Gibberellin delays floral transition in cultivated strawberry via the coordinated modulation of photoperiod signaling and nitrogen metabolism

Abstract

Gibberellins (GAs) play a critical role in regulating the balance between vegetative and reproductive growth in strawberries; however, the underlying molecular mechanisms remain largely unclear. In this study, a weekly foliar application of GA₃ was performed to plugs of the short-day strawberry cultivar ‘Ninglu’ (Fragaria ×  ananassa). During the vegetative growth stage, GA₃ treatment increased plant height by 57.7% and mean petiole length by 69.4%, in addition to enhancing the expansion of the leaf lamina and vascular tissues. Developmental analysis of the shoot apical meristem (SAM) revealed that GA₃ delayed floral transition: while all control plants initiated flower buds within 40 days, only 77% of GA₃-treated plants did so. Transcriptional analysis showed that GA₃ significantly upregulated the expression of photoperiod-related genes in leaves, including GIGANTEA (GI), CONSTANS (CO), and FLOWERING LOCUS T 1 (FT1), which activated floral integrators such as SUPPRESSOR OF OVEREXPRESSION OF CO 1 (SOC1) and TERMINAL FLOWER 1 (TFL1). These changes subsequently suppressed key floral activators (APETALA1, AP1; FRUITFULL, FUL; and LEAFY, LFY) in the SAM. Additionally, GA₃ influenced nitrogen partitioning in leaves by modulating the expression of genes associated with nitrogen metabolism (NITRATE REDUCTASE, NR; NITRITE REDUCTASE, NIR; GLUTAMINE SYNTHETASE, GS; and FD-GOGAT, GOGAT), transport (NITRATE TRANSPORTER 1.2/1.7, NRT1.2/NRT1.7; and AMMONIUM TRANSPORTER 1.1, AMT1.1), and flowering time control (FERREDOXIN-NADP( +)OXIDOREDUCTASE 1, FNR1; and CRYPTOCHROME 1, CRY1). These results suggest that GA₃ may delay floral transition in strawberries through the coordinated modulation of vegetative growth, photoperiod signaling, and nitrogen metabolism, providing mechanistic insights into GA-mediated flowering control and offering potential implications for cultivation management.

Keywords

Strawberry / Gibberellin / Floral transition / Photoperiod signaling / Nitrogen

References

[1] Alonso M, Prévost P, Potier A, Martin PGP, Caraglio Y, Nicolas M, et al. Molecular mechanisms underlying the determination of axillary bud fate and outgrowth into branch crown in strawberry. bioRxiv. 2025;645709. https://doi.org/10.1101/2025.03.27.645709.

[2] Andrés F, Coupland G. The genetic basis of flowering responses to seasonal cues. Nat Rev Genet. 2012, 13: 627-639.

[3] Bai L, Liu Y, Mu Y, He C, Yan Y, Xie B, et al. Gibberellin effects on nitrogen metabolism and uptake in cucumber seedlings under root-zone suboptimal temperature. Hortic Plant J. 2018;45:1917–28. (in Chinese) https://doi.org/10.16420/j.issn.0513-353x.2017-0863.

[4] Basu A, Nguyen A, Betts NM, Lyons TJ. Strawberry as a functional food: an evidence-based review. Crit Rev Food Sci Nutr. 2014, 54: 790-806.

[5] Blázquez MA, Green R, Nilsson O, Sussman MR, Weigel D. Gibberellins promote flowering of Arabidopsis by activating the LEAFY promoter. Plant Cell. 1998, 10: 791-800.

[6] Blázquez M, Koornneef M, Putterill J. Flowering on time: genes that regulate the floral transition. EMBO Rep. 2001, 2: 1078-1082.

[7] Camut L, Gallova B, Jilli L, Sirlin-Josserand M, Carrera E, Sakvarelidze-Achard Let al. . Nitrate signaling promotes plant growth by upregulating gibberellin biosynthesis and destabilization of DELLA proteins. Curr Biol. 2021, 31: 4971-4982.

[8] Castro Marín I, Loef I, Bartetzko L, Searle I, Coupland G, Stitt Met al. . Nitrate regulates floral induction in Arabidopsis, acting independently of light, gibberellin and autonomous pathways. Planta. 2011, 233: 539-552.

[9] Castro-Camba R, Sánchez C, Vidal N, Vielba JM. Interactions of gibberellins with phytohormones and their role in stress responses. Horticulturae. 2022, 8. 241

[10] Castro-Camba R, Sánchez C, Vidal N, Vielba JM. Plant development and crop yield: the role of gibberellins. Plants (Basel). 2022, 11. 2650

[11] Conti L. Hormonal control of the floral transition: can one catch them all?. Dev Biol. 2017, 430: 288-301.

