurus, Nat. Prod. Res., 14, 1
Zhou, 2019, Phytochemical content and antioxidant activity in aqueous extracts of Cyclocarya paliurus leaves collected from different populations, PeerJ, 2019, 1
Li, 1965, A study on the developmental characteristics of walnut buds, Acta Hortic. Sin., 4, 61
Grabherr, 2011, Full-length transcriptome assembly from RNA-Seq data without a reference genome, Nat. Biotechnol., 29, 644, 10.1038/nbt.1883
Altschul, S.F., Madden, T.L., Schäffer, A.A., Zhang, J.H., Zhang, Z., Miller, W., and Lipman, D.J. (1997). Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res.
Anders, S., and Huber, W. (2010). Differential expression analysis for sequence count data. Genome Biol., 11.
Liu, 2018, Light quality affects flavonoid production and related gene expression in Cyclocarya paliurus, J. Photochem. Photobiol. B Biol., 179, 66, 10.1016/j.jphotobiol.2018.01.002
He, H.H., Liang, G.P., Lu, S.X., Wang, P.P., Liu, T., Ma, Z.H., Zuo, C.W., Sun, X.M., Chen, B.H., and Mao, J. (2019). Genome-Wide Identification and Expression Analysis of GA2ox, GA3ox, and GA20ox Are Related to Gibberellin Oxidase Genes in Grape (Vitis vinifera L.). Genes, 10.
Huang, Y., Jiao, Y., Xie, N., Guo, Y., Zhang, F., Xiang, Z., Wang, R., Wang, F., Gao, Q., and Tian, L. (2019). OsNCED5, a 9-cis-epoxycarotenoid dioxygenase gene, regulates salt and water stress tolerance and leaf senescence in rice. Plant Sci., 287.
Pidal, 2009, The CArG-box located upstream from the transcriptional start of wheat vernalization gene VRN1 is not necessary for the vernalization response, J. Hered., 100, 355, 10.1093/jhered/esp002
Yu, D., Qanmber, G., Lu, L., Wang, L., Li, J., Yang, Z., Liu, Z., Li, Y., Chen, Q., and Mendu, V. (2018). Genome-wide analysis of cotton GH3 subfamily II reveals functional divergence in fiber development, hormone response and plant architecture. BMC Plant Biol., 18.
Cortleven, 2015, Regulation of chloroplast development and function by cytokinin, J. Exp. Bot., 66, 4999, 10.1093/jxb/erv132
Chen, H.J., Fu, T.Y., Yang, S.L., and Hsieh, H.L. (2018). FIN219/JAR1 and cryptochrome1 antagonize each other to modulate photomorphogenesis under blue light in Arabidopsis. PLoS Genet., 14.
Pokotylo, I., Kravets, V., and Ruelland, E. (2019). Salicylic Acid Binding Proteins (SABPs): The Hidden Forefront of Salicylic Acid Signalling. Int. J. Mol. Sci., 20.
Hung, 2019, The LDL1/2-HDA6 histone modification complex interacts with TOC1 and regulates the core circadian clock components in Arabidopsis, Front. Plant Sci., 10, 1, 10.3389/fpls.2019.00233
Golicz, A.A. (2019). Analysis of the quinoa genome reveals conservation and divergence of the flowering pathways. Funct. Integr. Genom., 1–14.
Granot, 2014, Substantial roles of hexokinase and fructokinase in the effects of sugars on plant physiology and development, J. Exp. Bot., 65, 809, 10.1093/jxb/ert400
Sung, S.S., Xu, D.P., Galloway, C.M., and Black, C.C. (1988). A reassessment of glycolysis and gluconeogenesis in higher plants. Physiol. Plant., 72.
Arro, 2019, RNA-Seq reveals new della targets and regulation in transgenic GA-insensitive grapevines, BMC Plant Biol., 19, 1, 10.1186/s12870-019-1675-4
2017, Modulation of CycD3;1-CDK complexes by phytohormones and sucrose during maize germination, Physiol. Plant, 160, 84, 10.1111/ppl.12537
Roca, 2012, Quantitative levels of Deficiens and Globosa during late petal development show a complex transcriptional network topology of B function, Plant J., 72, 294, 10.1111/j.1365-313X.2012.05080.x
Wen, J., Guo, P., Ke, Y., Liu, M., Li, P., Wu, Y., Ran, F., Wang, M., Li, J., and Du, H. (2019). The auxin response factor gene family in allopolyploid Brassica napus. PLoS ONE, 14.
Kruger, 2003, Von The oxidative pentose phosphate pathway: Structure and organization, Curr. Opin. Plant Biol., 6, 236, 10.1016/S1369-5266(03)00039-6
Singh, 2014, Purification and Characterization of Glucose-6-Phosphate Dehydrogenase from Pigeon Pea (Cajanus cajan) Seeds, Adv. Enzym. Res., 2, 134, 10.4236/aer.2014.24014
Dong, 2019, The transcription factors tcp4 and pif3 antagonistically regulate organ-specific light induction of saur genes to modulate cotyledon opening during de-etiolation in Arabidopsis, Plant Cell, 31, 1155, 10.1105/tpc.18.00803
Field, D.L., and Barrett, S.C.H. (2012). Disassortative mating and the maintenance of sexual polymorphism in painted maple. Mol. Ecol., 21.
Gleiser, 2008, Disassortative mating, sexual specialization, and the evolution of gender dimorphism in heterodichogamous Acer opalus, Evolution, 62, 1676, 10.1111/j.1558-5646.2008.00394.x
Jung, 2012, Arabidopsis RNA-binding Protein FCA regulates microRNA172 processing in thermosensory flowering, J. Biol. Chem., 287, 16007, 10.1074/jbc.M111.337485
Tiessen, 2010, Arabidopsis sucrose synthase 2 and 3 modulate metabolic homeostasis and direct carbon towards starch synthesis in developing seeds, Planta, 232, 701, 10.1007/s00425-010-1207-9
Han, G. (2018). Studies of hormonal regulation on flower bud differentiation and development in heterodichogamous Cyclocarya paliurus. Nanjing For. Univ., (In Chinese).
Baek, W., Lim, C.W., Luan, S., and Lee, S.C. (2019). The RING finger E3 ligases PIR1 and PIR2 mediate PP2CA degradation to enhance abscisic acid response in Arabidopsis. Plant J.
Martinez-Zapater, J.M., Coupland, G., Dean, C., and Koornneef, M. (1994). The Transition to Flowering in Arabidopsis, Cold Spring Harbor Laboratory Press.
Achard, 2006, Integration of plant responses to environmentally activated phytohormonal signals, Science, 311, 91, 10.1126/science.1118642
Schrader, 2004, Cambial meristem dormancy in trees involves extensive remodelling of the transcriptome, Plant J., 40, 173, 10.1111/j.1365-313X.2004.02199.x
Saure, 2011, Dormancy release in deciduous fruit trees, Hortic. Rev., 7, 239
Zhuang, 2013, Comparative proteomic and transcriptomic approaches to address the active role of GA4 in Japanese apricot flower bud dormancy release, J. Exp. Bot., 64, 4953, 10.1093/jxb/ert284
Binenbaum, 2018, Gibberellin localization and transport in plants, Trends Plant Sci., 23, 410, 10.1016/j.tplants.2018.02.005
Vachon, 2018, Interactions between transcription factors and chromatin regulators in the control of flower development, J. Exp. Bot., 69, 2461, 10.1093/jxb/ery079
Liu, 2009, Regulation of floral patterning by flowering time genes, Dev. Cell, 16, 711, 10.1016/j.devcel.2009.03.011
Liu, 2018, MIKC C-type MADS-box genes in Rosa chinensis: The remarkable expansion of ABCDE model genes and their roles in floral organogenesis, Hortic. Res., 5, 25, 10.1038/s41438-018-0031-4
Tian, 2010, Molecular mechanism of controlling flower formation by photoperiod inducement in plants, Acta Hortic. Sin., 37, 325
Wigge, 2005, Integration of spatial and temporal information during floral induction in Arabidopsis, Science, 312, 1600
Takatsuji, 1992, Characterization of a zinc finger DNA-binding protein expressed specifically in Petunia petals and seedlings, EMBO J., 11, 241, 10.1002/j.1460-2075.1992.tb05047.x
Takatsuji, 1994, A new family of zinc finger proteins in petunia: Structure, DNA sequence recognition, and floral organ-specific expression, Plant Cell, 6, 947
Chapman, 2009, Mechanism of auxin-regulated gene expression in plants, Annu. Rev. Genet., 43, 265, 10.1146/annurev-genet-102108-134148
Immink, 2010, The “ABC” of MADS domain protein behaviour and interactions, Semin. Cell Dev. Biol., 21, 87, 10.1016/j.semcdb.2009.10.004
Becker, 2003, The major clades of MADS-box genes and their role in the development and evolution of flowering plants, Mol. Phylogenet. Evol., 29, 464, 10.1016/S1055-7903(03)00207-0
Wang, 2004, The embryo MADS domain protein Agamous-like 15 directly regulates expression of a gene encoding an enzyme involved in gibberellin metabolism, Plant Cell, 16, 1206, 10.1105/tpc.021261
Zhou, 2018, The research progress of AGAMOUS-like orthologous genes in woody plants, For. Sci. Technol., 43, 26
Yamane, 2011, Expressional regulation of PpDAM5 and PpDAM6, peach (Prunus persica) dormancy-associated MADS-box genes, by low temperature and dormancy-breaking reagent treatment, J. Exp. Bot., 62, 3481, 10.1093/jxb/err028
Liu, 2017, Cloning and expression analysis of MADS-box gene VcDAM1 related to blueberry flower bud dormancy, Plant Physiol. J., 53, 1728
Kitamura, 2016, Simultaneous down-regulation of DORMANCY-ASSOCIATED MADS-box6 and SOC1 during dormancy release in Japanese apricot (Prunus mume) flower buds, J. Hortic. Sci. Biotechnol., 91, 1, 10.1080/14620316.2016.1173524
Lin, 2014, Isolation of a sweet cherry AGAMOUS-like gene and its expression under gibberellin treatment, Mol. Plant Breed, 12, 1181