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Journal of Integrative Agriculture  2019, Vol. 18 Issue (6): 1295-1311    DOI: 10.1016/S2095-3119(18)62131-8
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Effect of exogenous GA3 on flowering quality, endogenous hormones, and hormone- and flowering-associated gene expression in forcingcultured tree peony (Paeonia suffruticosa)
GUAN Yan-ren1, 2*, XUE Jing-qi1*, XUE Yu-qian1*, YANG Ruo-wen1, WANG Shun-li1, ZHANG Xiu-xin1
 
1 Key Laboratory of Biology and Genetic Improvement of Horticultural Crops, Ministry of Agriculture/Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing 100081, P.R.China
2 School of Landscape Architecture and Forestry, Qingdao Agricultural University, Qingdao 266109, P.R.China
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Abstract  
Gibberellins (GAs) promote flowering in the forcing-cultured tree peony (Paeonia suffruticosa), however, the mechanism of regulating flowering is not fully understood.  In this study, exogenous GA3 was applied to five-year-old Luoyang Hong plants to explore responses in terms of endogenous hormones, flowering quality, and the hormone- and flowering-associated gene expression.  Exogenous GA3 application significantly promoted flower bud development and new branch growth, as well as improved flowering quality.  Exogenous GA3 application also stimulated the synthesis of endogenous GA3 and indole-3-acetic acid (IAA) but reduced abscisic acid (ABA) levels.  To further elucidate the regulatory mechanism, eight genes for GA biosynthesis and signaling, including PsCPS, PsKS, PsGA3ox, PsGA2ox, PsGID1b, PsGID1c, PsDELLA, and PsGID2 were cloned for the first time, and sequence analysis was also performed.  The results suggested that all the cloned genes have conserved structure as each homologous gene reported in the other species.   Phylogenetic trees constructed by the each cloned gene showed that the phylogenetic evolutionary relationship of P. suffruticosa was closely related to Vitis vinifera.  The expression patterns of the above genes, and genes for ABA and IAA biosynthetic and signaling, and the flowering time were also investigated.  Most of the above genes showed higher expression in the control buds than those in the GA3 treated buds at six developmental stages, whereas the expression levels of PsSOC1 and PsSPL9 were up-regulated by GA3 treatment.  The results also showed that the GA-biosynthetic and signaling pathways are conserved in tree peony, and the PsCPS, PsGA3ox, PsGA2ox, PsGID1, PsDELLA, and PsGID2 genes are necessary for feedback regulation of GAs.  Furthermore, hormone changes promoted PsSOC1 and PsSPL9 expression, and repressed PsSVP expression, which contributed to the improvement flowering quality in tree peony of forcing culture. 
Keywords:  tree peony        forcing culture        hormones        gibberellic acid        GA biosynthesis and signaling        flowering quality  
Received: 22 June 2018   Accepted:
Fund: This study was funded by the National Natural Science Foundation of China (31501800 and 31572156) and the National Natural Science Foundation of China Youth Fund (2015QRNC001), the Science and Technology Cooperation Foundations of Henan Province of China (172106000005), and the Agricultural Science and Technology Innovation Program (ASTIP) of the Chinese Academy of Agricultural Sciences.
Corresponding Authors:  Correspondence WANG Shun-li, Tel: +86-10-82105944, Fax: +86-10-62174123, E-mail: wangshunli@caas.cn; ZHANG Xiu-xin, E-mail: zhangxiuxin@caas.cn, Tel: +86-10-82105944, Fax: +86-10-62174123   
About author:  *These authors contributed equally to this work.

Cite this article: 

GUAN Yan-ren, XUE Jing-qi, XUE Yu-qian, YANG Ruo-wen, WANG Shun-li, ZHANG Xiu-xin. 2019. Effect of exogenous GA3 on flowering quality, endogenous hormones, and hormone- and flowering-associated gene expression in forcingcultured tree peony (Paeonia suffruticosa). Journal of Integrative Agriculture, 18(6): 1295-1311.

Anderson J V, Gesch R W, Jia Y, Chao W S, Horvath D P. 2005. Seasonal shifts in dormancy status, carbohydrate metabolism, and related gene expression in crown buds of leafy spurge. Plant Cell Environment, 28, 1567–1578.
Boss P K, Thomas M R. 2002. Association of dwarfism and floral induction with a grape ‘green revolution’ mutation. Nature, 416, 847–850.
Campos-Rivero G, Osorio-Montalvo P, Sánchez-Borges R, Us-Camas R, Duarte-Aké F, De-la-Peña C. 2017. Plant hormone signaling in flowering: An epigenetic point of view. Journal of Plant Physiology, 214, 16–27.
Cheng C X, Chen J, Singer S D, Gao M, Xu S Z, Zhou Y M, Li Z, Fei Z J, Wang Y J, Wang X P. 2015. Gibberellin-induced changes in the transcriptome of grapevine (Vitis labrusca×
V. vinifera) cv. Kyoho flowers. BMC Genomics, 16, 1–16.
Davies P J. 1996. Plant hormones. Physiology, biochemistry and molecular biology. Scientia Horticulturae, 66, 267–270.
Domingos S, Fino J, Cardoso V, Sánchez C, Ramalho J C, Larcher R, Paulo O S, Oliveira C M, Goulao L F. 2016. Shared and divergent pathways for flower abscission are triggered by gibberellic acid and carbon starvation in seedless Vitis vinifera L. BMC Plant Biology, 16, 38.
Fronara F, de Montaigu A, Coupland G. 2010. SnapShot: control of flowering in Arabidopsis. Cell, 141, 550.e1–550.e2.
Fukazawa J, Mori M, Watanabe S, Miyamoto C, Ito T, Takahashi Y. 2017. DELLA-GAF1 complex is a main component in gibberellin feedback regulation of GA20 Oxidase 2. Plant Physiology, 175, 1395–1406.
Gai S P, Zhang Y X, Liu C Y, Zhang Y, Zheng G S. 2013. Transcript profiling of Paoenia ostii during artificial chilling induced dormancy release identifies activation of GA pathway and carbohydrate metabolism. PLoS ONE, 8, e55297.
Galvão V C, Horrer D, Küttner F, Schmid M. 2012. Spatial control of flowering by DELLA proteins in Arabidopsis thaliana. Development, 139, 4072–4082.
Goldberg-Moeller R, Shalom L, Shlizerman L, Samuels S, Zur N, Ophir R, Blumwald E, Sadka A. 2013. Effects of gibberellin treatment during flowering induction period on global gene expression and the transcription of flowering-control genes in Citrus buds. Plant Science, 198, 46–57.
Griffiths J, Murase K, Rieu I, Zentella R, Zhang Z L, Powers S J, Gong F, Phillips A L, Hedden P, Sun T P, Thomas S G. 2006. Genetic characterization and functional analysis of the GID1 gibberellin receptors in Arabidopsis. The Plant Cell, 18, 3399–3414.
Hao Q, Aoki N, Katayama J, Kako T, Cheon K S, Akazawa Y, Kobayashi N. 2013. Crossability of American tree peony ‘High Noon’ as seed parent with Japanese cultivars to breed superior cultivars. Euphytica, 191, 35–44.
Hartweck L M. 2008. Gibberellin signaling. Planta, 229, 1–13.
Hedden P, Phillips A L. 2000. Gibberellin metabolism: New insights revealed by the genes. Trends in Plant Science, 5, 523–530.
Hedden P, Thomas S G. 2012. Gibberellin biosynthesis and its regulation. Biochemical Journal, 444, 11–25.
Hirano K, Nakajima M, Asano K, Nishiyama T, Sakakibara H, Kojima M, Katoh E, Xiang H Y, Tanahashi T, Hasebe M, Banks J, Ashikari M, Kitano H, Ueguchi-Tanaka M, Matsuoka M. 2007. The GID1-mediated gibberellin perception mechanism is conserved in the Lycophyte Selaginella moellendorffii but not in the Bryophyte Physcomitrella patens. The Plant Cell, 19, 3058–3079.
Iwahori S, Weaver R J, Pool R M. 1968. Gibberellin-like activity in berries of seeded and seedless Tokay grapes. Plant Physiology, 43, 333–337.
Jung J H, Ju Y, Seo P J, Lee J H, Park C M. 2012. The SOC1-SPL module integrates photoperiod and gibberellic acid signals to control flowering time in Arabidopsis. The Plant Journal, 69, 577–588.
