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Genome-wide identification and analysis of the evolution and expression pattern of the SBP gene family in two Chimonanthus species

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Abstract

Background

Chimonanthus praecox and Chimonanthus salicifolius are closely related species that diverged approximately six million years ago. While both C. praecox and C. salicifolius could withstand brief periods of low temperatures of – 15 °C. Their flowering times are different, C. praecox blooms in early spring, whereas C. salicifolius blooms in autumn. The SBP-box (SQUAMOSA promoter-binding protein) is a plant-specific gene family that plays a crucial vital role in regulating plant flowering. Although extensively studied in various plants, the SBP gene family remains uncharacterized in Calycanthaceae.

Methods and results

We conducted genome-wide identification of SBP genes in both C. praecox and C. salicifolius and comprehensively characterized the chromosomal localization, gene structure, conserved motifs, and domains of the identified SBP genes. In total, 15 and 18 SBP genes were identified in C. praecox and C. salicifolius, respectively. According to phylogenetic analysis, the SBP genes from Arabidopsis, C. praecox, and C. salicifolius were clustered into eight groups. Analysis of the gene structure and conserved protein motifs showed that SBP proteins of the same subfamily have similar motif structures. The expression patterns of SBP genes were analyzed using transcriptome data. The results revealed that more than half of the genes exhibited lower expression levels in leaves than in flowers, suggesting their potential involvement in the flower development process and may be linked to the winter and autumn flowering of C. praecox and C. salicifolius.

Conclusion

Thirty-three SBPs were identified in C. praecox and C. salicifolius. The evolutionary characteristics and expression patterns were examined in this study. These results provide valuable information to elucidate the evolutionary relationships of the SBP family and help determine the functional characteristics of the SBP genes in subsequent studies.

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Data availability

The dataset generated or analyzed in this study is included in this article and its supplementary information files.

References

  1. Zhou Q, Zhang S, Chen F, Liu B, Wu L, Li F, Zhang J, Bao M, Liu G (2018) Genome-wide identification and characterization of the SBP-box gene family in Petunia. BMC Genom 19(1):193. https://doi.org/10.1186/s12864-018-4537-91

    Article  Google Scholar 

  2. Loconte H, Stevenson DW (1991) (1991) Cladistics of the magnoliidae. Cladistics 7(3):267–296

    Article  PubMed  Google Scholar 

  3. Lv Q, Qiu J, Liu J, Li Z, Zhang W, Wang Q et al (2020) (2020) The Chimonanthus salicifolius genome provides insight into magnoliid evolution and flavonoid biosynthesis. Plant J 103(5):1910–1923. https://doi.org/10.1111/tpj.14874

    Article  CAS  PubMed  Google Scholar 

  4. Crepet WL, Nixon KC, Gandolfo MA (2005) An extinct calycanthoid taxon, Jerseyanthus calycanthoides, from the late cretaceous of New Jersey. Am J Bot 92(9):1475–1485. https://doi.org/10.3732/ajb.92.9.1475

    Article  PubMed  Google Scholar 

  5. Chen J, Hao Z, Guang X, Zhao C, Wang P, Xue L et al (2019) (2019) Liriodendron genome sheds light on angiosperm phylogeny and species-pair differentiation. Nat Plants 5(1):18–25. https://doi.org/10.1038/s41477-018-0323-6

    Article  CAS  PubMed  Google Scholar 

  6. Renner SS (1999) (1999) Circumscription and phylogeny of the Laurales: evidence from molecular and morphological data. Am J Bot 86(9):1301–1315

    Article  CAS  PubMed  Google Scholar 

  7. Jamal A, Wen J, Ma ZY, Ahmed I, Abdullah CL et al (2021) Comparative chloroplast genome analyses of the winter-blooming Eastern Asian endemic genus Chimonanthus (Calycanthaceae) with implications for its phylogeny and diversification. Front Genet 12:709996. https://doi.org/10.3389/fgene.2021.709996

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Worboys SJ, Jackes BR (2005) (2005) Pollination Processes in Idiospermum australiense (Calycanthaceae), an arborescent basal angiosperm of Australia’s tropical rain forests. Plant Syst Evol 251(2/4):107–117

    Article  Google Scholar 

  9. Porwal MK (2002) Relative economics of weed management systems in winter sweet potato (Ipomoea batatus L.) in command area of Southern Rajasthan. Indian J Weed Sci 34:88–91

