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The role of strigolactone analog (GR24) in endogenous hormone metabolism and hormone-related gene expression in tobacco axillary buds

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Abstract

Key message

Strigolactone has the potential to influence hormone metabolism, in addition to having a role in inhibiting axillary bud elongation, which could be regulated by the expression of phytohormones-related genes.

Abstract

The elongation of axillary buds affects the economic benefits of tobacco. In this study, it was investigated the effect of strigolactone (SL) on the elongation of tobacco axillary buds and its endogenous hormone metabolism and related gene expression by applying the artificial analog of SL, GR24, and an inhibitor of SL synthesis, TIS-108, to the axillary buds. The results showed that the elongation of axillary buds was significantly inhibited by GR24 on day 2 and day 9. Ultra-high-performance liquid-chromatography-mass spectrometry results further showed that SL significantly affected the metabolism of endogenous plant hormones, altering both their levels and the ratios between each endogenous hormone. Particularly, the levels of auxin (IAA), trans-zeatin-riboside (tZR), N6-(∆2-isopentenyl) adenine (iP), gibberellin A4 (GA4), jasmonic acid (JA), and jasmonoyl isoleucine (JA-Ile) were decreased after GR24 treatment on day 9, but the levels of 1-aminocyclopropane-1-carboxylic acid (ACC) and gibberellin A1 (GA1) were significantly increased. Further analysis of endogenous hormonal balance revealed that after the treatment with GR24 on day 9, the ratio of IAA to cytokinin (CTK) was markedly increased, but the ratios of IAA to abscisic acid (ABA), salicylic acid (SA), ACC, JAs, and, GAs were notably decreased. In addition, according to RNA-seq analysis, multiple differentially expressed genes were found, such as GH3.1, AUX/IAA, SUAR20, IPT, CKX1, GA2ox1, ACO3, ERF1, PR1, and HCT, which may play critical roles in the biosynthesis, deactivation, signaling pathway of phytohormones, and the biosynthesis of flavonoids to regulate the elongation of axillary buds in tobacco. This work lays the certain theoretical foundation for the application of SL in regulating the elongation of axillary buds of tobacco.

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Data availability

All data generated or analyzed during this study are included in this article. All data during this study are available from the first author by request.

References

  • Ahmad P, Abass Ahanger M, Nasser Alyemeni M, Wijaya L, Alam P, Ashraf MA (2018) Mitigation of sodium chloride toxicity in Solanum lycopersicum L. by supplementation of jasmonic acid and nitric oxide. J Plant Interact 13(1):64–72

    Article  CAS  Google Scholar 

  • Balla J, Medveďová Z, Kalousek P, Matiješčuková N, Friml J, Reinöhl V, Procházka S (2016) Auxin flow-mediated competition between axillary buds to restore apical dominance. Sci Rep 6:35955

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barbier FF, Dun EA, Beveridge CA (2017) Apical dominance. Curr Biol 27(17):R864–R865

    Article  CAS  PubMed  Google Scholar 

  • Barbier FF, Dun EA, Kerr SC, Chabikwa TG, Beveridge CA (2019) An update on the signals controlling shoot branching. Trends Plant Sci 24(3):220–236

    Article  CAS  PubMed  Google Scholar 

  • Besseau S, Hoffmann L, Geoffroy P, Lapierre C, Pollet B, Legrand M (2007) Flavonoid accumulation in arabidopsis repressed in lignin synthesis affects auxin transport and plant growth. Plant Cell 19(1):148–162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Binenbaum J, Weinstain R, Shani E (2018) Gibberellin localization and transport in plants. Trends Plant Sci 23(5):410–421

    Article  CAS  PubMed  Google Scholar 

  • Brewer PB, Dun EA, Gui R, Mason MG, Beveridge CA (2015) Strigolactone inhibition of branching independent of polar auxin transport. Plant Physiol 168(4):1820–1829

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carbonnel I, Bennett T, Morffy LY, Stanga JP, Abbas A (2015) SMAX1-LIKE/D53 family members enable distinct MAX2-dependent responses to strigolactone and karrikins in Arabidopsis. Plant Cell 27:3143