Li C Y, Anneli V A, Tuula P, Olavi J, Pekka H, Palva E T. 2003. Ecotype-dependent control of growth dormancy and freezing tolerance under seasonal changes in Betula pendula Roth. Trees, 17, 127–132.
Li M Z, An F Y, Li W Y, Ma M D, Feng Y, Zhang X, Hong W G. 2016. DELLA proteins interact with FLC to repress flowering transition. Journal of Integrative Plant Biology, 7, 642–655.
Middleton A M, Úbeda-Tomás S, Griffiths J, Holman T, Hedden P, Thomas S G, Phillips A L, Holdsworth M J, Bennett M J, King J R, Owen M R. 2012. Mathematical modeling elucidates the role of transcriptional feedback in gibberellin signaling. Proceeding of the National Academy of Science of the United States of America, 109, 7571–7576.
Mornya P M P, Cheng F Y, Li H Y. 2011. Chronological changes in plant hormone and sugar contents in cv. Ao-Shuang autumn flowering tree peony. Horticultural Science, 3, 104–112.
Nakagawa M, Honsho C, Kanzaki S, Shimizu K, Utsunomiya N. 2012. Isolation and expression analysis of FLOWERING LOCUS T-like and gibberellin metabolism genes in biennial-bearing mango trees. Scientia Horticulturae, 139, 108–117.
Olszewski N, Sun T P, Gubler F. 2002. Gibberellin signaling: Biosynthesis, catabolism, and response pathways. The Plant Cell, 14, S61–S80.
Otani M, Meguro S, Gondaira H, Hayashi M, Saito M, Han D S, Inthima P, Supaibulwatana K, Mori S, Jikumaru Y, Kamiya Y, Li T, Niki T, Nishijima T, Koshioka M, Nakano M. 2013. Overexpression of the gibberellin 2-oxidase gene from Torenia fournieri induces dwarf phenotypes in the liliaceous monocotyledon Tricyrtis sp. Journal of Plant Physiology, 170, 1416–1423.
Pan X Q, Welti R, Wang X M. 2010. Quantitative analysis of major plant hormones in crude plant extracts by high-performance liquid chromatography-mass spectrometry. Nature Protocols, 5, 986–992.
Shan C, Mei Z L, Duan J L, Chen H Y, Feng H F, Cai W M. 2014. OsGA2ox5, a gibberellin metabolism enzyme, is involved in plant growth, the root gravity response and salt stress. PLoS ONE, 9, e87110.
Sumitomo K, Li T, Hisamatsu T. 2009. Gibberellin promotes flowering of chrysanthemum by upregulating CmFL, a chrysanthemum FLORICAULA/LEAFY, homologous gene. Plant Science, 176, 643–649.
Sun T P. 2011. The molecular mechanism and evolution of the GA-GID1-DELLA signaling module in plants. Current Biology, 21, 338–345.
Thomas S G, Phillips A L, Hedden P. 1999. Molecular cloning and functional expression of gibberellin 2-oxidases, multifunctional enzymes involved in gibberellin deactivation. Proceeding of the National Academy of Science of the United States of America, 96, 4698–4703.
Ueguchi-Tanaka M, Matsuoka M. 2010. The perception of gibberellins: Clues from receptor structure. Current Opinion in Plant Biology, 13, 503–508.
Voorend W, Nelissen H, Vanholme R, Vliegher A D, Breusegem F V, Boerjan W, Roldán-Ruiz I, Muylle H, Inzé D. 2016. Overexpression of GA20-OXIDASE1 impacts plant height, biomass allocation and saccharification efficiency in maize. Plant Biotechnology, 14, 997–1007.
Wang P, Xue L, Batelli G, Lee S, Hou Y J, Oosten M J V, Zhang H, Tao W A, Zhu J K. 2013. Quantitative phosphoproteomics identifies SnRK2 protein kinase substrates and reveals the effectors of abscisic acid action. Proceeding of the National Academy of Science of the United States of America, 110, 11205–11210.
Wang S L, Beruto M, Xue J Q, Zhu F Y, Liu C J, Yan Y M, Zhang X X. 2015. Molecular cloning and potential function prediction of homologous SOC1 genes in tree peony. Plant Cell Reports, 34, 1459–1471.
Wang S L, Li X H, Wang K, Li S S, Zhang Y Z, Guo G F, Zeller F J, Hsam S L, Yan Y. 2011. Phylogenetic analysis of C, M, N, and U genomes and their relationships with Triticum and other related genomes as revealed by LMW-GS genes at Glu-3 loci. Genome, 54, 273–284.
Wang S L, Xue J Q, Ahmadi N, Holloway P, Zhu F Y, Ren X X, Zhang X X. 2014. Molecular characterization and expression patterns of PsSVP genes reveal distinct roles in flower bud abortion and flowering in tree peony (Paeonia Suffruticosa). Canadian Journal of Plant Science, 94, 1181–1193.
Wang Y, Li L, Ye T, Lu Y, Chen X, Wu Y. 2013. The inhibitory effect of ABA on floral transition is mediated by ABI5 in Arabidopsis. Journal of Experimental Botany, 64, 675–684.
Wellmer F, Riechmann J L. 2010. Gene networks controlling the initiation of flower development. Trends in Genetics, 26, 519–527.
Willige B C, Ghosh S, Nill C, Zourelidou M, Dohmann E M, Maier A, Schwechheimer C. 2007. The DELLA domain of GA INSENSITIVE mediates the interaction with the GA INSENSITIVE DWARF1A gibberellin receptor of Arabidopsis. The Plant Cell, 19, 1209–1220.
Withanage S P, Hossain M A, Kumar M S, Roslan H A, Abdullah M P, Napis S B, Shukor N A. 2015. Overexpression of Arabidopsis thaliana gibberellic acid 20 oxidase (AtGA20ox) gene enhance the vegetative growth and fiber quality in kenaf (Hibiscus cannabinus L.) plants. Breeding Science, 65, 177–191.
Xue J Q, Wang S L, Zhang P, Zhu F Y, Ren X X, Liu C J, Zhang X X. 2015. On the role of physiological substances, abscisic acid and its biosynthetic genes in seed maturation and dormancy of tree peony (Paeonia ostii ‘Feng Dan’). Scientia Horticulture, 182, 92–101.
Yamaguchi S. 2008. Gibberellin metabolism and its regulation. Annual Review of Plant Biology, 59, 225–251.
Yamaguchi N, Winter C M, Wu M F, Kanno Y, Yamaguchi A, Seo M. 2014. Gibberellin acts positively then negatively to control onset of flower formation in Arabidopsis. Science, 344, 638–641.
Yan J, Liao X, He R, Zhong M, Feng P, Li X, Tang D, Liu X, Zhao X. 2017. Ectopic expression of GA 2-oxidase 6 from rapeseed (Brassica napus L.) causes dwarfism, late flowering and enhanced chlorophyll accumulation in Arabidopsis thaliana. Plant Physiology of Biochemistry, 111, 10–19.
Zhang D, Ren L, Yue J H, Wang L, Zhuo L H, Shen X H. 2014. GA4 and IAA were involved in the morphogenesis and development of flowers in Agapanthus praecox ssp. Orientalis. Journal of Plant Physiology, 171, 966–976.
Zhang S W, Dong Z, Sheng F, Du L S, Shen Y W, Xing L B, Li Y, Ma J, Han M. 2016. Effect of exogenous GA3 and its inhibitor paclobutrazol on floral formation, endogenous hormones, and flowering-associated genes in ‘Fuji’ apple (Malus domestica Borkh.). Plant Physiology and Biochemistry, 107, 178–186.
Zhong C M, Xu H, Ye S T, Wang S Y, Li L F, Zhang S C, Wang X J. 2015. Gibberellic acid-stimulated Arabidopsis6 serves as an integrator of gibberellin, abscisic acid, and glucose signaling during seed germination in Arabidopsis. Plant Physiology, 169, 2288–2303.
Zhou H, Cheng F Y, Wang R, Zhong Y, He C. 2013. Transcriptome comparison reveals key candidate genes responsible for the unusual reblooming trait in tree peonies. PLoS ONE, 8, e79996.
Zhu F Y, Wang S L, Xue J Q, Li D D, Ren X X, Xue Y Q, Zhang X X. 2018. Morphological and physiological changes, and the functional analysis of PdSPL9 in the juvenile-to-adult phase transition of Paeonia delavayi. Plant Cell, Tissue and Organ Culture, 133, 325–337.
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