    Google Scholar 

  10. Hiromitsu T, Yohei M, Kyohei M, Atsushi I, Mariko K, Norio A (2003) (2003) Isolation, structure elucidation, and total synthesis of two new Chimonanthus alkaloids, chimonamidine and chimonanthidine. Tetrahedron 60(4):893–900

    Google Scholar 

  11. Li Y, Dong X (2008) (2008) Distinctions and applications wintersweet and Chinese plums in landscaping. For Ecol Sci 03:324–326

    Google Scholar 

  12. Ye Y, Ye L (2015) The Research summary and application prospect of Chimonanthus salicifolius S.Y.H. J Huangshan Univ 17(05):68–71

    Google Scholar 

  13. Shang J, Tian J, Cheng H, Yan Q, Li L, Jamal A et al (2020) The chromosome-level wintersweet (Chimonanthus praecox) genome provides insights into floral scent biosynthesis and flowering in winter. Genome Biol 21(1):200. https://doi.org/10.1186/s13059-020-02088-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Wang N, Chen H, Xiong L, Liu X, Li X, An Q et al (2018) Phytochemical profile of ethanolic extracts of Chimonanthus salicifolius S. Y. Hu. leaves and its antimicrobial and antibiotic-mediating activity. Ind Crops Prod 125:328–334. https://doi.org/10.1016/j.indcrop.2018.09.021

    Article  CAS  Google Scholar 

  15. Li S-L, Zou Z-R (2018) Research progress on flavonoids and coumarins from Chimonanthus plants and its pharmacological activities. Chin Tradit Herbal Drugs 24:3425–3430

    Google Scholar 

  16. Wang K, Li D, Wu B, Cao X (2016) New cytotoxic dimeric and trimeric coumarins from Chimonanthus salicifolius. Phytochem Lett 16:115–120. https://doi.org/10.1016/j.phytol.2016.03.009

    Article  CAS  Google Scholar 

  17. Zhou X-L, Yu Y, Zhou C, Li S, Zhu Y-G, Xiao-Ling Y (2014) Anti-depression effect of Chimonanthus salicifolicus essential oil in chronic stressed rats. J Med Plants Res 8(10):430–435

    Article  Google Scholar 

  18. Guo AY, Zhu QH, Gu X, Ge S, Yang J, Luo J (2008) Genome-wide identification and evolutionary analysis of the plant specific SBP-box transcription factor family. Gene 418(1–2):1–8. https://doi.org/10.1016/j.gene.2008.03.016

    Article  CAS  PubMed  Google Scholar 

  19. Chang JZ, Yan FX, Qiao LY, Zheng J, Zhang FY, Liu QS (2016) Genome-wide identification and expression analysis of SBP-box gene family in Sorghum bicolor L. Hereditas 38(6):569–580. https://doi.org/10.16288/j.yczz.16-008

    Article  PubMed  Google Scholar 

  20. Valassakis C, Livanos P, Minopetrou M, Haralampidis K, Roussis A (2018) Promoter analysis and functional implications of the selenium binding protein (SBP) gene family in Arabidopsis thaliana. J Plant Physiol 2018:224–225

    Google Scholar 

  21. Mmadi M, Dossa K, Wang L, Zhou R, Wang Y, Cisse N et al (2017) Functional characterization of the versatile MYB Gene family uncovered their important roles in plant development and responses to drought and waterlogging in sesame. Genes 8(12):362

    Article  PubMed  PubMed Central  Google Scholar 

  22. Yong Z, Lingli G, Guanghua L, Lunwei J, Yingui Y (2018) Characterization and expression analysis of growth regulating factor (GRF) family genes in cucumber. Archives of Biol Sci 70(4):629–637

    Article  Google Scholar 

  23. Song S, Zhou H, Sheng S, Cao M, Li Y, Pang X (2017) Genome-wide organization and expression profiling of the SBP-box gene family in Chinese Jujube (Ziziphus jujuba Mill.). Int J Mol Sci 8(8):1734

    Article  Google Scholar 

  24. Zhou Q, Zhang S, Chen F, Liu B, Wu L, Li F et al (2018) (2018) Genome-wide identification and characterization of the SBP-box gene family in Petunia. BMC Genom 19(1):193. https://doi.org/10.1186/s12864-018-4537-9

    Article  CAS  Google Scholar 

  25. Tripathi RK, Overbeek W, Singh J (2020) Global analysis of SBP gene family in Brachypodium distachyon reveals its association with spike development. Sci Rep. https://doi.org/10.1038/s41598-020-72005-7

    Article  PubMed  PubMed Central  Google Scholar 

  26. Science; Reports on Science from McGill University Provide New Insights (Global analysis of SBP gene family in Brachypodium distachyon reveals its association with spike development). Science Letter. 2020.