    Article  Google Scholar 

  • Chang S, Chen Y, Jia S, Li Y, Liu K, Lin Z, Wang H, Chu Z, Liu J, Xi C, Zhao H, Han S, Wang Y (2020) Auxin apical dominance governed by the Osasp1-OsTIF1 complex determines distinctive rice caryopses development on different branches. PLoS Genet 16(10):e1009157

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chao WS, Doğramaci M, Horvath DP, Anderson JV, Foley ME (2016) Phytohormone balance and stress-related cellular responses are involved in the transition from bud to shoot growth in leafy spurge. BMC Plant Biol 16:47

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen XJ, Xia XJ, Guo X, Zhou YH, Shi K, Zhou J, Yu JQ (2016) Apoplastic H2O2 plays a critical role in axillary bud outgrowth by altering auxin and cytokinin homeostasis in tomato plants. New Phytol 211(4):1266–1278

    Article  CAS  PubMed  Google Scholar 

  • Chen J, Zhang L, Zhu M, Han L, Lv Y, Liu Y, Li P, Jing H, Cai H (2018a) Non-dormant Axillary Bud 1 regulates axillary bud outgrowth in sorghum. J Integr Plant Biol 60(10):938–955

    Article  CAS  PubMed  Google Scholar 

  • Chen S, Zhou Y, Chen Y, Gu J (2018b) Fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics (oxford, England) 34(17):i884–i890

    PubMed  Google Scholar 

  • Chen K, Li GJ, Bressan RA, Song CP, Zhu JK, Zhao Y (2020) Abscisic acid dynamics, signaling, and functions in plants. J Integr Plant Biol 62(2):25–54

    Article  CAS  PubMed  Google Scholar 

  • Cheng X, Ruyter-Spira C, Bouwmeester H (2013) The interaction between strigolactone and other plant hormones in the regulation of plant development. Front Plant Sci 4:199

    Article  PubMed  PubMed Central  Google Scholar 

  • Dierck R, Dhooghe E, Huylenbroeck JM, Riek JD, Keyser ED, Straeten DV (2016) Response to strigolactone treatment in chrysanthemum axillary buds is influenced by auxin transport inhibition and sucrose availability. Acta Physiol Plant 38:271

    Article  Google Scholar 

  • Ding N, Qin Q, Wu X, Miller RD, Zaitlin D, Li D, Yang S (2020) Antagonistic regulation of axillary bud outgrowth by the Branched genes in tobacco. Plant Mol Biol 103(1–2):185–196

    Article  CAS  PubMed  Google Scholar 

  • Duan J, Yu H, Yuan K, Liao Z, Meng X, Jing Y, Liu G, Chu J, Li J (2019) Strigolactone promotes cytokinin degradation through transcriptional activation of Cytokinin oxidase/dehydrogenase 9 in rice. Proc Natl Acad Sci USA 116(28):14319–14324

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dun EA, de Saint GA, Rameau C, Beveridge CA (2012) Antagonistic action of strigolactone and cytokinin in bud outgrowth control. Plant Physiol 158(1):487–498

    Article  CAS  PubMed  Google Scholar 

  • Faiss M, Zalubìlová J, Strnad M, Schmülling T (1997) Conditional transgenic expression of the ipt gene indicates a function for cytokinins in paracrine signaling in whole tobacco plants. Plant J 12(2):401–415

    Article  CAS  PubMed  Google Scholar 

  • Feng Lu, Liang X, Zhou Y, Zhang Y, Liu J, Cai M (2020) Functional analysis of Aux/IAAs and SAURs on shoot growth of Lagerstroemia indica through virus-induced gene silencing (VIGS). Forests 11(12):1288

    Article  Google Scholar 

  • Ferrero M, Pagliarani C, Novák O, Ferrandino A, Cardinale F, Visentin I, Schubert A (2018) Exogenous strigolactone interacts with abscisic acid-mediated accumulation of anthocyanins in grapevine berries. J Exp Bot 69(9):2391–2401