[12] Costes E, Crespel L, Denoyes B, Morel P, Demene MN, Lauri PEet al. . Bud structure, position and fate generate various branching patterns along shoots of closely related Rosaceae species: a review. Front Plant Sci. 2014, 5. 666

[13] Dong B, Deng Y, Wang H, Gao R, Stephen GK, Chen Set al. . Gibberellic acid signaling is required to induce flowering of chrysanthemums grown under both short and long days. Int J Mol Sci. 2017, 18. 1259

[14] Fan G, Andrés J, Olbricht K, Koskela E, Hytönen T. Natural variation in the control of flowering and shoot architecture in diploid Fragaria species. Front Plant Sci. 2022, 13. 832795

[15] Feng J, Yu F, Lu P, Yang Y, Li L, Yang Let al. . Morphological observation and transcriptome profiling of axillary buds with different identities in response to gibberellin in woodland strawberry. Plant Physiol Biochem. 2025, 229. 110347

[16] Forde BG. Glutamate signalling in roots. J Exp Bot. 2014, 65: 779-787.

[17] Fornara F, de Montaigu A, Coupland G. Snapshot: control of flowering in Arabidopsis. Cell. 2010, 141. 550

[18] Gaston A, Potier A, Alonso M, Sabbadini S, Delmas F, Tenreira Tet al. . The FveFT2 florigen/FveTFL1 antiflorigen balance is critical for the control of seasonal flowering in strawberry while FveFT3 modulates axillary meristem fate and yield. New Phytol. 2021, 232: 372-387.

[19] Giampieri F, Alvarez-Suarez JM, Battino M. Strawberry and human health: effects beyond antioxidant activity. J Agric Food Chem. 2014, 62: 3867-3876.

[20] Gramma V, Olas J, Zacharaki V, Ponnu J, Musialak-Lange M, Wahl V. Carbon and nitrogen signaling regulate FLOWERING LOCUS C and impact flowering time in Arabidopsis. Plant Physiol. 2025, 197. kiae594

[21] Guo W, Ren L, Zhou Z, Meng Q. Difference of nitrogen contents, determined by the combustion and kjeldahl method in response to nitrate nitrogen in some feedstuffs. J Anim Feed Sci. 2007, 16(Suppl. 2): 178-183.

[22] Guo L, Plunkert M, Luo X, Liu Z. Developmental regulation of stolon and rhizome. Curr Opin Plant Biol. 2021, 59. 101970

[23] Guttridge CG, Thompson PA. The effect of gibberellins on growth and flowering of Fragaria and Duchesnea. J Exp Bot. 1964, 15: 631-646.

[24] Hytönen T, Kurokura T. Control of flowering and runnering in strawberry. Hortic J. 2020, 89: 96-107.

[25] Hytönen T, Palonen P, Mouhu K, Junttila O. Crown branching and cropping potential in strawberry (Fragaria × ananassa Duch.) can be enhanced by daylength treatments. J Hortic Sci Biotechnol. 2004, 79: 466-471.

[26] Hytönen T, Elomaa P, Moritz T, Junttila O. Gibberellin mediates daylength-controlled differentiation of vegetative meristems in strawberry (Fragaria × ananassa Duch). BMC Plant Biol. 2009, 9. 18

[27] Jiang Y, Zhu Y, Zhang L, Su W, Peng J, Yang Xet al. . EjTFL1 genes promote growth but inhibit flower bud differentiation in loquat. Front Plant Sci. 2020, 11. 576

[28] Jing D, Chen W, Hu R, Zhang Y, Xia Y, Wang Set al. . An integrative analysis of transcriptome, proteome and hormones reveals key differentially expressed genes and metabolic pathways involved in flower development in loquat. Int J Mol Sci. 2020, 21. 5107

[29] Koskela EA, Mouhu K, Albani MC, Kurokura T, Rantanen M, Sargent DJet al. . Mutation in TERMINAL FLOWER1 reverses the photoperiodic requirement for flowering in the wild strawberry Fragaria vesca. Plant Physiol. 2012, 159: 1043-1054.

[30] Lee J, Lee I. Regulation and function of SOC1, a flowering pathway integrator. J Exp Bot. 2010, 61: 2247-2254.

[31] Li S, Tian Y, Wu K, Ye Y, Yu J, Zhang Jet al. . Modulating plant growth–metabolism coordination for sustainable agriculture. Nature. 2018, 560: 595-600.

[32] Li X, Lin C, Lan C, Tao Z. Genetic and epigenetic basis of phytohormonal control of floral transition in plants. J Exp Bot. 2024, 75: 4180-4194.

[33] Li Y, Jeong BR, Huang P, Qiu X, Zhu F, He Jet al. . Factors controlling runner formation in strawberries. Agronomy. 2025, 15. 2235

[34] Li Z, Ge X, Zhang L, Wang Q, Wu S, Wu Met al. . FaNRT2.7 transports nitrate and accelerates growth and development in plants. Sci Hortic. 2025, 350. 114360

[35] Li R, Yang S, Ma H, Wang M, Wang A, Huang W, et al. Advances in research on flower bud morphological differentiation of strawberry. Bot Res. 2020;9:101–13. (in Chinese) https://doi.org/10.12677/BR.2019.92013.

[36] Liang J, Wu Z, Zheng J, Koskela EA, Fan L, Fan Get al. . The GATA factor HANABA TARANU promotes runner formation by regulating axillary bud initiation and outgrowth in cultivated strawberry. Plant J. 2022, 110: 1237-1254.

[37] Liu W, Sun Q, Wang K, Du Q, Li W. Nitrogen limitation adaptation (NLA) is involved in source-to-sink remobilization of nitrate by mediating the degradation of NRT1.7 in Arabidopsis. New Phytol. 2017, 214: 734-744.

[38] Liu L, Xuan L, Jiang Y, Yu H. Regulation by FLOWERING LOCUS T and TERMINAL FLOWER 1 in flowering time and plant architecture. Small Structures. 2021, 2. 2000125

[39] Liu H, Gao X, Fan W, Fu X. Optimizing carbon and nitrogen metabolism in plants: from fundamental principles to practical applications. J Integr Plant Biol. 2025, 67: 1447-1466.

[40] Livak KJ, Schmittgen TD. Analysis of relative gene expression data using Real‐Time quantitative PCR and the 2^−ΔΔCT method. Methods. 2001, 25: 402-408.

[41] Loqué D, Yuan L, Kojima S, Gojon A, Wirth J, Gazzarrini Set al. . Additive contribution of AMT1;1 and AMT1;3 to high-affinity ammonium uptake across the plasma membrane of nitrogen-deficient Arabidopsis roots. Plant J. 2006, 48: 522-534.

[42] Manakasem Y, Goodwin PB. Responses of dayneutral and junebearing strawberries to temperature and daylength. J Hortic Sci Biotechnol. 2001, 76: 629-635

[43] Mao W, Han Y, Chen Y, Sun M, Feng Q, Li Let al. . Low temperature inhibits anthocyanin accumulation in strawberry fruit by activating FvMAPK3-induced phosphorylation of FvMYB10 and degradation of Chalcone Synthase 1. Plant Cell. 2022, 34: 1226-1249.

[44] McDaniel CN, Singer SR, Smith SME. Developmental states associated with the floral transition. Dev Biol. 1992, 153: 59-69.

[45] Mouhu K, Kurokura T, Koskela EA, Albert VA, Elomaa P, Hytönen T. The Fragaria vesca homolog of SUPPRESSOR OF OVEREXPRESSION OF CONSTANS1 represses flowering and promotes vegetative growth. Plant Cell. 2013, 25: 3296-3310.

[46] Mouradov A, Cremer F, Coupland G. Control of flowering time: interacting pathways as a basis for diversity. Plant Cell. 2002, 14: S111-S130.

[47] Mutasa-Göttgens E, Hedden P. Gibberellin as a factor in floral regulatory networks. J Exp Bot. 2009, 60: 1979-1989.

[48] Nilsson O, Lee I, Blázquez MA, Weigel D. Flowering-time genes modulate the response to LEAFY activity. Genetics. 1998, 150: 403-410.

[49] Nunes-Nesi A, Fernie AR, Stitt M. Metabolic and signaling aspects underpinning the regulation of plant carbon nitrogen interactions. Mol Plant. 2010, 3: 973-996.

[50] Osnato M, Castillejo C, Matías-Hernández L, Pelaz S. TEMPRANILLO genes link photoperiod and gibberellin pathways to control flowering in Arabidopsis. Nat Commun. 2012, 3. 808

[51] Paroussi G, Voyiatzis DG, Paroussis E, Drogoudi PD. Growth, flowering and yield responses to GA₃ of strawberry grown under different environmental conditions. Sci Hortic. 2002, 96: 103-113.

[52] Pipattanawong N, Fujishige N, Yamane K, Ijiro Y, Ogata R. Effects of growth regulators and fertilizer on runner production, flowering, and growth in day-neutral strawberries. Jpn J Trop Agric. 1996, 40: 101-105.

[53] Putterill J, Robson F, Lee K, Simon R, Coupland G. The CONSTANS gene of Arabidopsis promotes flowering and encodes a protein showing similarities to zinc finger transcription factors. Cell. 1995, 80: 847-857.

[54] Ramina A, Tonutti P, Tosi T. The effect of paclobutrazol on strawberry growth and fruiting. J Hortic Sci. 1985, 60: 501-506.

[55] Rana K, Chauhan N, Sharma JB. Effect of photoperiod and gibberellic acid (GA₃) on flowering and fruiting of strawberry: a review. J Pharmacogn Phytochem. 2020, 9: 1651-1655.

[56] Rantanen M, Kurokura T, Jiang P, Mouhu K, Hytönen T. Strawberry homologue of TERMINAL FLOWER1 integrates photoperiod and temperature signals to inhibit flowering. Plant J. 2015, 82: 163-173.

[57] Rehman S, Bahadur S, Xia W. An overview of floral regulatory genes in annual and perennial plants. Gene. 2023, 885. 147699

[58] Sanagi M, Aoyama S, Kubo A, Lu Y, Sato Y, Ito Set al. . Low nitrogen conditions accelerate flowering by modulating the phosphorylation state of FLOWERING BHLH 4 in arabidopsis. Proc Natl Acad Sci U S A. 2021, 118. e2022942118

[59] Shen T. The induction of nitrate reductase and the preferential assimilation of ammonium in germinating rice seedlings. Plant Physiol. 1969, 44: 1650-1655.

[60] Sønsteby A, Heide OM. Long-day control of flowering in everbearing strawberries. J Hortic Sci Biotechnol. 2007, 82: 875-884.

[61] Sussex IM. Developmental programming of the shoot meristem. Cell. 1989, 56: 225-229.

[62] Tenreira T, Lange MJP, Lange T, Bres C, Labadie M, Monfort Aet al. . A specific gibberellin 20-oxidase dictates the flowering-runnering decision in diploid strawberry. Plant Cell. 2017, 29: 2168-2182.

[63] Tsai SS, Chang YCA. Plant maturity affects flowering ability and flower quality in phalaenopsis, focusing on their relationship to carbon-to-nitrogen ratio. HortScience. 2022, 57: 191-196.

[64] Wagner D, Sablowski RWM, Meyerowitz EM. Transcriptional activation of APETALA1 by LEAFY. Science. 1999, 285: 582-584.

[65] Wan C, Mi L, Chen B, Li J, Huo H, Xu Jet al. . Effects of nitrogen during nursery stage on flower bud differentiation and early harvest after transplanting in strawberry. Braz J Bot. 2018, 41: 1-10.

[66] Wang Y, Yao Q, Zhang Y, Zhang Y, Xing J, Yang Bet al. . The role of gibberellins in regulation of nitrogen uptake and physiological traits in maize responding to nitrogen availability. Int J Mol Sci. 2020, 21. 1824

[67] Wang Y, Chen L, Su W, Hao Y, Liu H, Sun Get al. . Effect of nitrate concentration on the growth, bolting and related gene expression in flowering Chinese cabbage. Agronomy. 2021, 11. 936

[68] Wang M, Wang J, Wang Z, Teng Y. Nitrate signaling and its role in regulating flowering time in Arabidopsis thaliana. Int J Mol Sci. 2024, 25. 5310

[69] Yang J, Song J, Jeong B. Flowering and runnering of seasonal strawberry under different photoperiods are affected by intensity of supplemental or night-interrupting blue light. Plants. 2024, 13. 375

[70] Yoshida Y, Nishimoto T. Propagation and floral induction of transplant for forcing long-term production of seasonal flowering strawberries in Japan. Hortic J. 2020, 89: 87-95.

[71] Yu J, Yang X, Gao H, Sheng L. Transcriptome atlas provides novel insights into ABA-mediated modulation of strawberry fruit ripening and quality. Hort Adv. 2025, 3. 16

[72] Yuan S, Zhang Z, Zheng C, Zhao Z, Wang Y, Feng Let al. . Arabidopsis cryptochrome 1 functions in nitrogen regulation of flowering. Proc Natl Acad Sci U S A. 2016, 113: 7661-7666.

[73] Zhang Z, Fu Y, Zhou Y, Wang C, Lan T, Chen G. Nitrogen and nitric oxide regulate Arabidopsis flowering differently. Plant Sci. 2019, 284: 177-184.

[74] Zhang S, Zhang Y, Li K, Yan M, Zhang J, Yu Met al. . Nitrogen mediates flowering time and nitrogen use efficiency via floral regulators in rice. Curr Biol. 2021, 31: 671-683.

Funding

Jiangsu Agriculture Science and Technology Innovation Fund(CX(24)3055)

National Natural Science Foundation of China(32472696)

National Key Research and Development Program of China(2023YFF1001700)

Project of the Zhongshan Biological Breeding Laboratory(ZSBBL-KY2023-08)

RIGHTS & PERMISSIONS

The Author(s)