Abstract
SQUAMOSA promoter-binding protein (SBP) genes are important transcription factors involved in plant growth and development. However, the information about mungbean VrSBP genes is limited. In this study, we identified and characterized 22 VrSBP genes in the mungbean genome. Many characteristics of VrSBP genes were analyzed, and most VrSBP genes were considered to be expressed only in the nucleus. VrSBP genes were grouped into 9 subfamilies, with the exception of the g7 and ms subfamilies which are distinctive to Poaceae species. The g3 subfamily was the largest one with 6 VrSBP members. Eight segmental events were found among VrSBP genes, and all VrSBP duplicated genes were evolved via purification selection. The gene structure of VrSBP genes in the same subfamily was similar, and the conserved motifs are different among different subfamilies of VrSBP genes. Additionally, 12 VrSBP genes were considered to be the target genes of vra-miR156a. The types and numbers of cis-acting elements in VrSBP promoters were varied and VrSBP genes showed different expression patterns in different tissues. In addition, the protein interaction network revealed that VrSBP genes were involved in many development processes. Our study has provided important information which will allow the further functional characterization of VrSBP genes.
Similar content being viewed by others
References
Abellan A, Dominguez-Perles R, Moreno DA, Garcia-Viguera C (2019) Sorting out the value of cruciferous sprouts as sources of bioactive compounds for nutrition and health. Nutrients 11(2):429. https://doi.org/10.3390/nu11020429
Allen E, Xie Z, Gustafson AM, Sung GH, Spatafora JW, Carrington JC (2004) Evolution of microRNA genes by inverted duplication of target gene sequences in Arabidopsis thaliana. Nat Genet 36(12):1282–1290. https://doi.org/10.1038/ng1478
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215(3):403–410. https://doi.org/10.1016/S0022-2836(05)80360-2
Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37:W202–W208. https://doi.org/10.1093/nar/gkp335
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. Plant J 12(2):367–377. https://doi.org/10.1046/j.1365-313x.1997.12020367.x
Cardon G, Hohmann S, Klein J, Nettesheim K, Saedler H, Huijser P (1999) Molecular characterisation of the Arabidopsis SBP-box genes. Gene 237(1):91–104. https://doi.org/10.1016/s0378-1119(99)00308-x
Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He Y, Xia R (2020) TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant 13(8):1194–1202. https://doi.org/10.1016/j.molp.2020.06.009
Chou KC, Shen HB (2007) Large-scale plant protein subcellular location prediction. J Cell Biochem 100(3):665–678. https://doi.org/10.1002/jcb.21096
Chou KC, Shen HB (2008) Cell-PLoc: a package of Web servers for predicting subcellular localization of proteins in various organisms. Nat Protoc 3(2):153–162. https://doi.org/10.1038/nprot.2007.494
Chou KC, Shen HB (2010) Plant-mPLoc: a top-down strategy to augment the power for predicting plant protein subcellular localization. PLoS ONE 5(6):e11335. https://doi.org/10.1371/journal.pone.0011335
Crooks GE, Hon G, Chandonia JM, Brenner SE (2004) WebLogo: a sequence logo generator. Genome Res 14(6):1188–1190. https://doi.org/10.1101/gr.849004
Duvaud S, Gabella C, Lisacek F, Stockinger H, Ioannidis V, Durinx C (2021) Expasy, the swiss bioinformatics resource portal, as designed by its users. Nucleic Acids Res 49(W1):W216–W227. https://doi.org/10.1093/nar/gkab225
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32(5):1792–1797. https://doi.org/10.1093/nar/gkh340
Fahlgren N, Carrington JC (2010) miRNA target prediction in plants. Methods Mol Biol 592:51–57. https://doi.org/10.1007/978-1-60327-005-2_4
Gou J, Felippes FF, Liu C, Weigel D, Wang J (2011) Negative regulation of anthocyanin biosynthesis in Arabidopsis by a miR156-targeted SPL transcription factor. Plant Cell 23(4):1512–1522. https://doi.org/10.1105/tpc.111.084525
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
Hou D, Yousaf L, Xue Y, Hu J, Wu J, Hu X, Feng N, Shen Q (2019) Mung Bean (Vigna radiata L.): bioactive polyphenols, polysaccharides, peptides, and health benefits. Nutrients 11(6):1238. https://doi.org/10.3390/nu11061238
Hu B, Jin J, Guo AY, Zhang H, Luo J, Gao G (2015) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31(8):1296–1297. https://doi.org/10.1093/bioinformatics/btu817
Hu L, Zhang X, Ni H, Yuan F, Zhang S (2023) Identification and functional analysis of CAD gene family in Pomegranate (Punica granatum). Genes 14:26. https://doi.org/10.3390/genes14010026
Jia K, Yan C, Zhang J, Cheng Y, Li W, Yan H, Gao J (2021) Genome-wide identification and expression analysis of the JAZ gene family in turnip. Sci Rep 11(1):21330. https://doi.org/10.1038/s41598-021-99593-2
Jung JH, Ju Y, Seo PJ, Lee JH, Park CM (2012) The SOC1-SPL module integrates photoperiod and gibberellic acid signals to control flowering time in Arabidopsis. Plant J 69(4):577–588. https://doi.org/10.1111/j.1365-313X.2011.04813.x
Kang YJ, Kim SK, Kim MY, Lestari P, Kim KH, Ha BK, Jun TH, Hwang WJ, Lee T, Lee J, Shim S, Yoon MY, Jang YE, Han KS, Taeprayoon P, Yoon N, Somta P, Tanya P, Kim KS, Gwag JG, Moon JK, Lee YH, Park BS, Bombarely A, Doyle JJ, Jackson SA, Schafleitner R, Srinives P, Varshney RK, Lee SH (2014) Genome sequence of mungbean and insights into evolution within Vigna species. Nat Commun 5:5443. https://doi.org/10.1038/ncomms6443
Ke J, Ma H, Gu X, Thelen A, Brunzelle JS, Li J, Xu HE, Melcher K (2015) Structural basis for recognition of diverse transcriptional repressors by the TOPLESS family of corepressors. Sci Adv 1(6):e1500107. https://doi.org/10.1126/sciadv.1500107
Klein J, Saedler H, Huijser P (1996) A new family of DNA binding proteins includes putative transcriptional regulators of the Antirrhinum majus floral meristem identity gene SQUAMOSA. Mol Gen Genet 250(1):7–16. https://doi.org/10.1007/BF02191820
Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA (2009) Circos: an information aesthetic for comparative genomics. Genome Res 19(9):1639–1645. https://doi.org/10.1101/gr.092759.109
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35(6):1547–1549. https://doi.org/10.1093/molbev/msy096
Lamesch P, Berardini TZ, Li D, Swarbreck D, Wilks C, Sasidharan R, Muller R, Dreher K, Alexander DL, Garcia-Hernandez M, Karthikeyan AS, Lee CH, Nelson WD, Ploetz L, Singh S, Wensel A, Huala E (2012) The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools. Nucleic Acids Res 40:D1202–D1210. https://doi.org/10.1093/nar/gkr1090
Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouzé P, Rombauts S (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30(1):325–327. https://doi.org/10.1093/nar/30.1.325
Letunic I, Bork P (2021) Interactive tree of life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res 49(W1):W293–W296. https://doi.org/10.1093/nar/gkab301
Li J, Hou H, Li X, Xiang J, Yin X, Gao H, Zheng Y, Bassett CL, Wang X (2013) Genome-wide identification and analysis of the SBP-box family genes in apple (Malus x domestica Borkh.). Plant Physiol Biochem 70:100–114. https://doi.org/10.1016/j.plaphy.2013.05.021
Li XQ, Xing T, Du D (2016) Identification of top-ranked proteins within a directional protein interaction network using the pageRank algorithm: applications in humans and plants. Curr Issues Mol Biol 20:13–28. https://doi.org/10.21775/cimb.020.013
Li XY, Lin EP, Huang HH, Niu MY, Tong ZK, Zhang JH (2018) Molecular characterization of squamosa promoter binding protein-like (SPL) gene family in Betula luminifera. Front Plant Sci 9:608. https://doi.org/10.3389/fpls.2018.00608
Li J, Gao X, Zhang X, Liu C (2020a) Dynamic expansion and functional evolutionary profiles of plant conservative gene family SBP-Box in twenty-two flowering plants and the origin of miR156. Biomolecules 10(5):757. https://doi.org/10.3390/biom10050757
Li Y, Song Q, Zhang Y, Li Z, Guo J, Chen X, Zhang G (2020b) Genome-wide identification, characterization, and expression patterns analysis of the SBP-box gene family in wheat (Triticum aestivum L.). Sci Rep 10(1):17250. https://doi.org/10.1038/s41598-020-74417-x
Li S, Wang X, Xu W, Liu T, Cai C, Chen L, Clark CB, Ma J (2021) Unidirectional movement of small RNAs from shoots to roots in interspecific heterografts. Nat Plants 7(1):50–59. https://doi.org/10.1038/s41477-020-00829-2
Liu K, Cao J, Yu K, Liu X, Gao Y, Chen Q, Zhang W, Peng H, Du J, Xin M, Hu Z, Guo W, Rossi V, Ni Z, Sun Q, Yao Y (2019) Wheat TaSPL8 modulates leaf angle through auxin and brassinosteroid signaling. Plant Physiol 181(1):179–194. https://doi.org/10.1104/pp.19.00248
Liu C, Zhang Q, Dong J, Cai C, Zhu H, Li S (2022) Genome-wide identification and characterization of mungbean CIRCADIAN CLOCK ASSOCIATED 1 like genes reveals an important role of VrCCA1L26 in flowering time regulation. BMC Genomics 23(1):374. https://doi.org/10.1186/s12864-022-08620-7
Lu S, Yang C, Chiang VL (2011) Conservation and diversity of microRNA-associated copper-regulatory networks in Populus trichocarpa. J Integr Plant Biol 53(11):879–891. https://doi.org/10.1111/j.1744-7909.2011.01080.x
Mistry J, Chuguransky S, Williams L, Qureshi M, Salazar GA, Sonnhammer E, Tosatto S, Paladin L, Raj S, Richardson LJ, Finn RD, Bateman A (2021) Pfam: the protein families database in 2021. Nucleic Acids Res 49(D1):D412–D419. https://doi.org/10.1093/nar/gkaa913
Piriyapongsa J, Jordan IK (2008) Dual coding of siRNAs and miRNAs by plant transposable elements. RNA 14(5):814–821. https://doi.org/10.1261/rna.916708
Potter SC, Luciani A, Eddy SR, Park Y, Lopez R, Finn RD (2018) HMMER web server: 2018 update. Nucleic Acids Res 46(W1):W200–W204. https://doi.org/10.1093/nar/gky448
Price MN, Dehal PS, Arkin AP (2009) FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol 26(7):1641–1650. https://doi.org/10.1093/molbev/msp077
Ren L, Tang D, Zhao T, Zhang F, Liu C, Xue Z, Shi W, Du G, Shen Y, Li Y, Cheng Z (2018) OsSPL regulates meiotic fate acquisition in rice. New Phytol 218(2):789–803. https://doi.org/10.1111/nph.15017
Rogers K, Chen X (2013) Biogenesis, turnover, and mode of action of plant microRNAs. Plant Cell 25(7):2383–2399. https://doi.org/10.1105/tpc.113.113159
Schmutz J, McClean PE, Mamidi S, Wu GA, Cannon SB, Grimwood J, Jenkins J, Shu S, Song Q, Chavarro C, Torres-Torres M, Geffroy V, Moghaddam SM, Gao D, Abernathy B, Barry K, Blair M, Brick MA, Chovatia M, Gepts P, Goodstein DM, Gonzales M, Hellsten U, Hyten DL, Jia G, Kelly JD, Kudrna D, Lee R, Richard MM, Miklas PN, Osorno JM, Rodrigues J, Thareau V, Urrea CA, Wang M, Yu Y, Zhang M, Wing RA, Cregan PB, Rokhsar DS, Jackson SA (2014) A reference genome for common bean and genome-wide analysis of dual domestications. Nat Genet 46(7):707–713. https://doi.org/10.1038/ng.3008
Shen HB, Chou KC (2006) Ensemble classifier for protein fold pattern recognition. Bioinformatics 22(14):1717–1722. https://doi.org/10.1093/bioinformatics/btl170
Shi R, Xu W, Liu T, Cai C, Li S (2021) VrLELP controls flowering time under short-day conditions in Arabidopsis. J Plant Res 134(1):141–149. https://doi.org/10.1007/s10265-020-01235-7
Si L, Chen J, Huang X, Gong H, Luo J, Hou Q, Zhou T, Lu T, Zhu J, Shangguan Y, Chen E, Gong C, Zhao Q, Jing Y, Zhao Y, Li Y, Cui L, Fan D, Lu Y, Weng Q, Wang Y, Zhan Q, Liu K, Wei X, An K, An G, Han B (2016) OsSPL13 controls grain size in cultivated rice. Nat Genet 48(4):447–456. https://doi.org/10.1038/ng.3518
Sujay P, Amita P (2017) Genome-wide characterization of MicroRNAs from mungbean (Vigna radiata L.). Biotechnol J Int. https://doi.org/10.9734/BJI/2017/30984
Szklarczyk D, Gable AL, Nastou KC, Lyon D, Kirsch R, Pyysalo S, Doncheva NT, Legeay M, Fang T, Bork P, Jensen LJ, von Mering C (2021) The STRING database in 2021: customizable protein-protein networks, and functional characterization of user-uploaded gene/measurement sets. Nucleic Acids Res 49(D1):D605–D612. https://doi.org/10.1093/nar/gkaa1074
Varshney RK, Saxena RK, Upadhyaya HD, Khan AW, Yu Y, Kim C, Rathore A, Kim D, Kim J, An S, Kumar V, Anuradha G, Yamini KN, Zhang W, Muniswamy S, Kim JS, Penmetsa RV, von Wettberg E, Datta SK (2017) Whole-genome resequencing of 292 pigeonpea accessions identifies genomic regions associated with domestication and agronomic traits. Nat Genet 49(7):1082–1088. https://doi.org/10.1038/ng.3872
Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93(1):77–78. https://doi.org/10.1093/jhered/93.1.77
Wang S, Wu K, Yuan Q, Liu X, Liu Z, Lin X, Zeng R, Zhu H, Dong G, Qian Q, Zhang G, Fu X (2012) Control of grain size, shape and quality by OsSPL16 in rice. Nat Genet 44(8):950–954. https://doi.org/10.1038/ng.2327
Wang Y, Wang Z, Amyot L, Tian L, Xu Z, Gruber MY, Hannoufa A (2015) Ectopic expression of miR156 represses nodulation and causes morphological and developmental changes in Lotus japonicus. Mol Genet Genomics 290(2):471–484. https://doi.org/10.1007/s00438-014-0931-4
Wang H, Lu Z, Xu Y, Kong L, Shi J, Liu Y, Fu C, Wang X, Wang ZY, Zhou C, Han L (2019) Genome-wide characterization of SPL family in Medicago truncatula reveals the novel roles of miR156/SPL module in spiky pod development. BMC Genomics 20(1):552. https://doi.org/10.1186/s12864-019-5937-1
Wiese A, Elzinga N, Wobbes B, Smeekens S (2004) A conserved upstream open reading frame mediates sucrose-induced repression of translation. Plant Cell 16(7):1717–1729. https://doi.org/10.1105/tpc.019349
Xie K, Wu C, Xiong L (2006) Genomic organization, differential expression, and interaction of SQUAMOSA promoter-binding-like transcription factors and microRNA156 in rice. Plant Physiol 142(1):280–293. https://doi.org/10.1104/pp.106.084475
Yamaguchi N, Winter CM, