Comparative Analysis of Expressed Sequence Tags from Picea abies L. to Identify Dormancy Regulation-Implicated Genes in the Apical Meristem
محورهای موضوعی : مجله گیاهان زینتی
Shadi Heidari
1
,
Peivand Heidari
2
1 - Department of Plant Breeding, Science and Research Branch, Islamic Azad University, Tehran, Iran
2 - Department of Plant Breeding, Science and Research Branch, Islamic Azad University, Tehran, Iran
کلید واژه: Comparative Analysis, Secondary metabolites, Dormancy-release, Functional catalogs, ROS specificity,
چکیده مقاله :
The molecular basis of the plant meristem's dormancy-release is a sophisticated process and poorly understood. To find genes related to the release of the dormancy of the P. abies apical meristem, an expressed sequence tag analysis was used. The preliminary data for two cDNA libraries was gathered using the Harvard University database (Dormancy and dormancy-release libraries with 6987 and 6981 EST, respectively). The EGassembler software was used to assemble all EST sequences in order to find similarity between two libraries. After that, all contigs were processed using CLC bio software's X-blast against a non-redundant protein database. To detect genes with differential expression in two libraries, the IDEG6 software and the Audic-Claverie test were utilized. The GoMapMan comparative classification tool was used to categorize functional catalogs. All unigenes were grouped into 35 functional catalogs, of which 10 significantly different functional catalogs were identified, including major CHO metabolism, hormone metabolism, stress, transport, secondary metabolism, cofactors and vitamins, nucleotide metabolism, redox-regulation, mitochondrial electron transport/ATP synthesis, and fermentation. So far, there has been no report on the role of secondary metabolites in regulating plant meristem dormancy. This study provides insight into the probable function of secondary metabolites as major regulators of the apical meristem's dormancy in P. abies. In addition, redox and epigenetic changes downstream of hormones also appear to be involved in dormancy regulation. The potential of ROS specificity in terms of the spatio-temporal properties that characterize the expression of antioxidant enzymes allows them to be used as biomarkers in major developmental stages to develop a set of features in woody species that promote growth, wood, and fiber attributes. This research also provides information about the molecular mechanisms of the morphogenesis process in Norway spruce.
اساس مولکولی رهاسازی خواب مریستم گیاه یک فرآیند پیچیده است و به خوبی درک نشده است. برای یافتن ژن‌های مربوط به رهاسازی خواب مریستم آپیکال P. abies، از تجزیه و تحلیل برچسب توالی بیان شده استفاده شد. داده های اولیه برای دو کتابخانه cDNA با استفاده از پایگاه داده دانشگاه هاروارد (کتابخانه های خواب و رهاسازی خواب به ترتیب با 6987 و 6981 EST) جمع آوری شد. نرم افزار EGassembler برای جمع آوری تمام توالی های EST به منظور یافتن شباهت بین دو کتابخانه استفاده شد. پس از آن، همه کانتبگ ها با استفاده از نرم افزار CLC bio X-blast در برابر یک پایگاه داده پروتئین غیر تکراری پردازش شدند. برای شناسایی ژن‌های دارای بیان افتراقی در دو کتابخانه، از نرم‌افزار IDEG6 و آزمون Audic-Claverie استفاده شد. ابزار طبقه بندی مقایسه ای GoMapMan برای دسته بندی کاتالوگ های کاربردی استفاده شد. همه یونیژن ها در 35 کاتالوگ عملکردی گروه بندی شدند که 10 کاتالوگ عملکردی متفاوت از جمله متابولیسم اصلی CHO، متابولیسم هورمون، استرس، انتقال، متابولیسم ثانویه، کوفاکتورها و ویتامین ها، متابولیسم نوکلئوتید، تنظیم ردوکس، انتقال الکترون میتوکندری/ATP و تخمیر شناسایی شدند. تاکنون گزارشی مبنی بر نقش متابولیت های ثانویه در تنظیم خواب مریستم گیاهی گزارش نشده است. این مطالعه بینشی در مورد عملکرد احتمالی متابولیت های ثانویه به عنوان تنظیم کننده اصلی خواب مریستم آپیکال در P. abies ارائه می دهد. علاوه بر این، تغییرات ردوکس و اپی ژنتیک در پایین دست هورمون ها نیز به نظر می رسد که در تنظیم خواب دخیل هستند. پتانسیل اختصاصیت ROS از نظر ویژگی های مکانی-زمانی که بیان آنزیم های آنتی اکسیدانی را مشخص می کند به آنها اجازه می دهد تا به عنوان نشانگرهای زیستی در مراحل رشد استفاده شوند. این تحقیق همچنین اطلاعاتی در مورد مکانیسم‌های مولکولی فرآیند مورفوژنز در صنوبر نروژ ارائه می‌کند.
Agarwal, P.K., Agarwal, P., Reddy, M.K. and Sopory, S.K. 2006. Role of DREB transcription factors in abiotic and biotic stress tolerance in plants. Plant Cell Reports, 25: 1263-1274. https://doi.org/10.1007/s00299-006-0204-8
Antonescu, C., Antonescu, V., Sultana, R. and Quackenbush, J. 2010. Using the DFCI gene index databases for biological discovery. Current Protocols in Bioinformatics, 6: 36. https://doi.org/10.1002/0471250953.bi0106s29
Antony, N. 2010. The language of calcium signaling. Annual Review of Plant Biology, 61: 593-620. https://doi.org/10.1146/annurev-arplant-070109-104628
Bassel, G.W., Glaab, E., Marquez, J. and Bacardit, J. 2011. Functional network construction in Arabidopsis using rule-based machine learning on large-scale data sets. Plant Cell, 23: 3101-3116. https://doi.org/10.1105/tpc.111.088153
Bela, K., Horváth, E., Gallé, Á., Szabados, L., Tari, I. and Csiszár, J. 2015. Plant glutathione peroxidases: Emerging role of the antioxidant enzymes in plant development and stress responses. Journal of Plant Physiology, 176: 192-201. https://doi.org/ 10.1016/j.jplph.2014.12.014
Břiz, J., Pavingerova1, D., Vlasak, J. and Niedermeierova, H. 2013. Norway spruce (Picea abies). genetic transformation with modified Cry3A gene of B. thuringiensis. Acta Biochimica Polonica, 60: 395-400. PMID: 23888296.
Bryant, F.M., Hughes, D., Hassani-Pak, K. and Eastmond, P.J. 2019. Basic leucine zipper transcription factor 67 transactivates delay of germination 1 to establish primary seed dormancy in arabidopsis. The Plant Cell, 00892. https://doi.org/ 10.1105/tpc.18.00892
Castellano, M. and Sablowski, R. 2010. Intercellular signaling in the transition from stem cells to organogenesis in meristems. Plant Biology, 8: 26-31. https://doi.org/10.1016/j.pbi.2004.11.010
Chapman, J.M., Muhlemann, J.K., Gayomba, S.R. and Muday, G.K. 2019. RBOH-dependent ROS synthesis and ROS scavenging by plant specialized metabolites to modulate plant development and stress responses. Chemical Research in Toxicology, 32: 370-396. https://doi.org/10.1021/acs.chemrestox.9b00028
Cona, A., Rea, G., Angelini, R., Federico, R. and Tavladoraki, P. 2006. Functions of amine oxidases in plant development and defence. Trends in Plant Science, 11: 80-88. https://doi.org/10.1016/j.tplants.2005.12.009
Conde, D., González-Melendi, P. and Allona, I. 2013. Poplar stems show opposite epigenetic patterns during winter dormancy and vegetative growth. Trees - Structure and Function, 27: 311-320. https://doi.org/10.1007/s00468-012-0800-x
Conde, D., Le Gac, A.L., Perales, M., Dervinis, C., Kirst, M., Maury, S. and Allona, I. 2017. Chilling-responsive DEMETER-LIKE DNA demethylase mediates in poplar bud release. Plant, Cell & Environment, 40: 2236-2249. https://doi.org/ 10.1111/pce.13019
Cooke, J.E., Eriksson, M.E. and Junttila, O. 2012. The dynamic nature of bud dormancy in trees: Environmental control and molecular mechanisms. Plant, Cell & Environment, 35: 1707-1728. https://doi.org/10.1111/j.1365-3040.2012.02552.x
Cooley, M.B., Yang, H., Dahal, P., Mella, R.A., Downie, A.B., Haigh A.M. and Bradford, K.J. 1999. Vacuolar H+-ATPase is expressed in response to gibberellin during tomato seed germination. Plant Physiology, 121: 1339-1347. https://doi.org/10.1104/pp.121.4.1339
Deppmann, C.D., Alvania, R.S. and Taparowsky, E.J. 2006. Cross-species annotation of basic leucine zipper factor interactions: Insight into the evolution of closed interaction networks. Molecular Biology and Evolution, 23: 1480-1492. https://doi.org/10.1093/molbev/msl022
Depta, H., Elisele, K. and Hertel, R. 2006. Specific inhibitors of auxin transport: Action on tissue segments and in vitro binding to membranes from maize coleoptiles. Plant Science Letters, 31: 181-192. https://doi.org/10.1016/0304-4211.83.90055-X
Depuydt, S. and Hardtke, C.S. 2011. Hormone signaling crosstalk in plant growth regulation. Current Biology, 21: R365-R373. https://doi.org/10.1016/j.cub.2011.03.013
Dietz, K.J., Tavakoli, N., Kluge, C., Mimura, T., Sharma, S.S., Harris, G.C. and Golldack, D. 2001. Significance of the V‐type ATPase for the adaptation to stressful growth conditions and its regulation on the molecular and biochemical level. Journal of Experimental Botany, 52: 1969-1980. https://doi.org/10.1093/jexbot/52.363.1969
Erb, M. and Kliebenstein, D.J. 2020. Plant secondary metabolites as defenses, regulators, and primary metabolites: The blurred functional trichotomy. Plant Physiology, 00433. https://doi.org/10.1104/pp.20.00433
Finkelstein, R. 2013. Abscisic acid synthesis and response. Arabidopsis Book, 11, e0166. https://doi.org/ 10.1199/tab.0166
Gorelova, V., de Lepeleire, J., van Daele, J., Pluim, D., Meï, C., Cuypers, A. and van der Straeten, D. 2017. Dihydrofolate reductase/thymidylate synthase fine-tunes the folate status and controls redox homeostasis in plants. The Plant Cell, 29: 2831-2853. https://doi.org/10.1105/tpc.17.00433
Harborne, J.B. 2005. Recent advances in chemical ecology. Natural Product Reports, 12: 83-98. https://doi.org/ 10.1039/np9890600085
Hartmann, T. 2007. From waste products to ecochemicals: Fifty years’ research of plant secondary metabolism. Phytochemistry, 68: 2831-2846. https://doi.org/10.1016/j.phytochem. 2007.09.017
Heidari, Sh., Azizinezhad, R., Haghparast, R. and Heidari, P. 2019. Evaluation of the association among yield and contributing characters through path coefficient analysis in advanced lines of durum wheat under diverse conditions. Journal of Animal and Plant Sciences, 29: 1325-1335. http://www.thejaps.org.pk/docs/v-29-05/13
Heidari, Sh., Heidari, P., Azizinezhad, R., Etminan, A. and Khosroshahli, M. 2020. Assessment of genetic variability, heritability and genetic advance for agro-morphological and some in vitro related-traits in durum wheat. Bulgarian Journal of Agricultural Science, 26: 120-127. https://www.agrojournal.org/26/01-15.html
Heidari, S., Heidari, P. and Heidari, B. 2021. A survey of evolutionary changes of fatty acids and storage proteins in three Brassica species by comparative genomics method. New Cellular and Molecular Biotechnology Journal, 12 (45): 27-38. https://dor.org/20.1001.1.22285458.1400.12.45.7.6
Heidari, Sh. and Heidari, P. 2022. Evolutionary mechanisms underlying secondary metabolite diversity of the three Brassica species using insilico comparative analysis of the related genes. Crop biotech., 11(35): 23-36. https://doi.org/10.30473/CB.2022.62425.1864
Hua, J., Jing, C., Xiao-Ling, G., Jia, W., Ping-Rong, W., Xu-Dong, W. and Jun, X. 2006. Effect of ABA on rice callus and development of somatic embryo and plant regeneration. Acta Agronomica Sinica, 32: 1379-1383. http://zwxb.chinacrops.org/V32/I09/1379
Jouili, H., Bouazizi, H. and El Ferjani, E. 2011. Plant peroxidases: Biomarkers of metallic stress. Acta Physiologiae Plantarum, 33: 2075-2082. https://doi.org/10.1007/s11738-011-0780-2
Karlberg, A., Englund, M., Petterle, A., Molnar, G., Sjödin, A., Bako, L. and Bhalerao, R.P. 2010. Analysis of global changes in gene expression during activity-dormancy cycle in hybrid aspen apex. Plant Biotechnology Journal, 27:1-16. https://doi.org/ 10.5511/plantbiotechnology.27.1
Kumar, G., Rattan, U.K. and Singh, A.K. 2016. Chilling-mediated DNA methylation changes during dormancy and its release reveal the importance of epigenetic regulation during winter dormancy in apple. Malus x domestica Borkh. PLoS One, 11: e0149934. https://doi.org/10.1371/journal.pone.0149934
Leida, C., Conejero, A., Arbona, V., Gómez-Cadenas, A., Llácer, G., Badenes, M.L. and Ríos, G. 2012. Chilling-dependent release of seed and bud dormancy in peach associates to common changes in gene expression. PLoS ONE, 7: e35777. https://doi.org/10.1371/journal.pone.0035777
Li, H., Xu, T., Lin, D., Wen, M., Xie, M., Duclercq, J., Bielach, A., Kim, J., Reddy, G.V., Zuo, J., Benková. E., Friml, J., Guo, H. and Yang, Z. 2013. Cytokinin signaling regulates pavement cell morphogenesis in Arabidopsis. Cell Research, 23: 290-299. https://doi.org/10.1038/cr.2012.146
Li, J., Xu, Y., Niu, Q., He, L., Teng, Y. and Bai, S. 2018. Abscisic acid promotes the induction and maintenance of P. pyrifolia flower bud endodormancy. International Journal of Molecular Sciences, 19: 310. https://doi.org/10.3390/ijms19010310
Lin, C.J., Laiho, O. and Lähde, E. 2011. Norway spruce. P. abies L. regeneration and growth of understory trees under single-tree selection silviculture in Finland. European Journal of Medical Research, 131: 683-691. https://doi.org/10.1007/s10342-011-0541-1
Liu, B., Zhao, S., Tan, F., Zhao, H., Si, H. and Chen, Q. 2017. Changes in ROS production and antioxidant capacity during tuber sprouting in potato. Food Chemistry, 237: 205-213. https://doi.org/10.1016/j.foodchem.2017.05.107
Ma, X., Lv, S., Zhang, C. and Yang, C. 2013. Histone deacetylases and their functions in plants. Plant Cell Reports, 32: 465-478. https://doi.org/10.1007/s00299-013-1393-6
Marques, M.C., Alonso-Cantabrana, H., Forment, J., Arribas, R., Alamar, S., Conejero, V. and Perez-Amador, M.A. 2009. A new set of ESTs and cDNA clones from full-length and normalized libraries for gene discovery and functional characterization in citrus. BMC Genomics, 10: 428. https://doi.org/10.1186/1471-2164-10-428
Masoudi Nejad, A., Tonomura, K., Kawashima, S., Moriya, Y., Suzuki, M., Itoh, M. and Goto, S. 2006. EG assembler: online bioinformatics service for large-scale processing, clustering and assembling ESTs and genomic DNA fragments. Nucleic Acids Research, 34: 459-462. https://doi.org/10.1093/nar/gkl066
Ménard, R., Verdier, G., Ors, M., Erhardt, M., Beisson, F. and Shen, W.H. 2014. Histone H2B Monoubiquitination is involved in the regulation of cutin and wax composition in Arabidopsis thaliana. Plant and Cell Physiology, 55: 455-466. https://doi.org/10.1093/pcp/pct182
Murcia, G., Pontin, M., Reinoso, H., Baraldi, R., Bertazza, G., Gómez-Talquenca, S., Bottini, R. and Piccoli, P.N. 2016. ABA and GA3 increase carbon allocation in different organs of grapevine plants by inducing accumulation of non-structural carbohydrates in leaves, enhancement of phloem area and expression of sugar transporters. Physiologia Plantarum, 156: 323-37. https://doi.org/10.1111/ppl.12390
Oide, S., Bejai, S., Staal, J., Guan, N., Kaliff, M. and Dixelius, C. 2013. A novel role of PR2 in abscisic acid mediated, pathogen-induced callose deposition in Arabidopsis thaliana. New Phytologist, 200: 1187-1199. https://doi.org/10.1111/nph.12436
Pang, X.Q., Halaly, T., Crane, O., Keilin, T., Keren-Keiserman, A., Ogrodovitch, A., Galbraith, D. and Or. E. 2007. Involvement of calcium signaling in dormancy release of grape buds. Journal of Experimental Botany, 58: 3249-3262. https://doi.org/10.1093/jxb/erm172
Pedrosa, A.M., Martins, C., De, P.S., Gonçalves, L.P. and Costa, M.G.C. 2015. Late embryogenesis abundant (LEA) constitutes a large and diverse family of proteins involved in development and abiotic stress responses in sweet orange (Citrus sinensis L. Osb.). PloS One, 10 (12): e0145785. https://doi.org/10.1371/journal.pone.0145785
Pinder, J.B., Attwood. K.M. and Dellaire, G. 2013. Reading, writing, and repair: The role of ubiquitin and the ubiquitin-like proteins in DNA damage signaling and repair. Frontiers in Genetics, 4: 45. https://doi.org/10.3389/fgene.2013.00045
Prudencio, Á.S., Werner, O., Martínez-García, P.J., Dicenta, F., Ros, R.M. and Martínez-Gómez, P. 2018. DNA methylation analysis of dormancy release in P. dulcis flower buds using epi-genotyping by sequencing. International Journal of Molecular Sciences, 19: E3542. https://doi.org/10.3390/ijms19113542
Ramšak, Ž., Baebler, Š., Rotter, A., Korbar, M., Mozetič, I., Usadel, B. and Gruden, K. 2014. GoMapMan: Integration, consolidation and visualization of plant gene annotations within the MapMan ontology. Nucleic Acids Research, 42(D1): D1167-D1175. https://doi.org/10.1093/nar/gkt1056
Riou-Khamlichi, C., Menges, M., Healy, J.M.S. and Murray, J.A.H. 2000. Sugar control of the plant cell cycle: Differential regulation of Arabidopsis D-type cyclin gene expression. Molecular and Cellular Biology, 20: 4513-4521. https://doi.org/ 10.1128/MCB.20.13.4513-4521.2000
Rohde, A., Ruttink, T., Hostyn, V., Sterck, L., Driessche, K.V. and Boerjan, W. 2007. Gene expression during the induction, maintenance, and release of dormancy in apical buds of poplar. Journal of Experimental Botany, 58: 4047-4060. https://doi.org/ 10.1093/jxb/erm261
Rohde, A. and Bhalerao, R.P. 2007. Plant dormancy in the perennial context. Trends in Plant Science, 12: 217-223. https://doi.org/ 10.1016/j.tplants.2007.03.012
Romualdi, C., Bortoluzzi, S., Dalessi, F. and Danieli, G.A. 2003. IDEG6: A web tool for detection of differential expressed gene in multiple tag sampling experiments. Physiological Genomics, 12:159-162. http://doi.org/10.1152/physiolgenomics
Santamaría, M., Hasbún, R., Valera, M., Meijón, M., Valledor, L. and Rodríguez, J.L. 2009. Acetylated H4 histone and genomic DNA methylation patterns during bud set and bud burst in Castanea sativa. Journal of Plant Physiology, 166: 1360-1369. https://doi.org/10.1016/j.jplph.2009.02.014
Schäffer, A.A., Nawrocki, E.P., Choi, Y., Kitts, P.A., Karsch-Mizrachi, I. and McVeigh, R. 2018. VecScreen-plus-taxonomy: imposing a taxonomy increase on vector contamination screening. Bioinformatic, 34: 755-759. https://doi.org/ 10.1093/bioinformatics/btx669
Shim, D., Ko, J.H., Kim, W.C., Wang, Q., Keathley, D.E. and Han, K.H. 2014. A molecular framework for seasonal growth-dormancy regulation in perennial plants. Horticulture Research, 1: 14059. https://doi.org/ 10.1038/hortres.2014.59
Skrøppa, T. 2003. Technical guidelines for genetic conservation and use for N. spruce (P. abies). International Plant Genetic Resources Institute, Rome, Italy. 6 pages. http://www.euforgen.org/
Skylar, A., Sung, F., Hong, F., Chory, J. and Wu, X. 2011. Metabolic sugar signal promotes Arabidopsis meristematic proliferation via G2. Developmental Biology, 351: 82-89. https://doi.org/10.1016/j.ydbio.2010.12.019
Smith, A.G., Croft, M.T., Moulin, M. and Webb, M.E. 2007. Plants need their vitamins too. Current Opinion in Plant Biology, 10: 266-275. https://doi.org/10.1016/j.pbi.2007.04.009
Sun, M.Y., Fu, X.L., Tan, Q.P., Liu, L., Chen, M., Zhu, C.Y. and Gao, D.S. 2016. Analysis of basic leucine zipper genes and their expression during bud dormancy in peach (P. persica). Plant Physiology and Biochemistry, 104: 54-70. https://doi.org/ 10.1016/j.plaphy.2016.03.004
Swarbreck, S.M., Lindquist, E.A., Ackerly, D.D. and Andersen, G.L. 2011. Analysis of leaf and root transcriptomes of soil-grown A. barbata plants. Plant Cell Physiology, 52:317-332. https://doi.org/10.1093/pcp/pcq188
Takemura, Y. and Tamura, F. 2016. Induction of heat shock proteins during the bud dormancy stage in woody fruit plants. Heat Shock Proteins and Plants, 65-77. https://doi.org/10.1007/978-3-319-46340-7_4
Tylewicz, S., Petterle, A., Marttila, S., Miskolczi, P. and Singh, R.K. 2018. Photoperiodic control of seasonal growth is mediated by ABA acting on cell-cell communication. Science, 360: 212-215. https://doi.org/ 10.1126/science.aan8576
Ueno, S. 2013. Transcriptional profiling of bud dormancy induction and release in oak by next-generation sequencing. BMC Genomics, 14: 1988-1994. https://doi.org/10.1186/1471-2164-14-236
Vanyushin, B.F. 2006. DNA methylation in plants. In: Doerfler, W., Böhm, P. DNA methylation: Basic mechanisms. Current Topics in Microbiology and Immunology, 301. Springer, Berlin, Heidelberg. https://doi.org/10.1007/3-540-31390-7
Varkonyi-Gasic, E., Lough, R.H., Moss, S.M.A., Wu, R. and Hellens, R.P. 2012. Kiwifruit floral gene APETALA2 is alternatively spliced and accumulates in aberrant indeterminate flowers in the absence of miR172. Plant Molecular Biology, 78: 417-429. https://doi.org/10.1007/s11103-012-9877-2
Vergara, R., Noriega, X., Aravena, K., Prieto, H. and Perez, F.J. 2017. ABA represses the expression of cell cycle genes and may modulate the development of endodormancy in grapevine buds. Front Plant Science, 8: 812. https://doi.org/ 10.3389/fpls.2017.00812
Wang, H., Qi, Q., Schorr, P., Cutler, A.J., Crosby, W.L. and Fowke, L.C. 1998. ICK1, a cyclin-dependent protein kinase inhibitor from Arabidopsis thaliana interacts with both Cdc2a and CycD3, and its expression is induced by abscisic acid. Plant Journal, 15: 501-510. https://doi.org/10.1046/j.1365-313x.1998.00231.x
Wisniewski, M., Norelli, J., Bassett, C., Artlip, T. and Macarisin, D. 2011. Ectopic expression of a novel peach P. persica CBF transcription factor in apple (Malus×domestica) results in short-day induced dormancy and increased chilling hardiness. Planta, 233:971-983. https://doi.org/10.1007/s00425-011-1358-3
Xu, H., Cao, D., Chen, Y., Wei, D., Wang, Y. and Stevenson, R.A. 2016. Gene expression and proteomic analysis of shoot apical meristem transition from dormancy to activation in C. lanceolata. Scientific Reports, 6: 19938. https://doi.org/ 10.1038/srep19938
Zafra, A., Rodríguez-García, M.I. and Alche, J.D. 2010. Cellular localization of ROS and NO in olive reproductive tissues during flower development. BMC Plant Biology, 19: 36. https://doi.org/10.1186/1471-2229-10-36
Zanewich, K.P. and Rood, S.B. 1995. Vernalization and gibberellin physiology of winter canola-endogenous gibberellin content and metabolism of [3H] GA1 and [3H] GA20. Plant Physiology, 108: 615-621. https://doi.org/ 10.1104/pp.108.2.615
Zawaski, C., Kadmiel, M., Pickens, J., Ma, C., Strauss, S. and Busov, V. 2011. Repression of gibberellin biosynthesis or signaling produces striking alterations in poplar growth, morphology and flowering. Planta, 234: 1285-1298. https://doi.org/10.107/s00425-011-1485-x
Zhang, Y.X., Yu, D., Tian, X.L., Liu, C.Y., Gai, S.P. and Zheng, G.S. 2014. Differential expression proteins associated with bud dormancy release during chilling treatment of tree peony (P. suffruticosa). Plant Biology, 17: 114-122. https://doi.org/ 10.1111/plb.12213
Zhang, Z., Zhuo, X., Zhao, K., Zheng, T., Han, Y., Yuan, C. and Zhang, Q. 2018. Transcriptome profiles reveal the crucial roles of hormone and sugar in the bud dormancy of P. mume. Scientific Reports, 8: 5090. https://doi.org/10.1038/s41598-018-23108-9
Zheng, C., Halaly, T., Acheampong, A.K., Takebayashi, Y., Jikumaru, Y. and Kamiya, Y. 2015. Abscisic acid regulates grape bud dormancy, and dormancy release stimuli may act through modification of ABA metabolism. Journal of Experimental Botany, 66: 1527-1542. https://doi.org/10.1093/jxb/eru519
Zhuang, W., Gao, Z., Wen, L., Huo, X., Cai, B. and Zhang, Z. 2015. Metabolic changes upon flower bud release in Japanese apricot are enhanced by exogenous GA4. Horticulture Research, 2: 15046. https://doi.org/10.1038/hortres.2015.46