  27. Teng MR, Wang XY, Li H et al (2021) Identification and expression analysis of the SBP-box gene family related to abiotic stress in tea plant (Camellia sinensis (L.) O. Kuntze). Plant Mol Biol Rep 40(1):1418–2162

    Google Scholar 

  28. Valassakis C, Livanos P, Minopetrou M, Haralampidis K, Roussis A (2018) (2018) Promoter analysis and functional implications of the selenium binding protein (SBP) gene family in Arabidopsis thaliana. J Plant Physiol 224–225:19–29. https://doi.org/10.1016/j.jplph.2018.03.008

    Article  CAS  PubMed  Google Scholar 

  29. Cheng H, Hao M, Wang W, Mei D, Tong C, Wang H et al (2016) (2016) Genomic identification, characterization and differential expression analysis of SBP-box gene family in Brassica napus. BMC Plant Biol 16(1):196. https://doi.org/10.1186/s12870-016-0852-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Salinas M, Xing S, Höhmann S, Berndtgen R, Huijser P (2012) (2012) Genomic organization, phylogenetic comparison and differential expression of the SBP-box family of transcription factors in tomato. Planta 235(6):1171–1184. https://doi.org/10.1007/s00425-011-1565-y

    Article  CAS  PubMed  Google Scholar 

  31. Cardon G, Höhmann S, Klein J, Nettesheim K, Saedler H, Huijser P (1999) (1999) Molecular characterisation of the Arabidopsis SBP-box genes. Gene 237(1):91–104. https://doi.org/10.1016/s0378-1119(99)00308-x

    Article  CAS  PubMed  Google Scholar 

  32. Li J, Hou H, Li X, Xiang J, Yin X, Gao H et al (2013) Genome-wide identification and analysis of the SBP-box family genes in apple (Malus × domestica Borkh.). Plant Physiol Biochem: PPB. 70:100–114. https://doi.org/10.1016/j.plaphy.2013.05.021

    Article  CAS  PubMed  Google Scholar 

  33. Zhang X, Dou L, Pang C, Song M, Wei H, Fan S et al (2015) (2015) Genomic organization, differential expression, and functional analysis of the SPL gene family in Gossypium hirsutum. Mol Genet Genom 290(1):115–126. https://doi.org/10.1007/s00438-014-0901-x

    Article  CAS  Google Scholar 

  34. Han YY, Ma YQ, Li DZ, Yao JW, Xu ZQ (2016) Characterization and phylogenetic analysis of fifteen NtabSPL genes in Nicotiana tabacum L. cv. Qinyan95. Develop Genes Evol 226(1):1–14. https://doi.org/10.1007/s00427-015-0522-3

    Article  CAS  Google Scholar 

  35. Pan F, Wang Y, Liu H, Wu M, Chu W, Chen D et al (2017) 2017) Genome-wide identification and expression analysis of SBP-like transcription factor genes in Moso Bamboo (Phyllostachys edulis. BMC Genom 18(1):486. https://doi.org/10.1186/s12864-017-3882-4

    Article  CAS  Google Scholar 

  36. Hou H, Li J, Gao M, Singer SD, Wang H, Mao L et al (2013) Genomic organization, phylogenetic comparison and differential expression of the SBP-box family genes in grape. PLoS ONE 8(3):e59358. https://doi.org/10.1371/journal.pone.0059358

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Li C, Lu S (2014) (2014) Molecular characterization of the SPL gene family in Populus trichocarpa. BMC Plant Biol 14:131. https://doi.org/10.1186/1471-2229-14-131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Zhang HX, Jin JH, He YM, Lu BY, Li DW, Chai WG et al (2016) Genome-wide identification and analysis of the SBP-Box family genes under phytophthora capsici stress in pepper (Capsicum annuum L.). Front Plant Sci 7:504. https://doi.org/10.3389/fpls.2016.00504