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fujita Y, Yoshida T, Yamaguchi-Shinozaki K (2013) Pivotal role of the AREB/ABF-SnRK2 pathway in ABRE-mediated transcription in response to osmotic stress in plants. Physiol Plant 147(1):15–27

    Article  CAS  PubMed  Google Scholar 

  • Gao YL, Song ZB, Li WZ, Jiao FC, Wang R, Huang CJ, Li YP, Wang BW (2016) NtBRC1 suppresses axillary branching in tobacco after decapitation. Genet Mol Res 15(4). https://doi.org/10.4238/gmr15049320

    Article  PubMed  Google Scholar 

  • Gomez-Roldan V, Fermas S, Brewer PB, Puech-Pagès V, Dun EA, Pillot JP (2008) Strigolactone inhibition of shoot branching. Nature 455(7210):189–194

    Article  CAS  PubMed  Google Scholar 

  • González-Grandío E, Pajoro A, Franco-Zorrilla JM, Tarancón C, Immink RG, Cubas P (2017) Abscisic acid signaling is controlled by a Branched1/HD-ZIP I cascade in Arabidopsis axillary buds. Proc Natl Acad Sci USA 114(2):E245–E254

    Article  PubMed  Google Scholar 

  • Grundmann L, Känel A, Muth J, Beinecke F, Jekat M, Shen Y (2022) Tissue-specific expression of barnase in tobacco delays axillary shoot development after topping. Plant Biotechnol J 20(3):411–413

    Article  PubMed  Google Scholar 

  • Hall W, Truchelut GB, Leinweber CL, Herrero FA (1957) Ethylene production by the cotton plant and its effects under experimental and field conditions. Physiol Plant 10(2):306–317

    Article  CAS  Google Scholar 

  • Hayward A, Stirnberg P, Beveridge CA, Leyser O (2009) Interactions between auxin and strigolactone in shoot branching control. Plant Physiol 151(1):400–412

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hedden P, Sponsel VM (2015) A century of gibberellin research. J Plant Growth Regul 34(4):740–760

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu Q, Zhang S, Huang B (2018) Strigolactone and interaction with auxin regulating root elongation in tall fescue under different temperature regimes. Plant Sci 271:34–39

    Article  CAS  PubMed  Google Scholar 

  • Ito S, Umehara M, Hanada A, Kitahata N, Hayase H, Yamaguchi S, Asami T (2011) Effects of triazole derivatives on strigolactone levels and growth retardation in rice. PLoS ONE 6(7):e21723

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ito S, Yamagami D, Asami T (2018) Effects of gibberellin and strigolactone on rice tiller bud growth. J Pestic Sci 43(3):220–223

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ivanchenko M, Muday G, Dubrovsky J (2008) Ethylene-auxin interactions regulate lateral root initiation and emergence in Arabidopsis thaliana. Plant J 55(2):335–347

    Article  CAS  PubMed  Google Scholar 

  • Jiang B, Miao H, Chen S, Zhang SM, Chen FD, Fang WM (2010) The Lateral Suppressor-Like gene, DgLsL, alternated the axillary branching in transgenic chrysanthemum (Chrysanthemum × morifolium) by modulating IAA and GA content. Plant Mol Biol Rep 28:144–151

    Article  CAS  Google Scholar 

  • Jiu ST, Xu Y, Wang JY, Haider MS, Xu JM, Wang L (2022) Molecular mechanisms underlying the action of strigolactone involved in grapevine root development by interacting with other phytohormone signaling. Sci Hortic 293:110709

    Article  CAS  Google Scholar 

  • Kanehisa FM, Tanabe M, Sato Y, Morishima K (2017) KEGG: new perspectives on genomes, pathways, diseases and drugs. Nucleic Acids Res 45(D1):D353–D361

    Article  CAS  PubMed  Google Scholar 

  • Katyayini NU, Rinne PLH, Tarkowská D, Strnad M, van der Schoot C (2020) Dual role of gibberellin in perennial shoot branching: inhibition and activation. Front Plant Sci 11:736

    Article  PubMed  PubMed Central  Google Scholar 

  • Kerr SC, de Saint Germain A, Dissanayanke IM, Mason MG, Dun EA, Beveridge CA (2020) Hormonal regulation of the BRC1-dependent strigolactone transcriptome involved in shoot branching responses. bioRxiv

  • King RW, Evans LT, Mander LN, Moritz T, Pharis RP, Twitchin B (2003) Synthesis of gibberellin GA6 and its role in flowering of Lolium temulentum. Phytochemistry 62(1):77–82

    Article  CAS  PubMed  Google Scholar 

  • Koltai H, Beveridge CA (2013) Strigolactone and the coordinated development of shoot and root//Long-distance systemic signaling and communication in plants. Springer, Berlin, pp 189–204

    Google Scholar 

  • Kotov AA, Kotova LM, Romanov GA (2021) Signaling network regulating plant branching: recent advances and new challenges. Plant Sci 307:110880

    Article  CAS  PubMed  Google Scholar 

  • Li ZY, Qiu LH, Yan HF, Zhou HW, Chen RF, Fan YG (2021) Effect of exogenous gibberellin signal on sugarcane tillering and its endogenous hormones. Chinese J Trop Crops 42(10):2942–2951

    Google Scholar 

  • Li L, Xia T, Li B, Yang H (2022) Hormone and carbohydrate metabolism associated genes play important roles in rhizome bud full-year germination of Cephalostachyum pingbianense. Physiol Plant 174(2):e13674

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Xu J, Ding Y, Wang QS, Li GH, Wang SH (2011) Auxin inhibits the outgrowth of tiller buds in rice (Oryza sativa L.) by downregulating OsIPT expression and cytokinin biosynthesis in nodes. Aust J Crop Sci 5:169–174

    CAS  Google Scholar 

  • Liu J, Shi M, Wang J, Zhang B, Li Y, Wang J (2020) Comparative transcriptomic analysis of the development of sepal morphology in tomato (Solanum lycopersicum L.). Int J Mol Sci 21(16):5914

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Z, Su J, Luo X, Meng J, Zhang H, Li P (2022a) Nitrogen limits zinc-mediated stimulation of tillering in rice by modifying phytohormone balance under low-temperature stress. Food Energy Secur 11(1):e359. https://doi.org/10.1002/fes3.359

    Article  Google Scholar 

  • Liu ZL, Meng JR, Sun ZF, Su JK, Luo XY, Song JM (2022b) b) Zinc application after low temperature stress promoted rice tillers recovery: aspects of nutrient absorption and plant hormone regulation. Plant Sci 314:111104

    Article  CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2 (-Delta Delta C (T)) method. Methods 25(4):402-408

    Article  CAS  PubMed  Google Scholar 

  • Ljung K, Nemhauser JL, Perata P (2015) New mechanistic links between sugar and hormone signalling networks. Curr Opin Plant Biol 25:130–137

    Article  CAS  PubMed  Google Scholar 

  • Lowe GE, Shepherd M, Rose T (2021) Strigolactone analogue GR24 reduces axillary bud out break and growth in tea tree, Melaleuca alternifolia (Maiden and Betche) Cheel. Adv Hortic Sci 35:399–405

    Article  Google Scholar 

  • Luan YX, Wang BS, Zhao Q, Ao G, Yu J (2010) Ectopic expression of foxtail millet zip-like gene, SiPf40, in transgenic rice plants causes a pleiotropic phenotype affecting tillering, vascular distribution and root development. Sci China Life Sci 53(12):1450–1458

    Article  CAS  PubMed  Google Scholar 

  • Luisi A, Lorenzi R, Sorce C (2011) Strigolactone may interact with gibberellin to control apical dominance in pea (Pisum sativum). Plant Growth Regul 65(2):415–419. https://doi.org/10.1007/s10725-011-9603-0

    Article  CAS  Google Scholar 

  • Luo L, Takahashi M, Kameoka H, Qin R, Shiga T, Kanno Y, Seo M, Ito M, Xu G, Kyozuka J (2019) Developmental analysis of the early steps in strigolactone-mediated axillary bud dormancy in rice [J]. Plant J 97(6):1006–1021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lv J, Chen YQ, Ding AM, Lei B, Yu J, Gao XM (2021) Control of axillary bud growth in tobacco through toxin gene expression system. Sci Rep 11(1):17513

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma J, Xie L, Zhao Q, Sun Y, Zhang D (2022) Cyclanilide induces lateral bud outgrowth by modulating cytokinin biosynthesis and signalling pathways in apple identified via transcriptome analysis. Int J Mol Sci 23(2):581

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Manandhar S, Funnell KA, Woolley DJ, Cooney JM (2018) Interaction between strigolactone and cytokinin on axillary and adventitious bud development in Zantedeschia. J Plant Physiol Pathol 6:1

    Google Scholar 

  • Mason MG, Ross JJ, Babst BA, Wienclaw BN, Beveridge CA (2014) Sugar demand, not auxin, is the initial regulator of apical dominance. Proc Natl Acad Sci 111(16):6092–6097

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Min Z, Li Z, Chen L, Zhang Y, Liu M, Yan X (2021) Transcriptome analysis revealed hormone signaling response of grapevine buds to strigolactone. Sci Hortic 283:109936

    Article  CAS  Google Scholar 

  • Müller D, Waldie T, Miyawaki K, To JP, Melnyk CW, Kieber JJ, Kakimoto T, Leyser O (2015) Cytokinin is required for escape but not release from auxin mediated apical dominance. Plant J 82(5):874–886

    Article  PubMed  PubMed Central  Google Scholar 

  • Muñoz A, Pillot JP, Cubas P, Rameau C (2021) Methods for phenotyping shoot branching and testing strigolactone bioactivity for shoot branching in Arabidopsis and Pea. Methods in Molecular Biology (Clifton, N.J.) 2309: 115–127.

  • Negi S, Sukumar P, Liu X, Cohen J, Muday G (2010) Genetic dissection of the role of ethylene in regulating auxin-dependent lateral and adventitious root formation in tomato. Plant J 61(1):3–15

    Article  CAS  PubMed  Google Scholar 

  • Nguyen TQ, Emery RJN (2017) Is ABA the earliest upstream inhibitor of apical dominance? J Exp Bot 68(5):881–884

    Article  CAS  PubMed Central  Google Scholar 

  • Ni J, Gao C, Chen MS, Pan BZ, Ye K, Xu ZF (2015) Gibberellin promotes shoot branching in the perennial woody plant Jatropha curcas. Plant Cell Physiol 56(8):1655–1666

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ni J, Zhao ML, Chen MS, Pan BZ, Tao YB, Xu ZF (2017) Comparative transcriptome analysis of axillary buds in response to the shoot branching regulators gibberellin A3 and 6-benzyladenine in Jatropha curcas. Sci Rep 7(1):11417

    Article  PubMed  PubMed Central  Google Scholar 

  • Ohashi M, Ishiyama K, Kojima S, Kojima M, Sakakibara H, Yamaya T (2017) Lack of cytosolic glutamine synthetase1; 2 activity reduces nitrogen-dependent biosynthesis of cytokinin required for axillary bud outgrowth in rice seedlings. Plant Cell Physiol 58(4):679–690

    Article  CAS  PubMed  Google Scholar 

  • Omoarelojie LO, Kulkarni MG, Finnie JF, Van Staden J (2019) Strigolactone and their crosstalk with other phytohormones. Ann Bot 124(5):749–767

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ono E, Hatayama M, Isono Y, Sato T, Watanabe R, Yonekura-Sakakibara K, Fukuchi-Mizutani M, Tanaka Y, Kusumi T, Nishino T, Nakayama T (2006) Localization of a flavonoid biosynthetic polyphenol oxidase in vacuoles. Plant J 45(2):133–143

    Article  CAS  PubMed  Google Scholar 

  • Parada F, Noriega X, Dantas D, Bressan-Smith R, Pérez FJ (2016) Differences in respiration between dormant and non-dormant buds suggest the involvement of ABA in the development of endodormancy in grapevines. J Plant Physiol 201:71–78

    Article  CAS  PubMed  Google Scholar 

  • Reddy SK, Holalu SV, Casal JJ, Finlayson SA (2013) Abscisic acid regulates axillary bud outgrowth responses to the ratio of red to far-red light. Plant Physiol 163(2):1047–1058

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rong C, Liu Y, Chang Z, Liu Z, Ding Y, Ding C (2022) Cytokinin oxidase/dehydrogenase family genes exhibit functional divergence and overlap in rice growth and development, especially in control of tillering. J Exp Bot 73(11):3552–3568

    Article  CAS  PubMed  Google Scholar 

  • Rubio-Moraga A, Ahrazem O, Pérez-Clemente RM, Gómez-Cadenas A, Yoneyama K, López-Ráez JA (2014) Apical dominance in saffron and the involvement of the branching enzymes CCD7 and CCD8 in the control of bud sprouting. BMC Plant Biol 14:171

    Article  PubMed  PubMed Central  Google Scholar 

  • Ruzicka K, Ljung K, Vanneste S, Podhorská R, Beeckman T, Friml J (2007) Ethylene regulates root growth through effects on auxin biosynthesis and transport-dependent auxin distribution. Plant Cell 19(7):2197–2212

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scaffidi A, Waters MT, Ghisalberti EL, Dxion KW, Flematti GR, Smith SM (2013) Carlactone-independent seedling morphogenesis in Arabidopsis[J]. Plant J 76(1):1–9

    Article  CAS  PubMed  Google Scholar 

  • Schneider A, Godin C, Boudon F, Demotes-Mainard S, Sakr S, Bertheloot J (2019) Light regulation of axillary bud outgrowth along plant axes: an overview of the roles of sugars and hormone. Front Plant Sci 10:1296

    Article  PubMed  PubMed Central  Google Scholar 

  • Shen J, Zhang Y, Ge D, Wang Z, Song W, Gu R (2019) CsBRC1 inhibits axillary bud outgrowth by directly repressing the auxin efflux carrier CsPIN3 in cucumber. Proc Natl Acad Sci 116(34):17105–17114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shi JB, Wang N, Zhou H, Xu QH, Yan GT (2019) The role of gibberellin synthase gene GhGA2ox1 in upland cotton (Gossypium hirsutum L.) responses to drought and salt stress. Biotechnol Appl Biochem 66(3):298–308

    Article  CAS  PubMed  Google Scholar 

  • Shi J, Zhou H, Liu X, Wang N, Xu Q, Yan G (2021) Correlation analysis of the transcriptome and metabolome reveals the role of the flavonoid biosynthesis pathway in regulating axillary buds in upland cotton (Gossypium hirsutum L.). Planta 254(1):7

    Article  CAS  PubMed  Google Scholar 

  • Sirhindi G, Mir MA, Abd-Allah EF, Ahmad P, Gucel S (2016) Jasmonic acid modulates the physio-biochemical attributes, antioxidant enzyme activity, and gene expression in glycine max under nickel toxicity. Front Plant Sci 7:591

    Article  PubMed  PubMed Central  Google Scholar 

  • Stepanova AN, Alonso JM (2009) Ethylene signaling and response: where different regulatory modules mee. Curr Opin Plant Biol 12(5):548–555

    Article  CAS  PubMed  Google Scholar 

  • Tan M, Li G, Liu X, Cheng F, Ma J, Zhao C (2018a) a) Exogenous application of GA3 inactively regulates axillary bud outgrowth by influencing of branching-inhibitors and bud-regulating hormones in apple (Malus domestica Borkh.). Mol Genet Genom 293:1547–1563

    Article  CAS  Google Scholar 

  • Tan M, Li GF, Qi SY, Liu XJ, Chen XL, Ma JJ, Zhang D, Han MY (2018b) b) Identification and expression analysis of the IPT and CKX gene families during axillary bud outgrowth in apple (Males domestica Borkh.). Gene 651:106–117

    Article  CAS  PubMed  Google Scholar 

  • Tan M, Li G, Chen X, Xing L, Ma J, Zhang D (2019) Role of cytokinin, strigolactone, and auxin export on outgrowth of axillary buds in apple. Front Plant Sci 10:616

    Article  PubMed  PubMed Central  Google Scholar 

  • Tenreira T, Lange MJP, Lange T, Bres C, Labadie M, Monfort A (2017) A specific gibberellin 20-oxidase dictates the flowering-runnering decision in diploid strawberry. Plant Cell 29(9):2168–2182

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tischer SV, Wunschel C, Papacek M, Kleigrewe K, Hofmann T, Christmann A (2017) Combinatorial interaction network of abscisic acid receptors and coreceptors from Arabidopsis thalian. Proc Natl Acad Sci 114(38):10280–10285

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vann MC (2017) Soil applied maleic hydrazide does not suppress tobacco axillary bud growth. Crop Forage Turfgrass Manag 3:1–8

    Article  Google Scholar 

  • Vergara R, Noriega X, Aravena KX, Aravena K (2017) ABA represses the expression of cell cycle genes and may modulate the development of endodormancy in grapevine buds. Front Plant Sci 8:812

    Article  PubMed  PubMed Central  Google Scholar 

  • Waldie T, Leyser O (2018) Cytokinin targets auxin transport to promote shoot branching. Plant Physiol 177(2):803–818

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Yao R (2019) Increased endogenous indole-3-acetic acid: abscisic acid ratio is a reliable marker of Pinus massoniana rejuvenation. Biotech Histochem 94(7):546–553

    Article  CAS  PubMed  Google Scholar 

  • Wang D, Gao Z, Du P, Xiao W, Tan Q, Chen X (2016) Expression of ABA metabolism-related genes suggests similarities and differences between seed dormancy and bud dormancy of peach (Prunus persica). Front Plant Sci 6:1248

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang J, Lu K, Nie H, Zeng Q, Wu B, Qian J (2018) Rice nitrate transporter OsNPF7.2 positively regulates tiller number and grain yield. Rice 11(1):12

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang R, Qian J, Fang Z, Tang J (2020) Transcriptomic and physiological analyses of rice seedlings under different nitrogen supplies provide insight into the regulation involved in axillary bud outgrowth. BMC Plant Biol 20(1):197

    Article  PubMed  PubMed Central  Google Scholar 

  • Waters MT, Brewer PB, Bussell JD, Smith SM, Beveridge CA (2012a) The Arabidopsis ortholog of rice DWARF27 acts upstream of MAX1 in the control of plant development by strigolactone. Plant Physiol 159(3):1073–1085

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Waters MT, Nelson DC, Scaffidi A, Flematti GR, Sun YK, Dixon KW, Smith SM (2012b) Specialisation within the DWARF14 protein family confers distinct responses to karrikins and strigolactones in Arabidopsis. Development (cambridge, England) 139(7):1285–1295

    Article  CAS  PubMed  Google Scholar 

  • Waters MT, Nelson DC, Scaffidi A, Flematti GR, Sun YK, Dixon KW, Smith SM, Wen C, Zhao Q, Nie J, Liu G, Shen L, Cheng C (2016) Physiological controls of chrysanthemum DgD27 gene expression in regulation of shoot branching. Plant Cell Rep 35(5):1053–1070

    Article  Google Scholar 

  • Wigchert SCM, Zwanenburg BA (1999) critical account on the inception of Striga seed germination. J Agric Food Chem 47(4):1320–1325

    Article  CAS  PubMed  Google Scholar 

  • Xia F, Sun T, Yang S, Wang X, Chao J, Li X (2019) Insight into the B3transcription factor superfamily and expression profiling of B3 genes in axillary buds after topping in tobacco (Nicotiana tabacum L.). Genes 10(2):164

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xia X, Dong H, Yin Y, Song X, Gu X, Sang K, Zhou J, Shi K, Zhou Y, Foyer CH, Yu J (2021) Brassinosteroid signaling integrates multiple pathways to release apical dominance in tomato. Proc Natl Acad Sci USA 118(11):e2004384118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu J, Zha M, Li Y, Ding Y, Chen L, Ding C (2015) The interaction between nitrogen availability and auxin, cytokinin, and strigolactone in the control of shoot branching in rice (Oryza sativa L.). Plant Cell Rep 34(9):1647–1662

    Article  CAS  PubMed  Google Scholar 

  • Xu J, Li Q, Yang L, Li X, Wang Z, Zhang Y (2020) Changes in carbohydrate metabolism and endogenous hormone regulation during bulblet initiation and development in Lycoris radiata. BMC Plant Biol 20(1):180

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang H, Xu F, Liao H, Pan W, Zhang W, Xu B (2021) Transcriptome and metabolite analysis related to branch development in two genotypes of Eucalyptus urophylla. Mol Genet Genom 296:1071–1083

    Article  CAS  Google Scholar 

  • Yao C, Finlayson SA (2015) Abscisic acid is a general negative regulator of Arabidopsis axillary bud growth. Plant Physiol 169(1):611–626

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoneyama K, Brewer PB (2021) Strigolactone, how are they synthesized to regulate plant growth and development? Curr Opin Plant Biol 63:102072

    Article  CAS  PubMed  Google Scholar 

  • Yu C, Chen W, Wang Z, Lou H (2021) Comparative proteomic analysis of tomato (Solanum lycopersicum L.) shoots reveals crosstalk between strigolactone and auxin. Genomics 113(5):3163–3173

    Article  CAS  PubMed  Google Scholar 

  • Yue P, Wang Y, Bu H, Li X, Yuan H, Wang A (2019) Ethylene promotes IAA reduction through PuERFs-activated PuGH31 during fruit ripening in pear (Pyrus ussuriensis). Postharvest Biol Technol 157:110955

    Article  CAS  Google Scholar 

  • Zha M, Imran M, Wang Y, Xu DY, Wang S (2019) Transcriptome analysis revealed the interaction among strigolactone, auxin, and cytokinin in controlling the shoot branching of rice. Plant Cell Rep 38(3):279–293

    Article  CAS  PubMed  Google Scholar 

  • Zhao B, Wu TT, Ma SS, Jiang DJ, Bie XM, Sui N (2020) TaD27-B gene controls the tiller number in hexaploid wheat. Plant Biotechnol J 18(2):513–525

    Article  CAS  PubMed  Google Scholar 

  • Zhao Y, Feng Y, Sun P, Wang B, Qiao J, Duan W (2021) Responses of phytohormones, carbon and nitrogen status to the trunk-extension pruning in three-year-old paulownia plantation. J Animal Plant Sci 31(2):450–458

    CAS  Google Scholar 

  • Zhuang W, Gao Z, Wang L, Zhong W, Ni Z, Zhang Z (2013) Comparative proteomic and transcriptomic approaches to address the active role of GA4 in Japanese apricot flower bud dormancy release. J Exp Bot 64(16):4953–4966

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhuang L, Wang J, Huang B (2017) Drought inhibition of tillering in Festuca arundinacea associated with axillary bud development and strigolactone signaling. Environ Exp Bot 142:15–23

    Article  CAS  Google Scholar 

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Funding

This study was funded by the National Natural Science Foundation of China (Grant No. 32060420).

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HYT was responsible for experimental implementation, data analysis and manuscript drafting. BXT carried out the experiment and contributed to the reagents / materials / analytical tools; WWF carried out the experiment and participated in data collection; ZYP participated in data collection; YXW and FL participated in data analysis; JTP helped to revise the manuscript; GQL initiated and supervised the study. All authors read and approved the final manuscript.

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Correspondence to Guoqin Liu.

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Communicated by Zsuzsanna Kolbert.

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Tian, H., Tang, B., Fan, W. et al. The role of strigolactone analog (GR24) in endogenous hormone metabolism and hormone-related gene expression in tobacco axillary buds. Plant Cell Rep 43, 21 (2024). https://doi.org/10.1007/s00299-023-03081-y

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