    Article  PubMed  PubMed Central  Google Scholar 

  39. He F, Long R, Wei C, Zhang Y, Li M, Kang J et al (2022) Genome-wide identification, phylogeny and expression analysis of the SPL gene family and its important role in salt stress in Medicago sativa L. BMC Plant Biol 22(1):295. https://doi.org/10.1186/s12870-022-03678-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Kavas M, Kızıldoğan AK, Abanoz B (2017) Comparative genome-wide phylogenetic and expression analysis of SBP genes from potato (Solanum tuberosum. Comput Biol Chem 67:131–140. https://doi.org/10.1016/j.compbiolchem.2017.01.001

    Article  CAS  PubMed  Google Scholar 

  41. Lai D, Fan Y, Xue G, He A, Yang H, He C et al (2022) Genome-wide identification and characterization of the SPL gene family and its expression in the various developmental stages and stress conditions in foxtail millet (Setaria italic). BMC Genom 23(1):389. https://doi.org/10.1186/s12864-022-08633-2

    Article  CAS  Google Scholar 

  42. Yang Z, Wang X, Gu S, Hu Z, Xu H, Xu C (2008) Comparative study of SBP-box gene family in Arabidopsis and rice. Gene 407(1–2):1–11. https://doi.org/10.1016/j.gene.2007.02.034

    Article  CAS  PubMed  Google Scholar 

  43. Jung JH, Lee HJ, Ryu JY, Park CM (2016) SPL3/4/5 integrate developmental aging and photoperiodic signals into the FT-FD module in Arabidopsis flowering. Mol Plant 9(12):1647–1659. https://doi.org/10.1016/j.molp.2016.10.014

    Article  CAS  PubMed  Google Scholar 

  44. Zheng C, Ye M, Sang M, Wu R (2019) A Regulatory Network for miR156-SPL Module in Arabidopsis thaliana. Int J Mol Sci 20(24):6166

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Mingli X, Tieqiang H, Jianfei Z, Mee-Yeon P, Earley KW, Wu G et al (2016) Developmental Functions of miR156-Regulated SQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL) Genes in Arabidopsis thaliana. PLoS Genet 12(8):e1006263

    Article  Google Scholar 

  46. Gang W, Scott PR (2006) (2006) Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3. Development 133(18):3539–3547

    Article  Google Scholar 

  47. Cardon GH, Hohmann S, Nettesheim K, Saedler H, Huijser P (1997) Functional analysis of the Arabidopsis thaliana SBP-box gene SPL3: a novel gene involved in the floral transition. The Plant J 12(2):367–377

    Article  CAS  PubMed  Google Scholar 

  48. Yamaguchi N, Winter CM, Wu MF, Kanno Y, Yamaguchi A, Seo M et al (2014) (2014) Gibberellin acts positively then negatively to control onset of flower formation in Arabidopsis. Science 344(6184):638–641. https://doi.org/10.1126/science.1250498

    Article  CAS  PubMed  Google Scholar 

  49. Schwarz S, Grande AV, Bujdoso N, Saedler H, Huijser P (2008) (2008) The microRNA regulated SBP-box genes SPL9 and SPL15 control shoot maturation in Arabidopsis. Plant Mol Biol 67(1–2):183–195. https://doi.org/10.1007/s11103-008-9310-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Li L, Shi F, Wang Y, Yu X, Zhi J, Guan Y et al (2020) TaSPL13 regulates inflorescence architecture and development in transgenic wheat (Triticum aestivum L. ). Plant Sci 296:110516

    Article  CAS  PubMed  Google Scholar 

  51. Song J, Ma D, Yin J, Yang L, He Y, Zhu Z et al (2019) Genome-wide characterization and expression profiling of squamosa promoter binding protein-like (SBP) transcription factors in wheat (Triticum aestivum L.). Agronomy 9(9):527

    Article  CAS  Google Scholar 

  52. Singh RP, Jha PN (2016) Mitigation of salt stress in wheat plant (Triticum aestivum) by ACC deaminase bacterium Enterobacter sp. SBP-6 isolated from Sorghum bicolor. Acta Physiol Plant 38(5):110

    Article  Google Scholar 

  53. Singh RP, Jha P, Jha PN (2015) The plant-growth-promoting bacterium Klebsiella sp. SBP-8 confers induced systemic tolerance in wheat (Triticum aestivum ) under salt stress. J Plant Physiol 184(2015):57–67

    Article  CAS  PubMed  Google Scholar 

  54. Li Y, Song Q, Zhang Y, Li Z, Guo J, Chen X et al (2020) Genome-wide identification, characterization, and expression patterns analysis of the SBP-box gene family in wheat (Triticum aestivum L.). Scientific Rep 10(1):17250. https://doi.org/10.1038/s41598-020-74417-x

    Article  CAS  Google Scholar 

  55. Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He Y et al (2020) (2020) TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant 13(8):1194–1202

    Article  CAS  PubMed  Google Scholar 

  56. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874. https://doi.org/10.1093/molbev/msw054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Zhang Y, Tang D, Lin X, Ding M, Tong Z (2018) (2018) Genome-wide identification of MADS-box family genes in moso bamboo (Phyllostachys edulis) and a functional analysis of PeMADS5 in flowering. BMC Plant Biol 18(1):176. https://doi.org/10.1186/s12870-018-1394-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Bolger AM, Lohse M, Usadel B (2014) (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30(15):2114–2120. https://doi.org/10.1093/bioinformatics/btu170

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Mizoguchi T, Wright L, Fujiwara S, Cremer F, Lee K, Onouchi H et al (2005) (2005) Distinct roles of GIGANTEA in promoting flowering and regulating circadian rhythms in Arabidopsis. Plant Cell 17(8):2255–2270. https://doi.org/10.1105/tpc.105.033464

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Fowler S, Lee K, Onouchi H, Samach A, Richardson K, Morris B et al (1999) GIGANTEA: a circadian clock-controlled gene that regulates photoperiodic flowering in Arabidopsis and encodes a protein with several possible membrane-spanning domains. EMBO J 18(17):4679–5688. https://doi.org/10.1093/emboj/18.17.4679

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Putterill J, Robson F, Lee K, Simon R, Coupland G (1995) (1995) The CONSTANS gene of Arabidopsis promotes flowering and encodes a protein showing similarities to zinc finger transcription factors. Cell 80(6):847–857. https://doi.org/10.1016/0092-8674(95)90288-0

    Article  CAS  PubMed  Google Scholar 

  62. Wang Q, Liu M, Quan S, Shi Q, Tian T, Zhang H et al (2023) FAR-RED ELONGATED HYPOCOTYL3 increases leaf longevity by delaying senescence in arabidopsis. Plant, Cell Environ 46(5):1582–1595. https://doi.org/10.1111/pce.14554

    Article  CAS  PubMed  Google Scholar 

  63. Qin SW, Bao LH, He ZG, Li CL, La HG, Zhao LF (2022) Identification and regulatory network analysis of SPL family transcription factors in Populus euphratica Oliv heteromorphic leaves. Sci Rep 12(1):2856. https://doi.org/10.1038/s41598-022-06942-w

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Preston JC, Hileman LC (2013) Functional evolution in the plant SQUAMOSA-PROMOTER BINDING PROTEIN-LIKE (SPL) gene family. Front Plant Sci 4:80. https://doi.org/10.3389/fpls.2013.00080

    Article  PubMed  PubMed Central  Google Scholar 

  65. Li J, Gao X, Sang S, Liu C (2019) Genome-wide identification, phylogeny, and expression analysis of the SBP-box gene family in Euphorbiaceae. BMC Genomics 20:912. https://doi.org/10.1186/s12864-019-6319-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Li X, Fan Z, Guo H, Ye N, Lyu T, Yang W et al (2018) (2018) Comparative genomics analysis reveals gene family expansion and changes of expression patterns associated with natural adaptations of flowering time and secondary metabolism in yellow Camellia. Funct Integr Genom 18(6):659–671. https://doi.org/10.1007/s10142-018-0617-9

    Article  CAS  Google Scholar 

  67. Ma J, Nie G, Yang Z, Ma S, Fan J, Hu R et al (2022) Genome-wide identification, characterization, and expression profiling analysis of SPL gene family during the inflorescence development in Trifolium repens. Genes (Basel) 13(5):900. https://doi.org/10.3390/genes13050900

    Article  CAS  PubMed  Google Scholar 

  68. Zhang Y, Schwarz S, Saedler H, Huijser P (2007) (2007) SPL8, a local regulator in a subset of gibberellin-mediated developmental processes in Arabidopsis. Plant Mol Biol 63(3):429–439. https://doi.org/10.1007/s11103-006-9099-6

    Article  CAS  PubMed  Google Scholar 

  69. Unte US, Sorensen AM, Pesaresi P, Gandikota M, Leister D, Saedler H et al (2003) (2003) SPL8, an SBP-box gene that affects pollen sac development in Arabidopsis. Plant Cell 15(4):1009–1019. https://doi.org/10.1105/tpc.010678

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Shikata M, Koyama T, Mitsuda N, Ohme-Takagi M (2009) (2009) Arabidopsis SBP-box genes SPL10, SPL11 and SPL2 control morphological change in association with shoot maturation in the reproductive phase. Plant Cell Physiol 50(12):2133–2145. https://doi.org/10.1093/pcp/pcp148

    Article  CAS  PubMed  Google Scholar 

  71. Chao LM, Liu YQ, Chen DY, Xue XY, Mao YB, Chen XY (2017) (2017) Arabidopsis transcription factors SPL1 and SPL12 Confer Plant Thermotolerance at Reproductive Stage. Mol Plant 10(5):735–748. https://doi.org/10.1016/j.molp.2017.03.010

    Article  CAS  PubMed  Google Scholar 

  72. Zhang SD, Ling LZ (2014) Genome-wide identification and evolutionary analysis of the SBP-box gene family in castor bean. PLoS ONE 9(1):e86688. https://doi.org/10.1371/journal.pone.0086688

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Yao T, Park BS, Mao HZ, Seo JS, Ohama N, Li Y et al (2019) Regulation of flowering time by SPL10/MED25 module in Arabidopsis. New Phytol 224(1):493–504. https://doi.org/10.1111/nph.15954

    Article  CAS  PubMed  Google Scholar 

  74. Gao R, Wang Y, Gruber MY, Hannoufa A (2017) (2017) miR156/SPL10 modulates lateral root development, branching and leaf morphology in Arabidopsis by silencing AGAMOUS-LIKE 79. Front Plant Sci 8:2226. https://doi.org/10.3389/fpls.2017.02226

    Article  PubMed  Google Scholar 

  75. Cardon GH, Höhmann S, Nettesheim K, Saedler H, Huijser P (1997) Functional analysis of the Arabidopsis thaliana SBP-box gene SPL3: a novel gene involved in the floral transition. Plant J 12(2):367–377. https://doi.org/10.1046/j.1365-313x.1997.12020367.x

    Article  CAS  PubMed  Google Scholar 

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Funding

This work was supported by Open Fund of Zhejiang Provincial Key Laboratory of Germplasm Innovation and Utilization for Garden Plants (2020E10013-K202104), Research Development Fund of Zhejiang A&F University (2019FR028), and "Fourteenth Five-Year Plan" major scientific and technological project of new agricultural varieties breeding-new flower varieties breeding (2021C02071-5).

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  1. Ge-Ge Jiang, Qian-Qian Wan, and Wei-Zou have contributed equally to this work.

Authors and Affiliations

  1. School of Landscape Architecture, Zhejiang Agriculture and Forestry University, Hangzhou, 311100, China

    Ge-Ge Jiang, Qian-Qian Wan, Wei Zou, Gui-Ting Hu, Li-Yuan Yang & Hui-Juan Ning

  2. Hubei Key Laboratory of Economic Forest Germplasm Improvement and Resources Comprehensive Utilization, College of Biology and Agricultural Resources, Huanggang Normal University, Huanggang, 438000, China

    Li-Yuan Yang & Li Zhu

  3. Zhejiang Provincial Key Laboratory of Germplasm Innovation and Utilization for Garden Plants, Zhejiang Agriculture & Forestry University, Hangzhou, 311300, China

    Hui-Juan Ning

  4. Key Laboratory of National Forestry and Grassland Administration On Germplasm Innovation and Utilization for Southern Garden Plants, Zhejiang Agriculture & Forestry University, Hangzhou, 311300, China

    Hui-Juan Ning

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HN, LY, and LZ designed the experiments and wrote the manuscript. GJ, QW, WZ, FG, and DW analyzed the data. All authors contributed to the article and approved the submitted version.

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Jiang, GG., Wan, QQ., Zou, W. et al. Genome-wide identification and analysis of the evolution and expression pattern of the SBP gene family in two Chimonanthus species. Mol Biol Rep 50, 9107–9119 (2023). https://doi.org/10.1007/s11033-023-08799-2

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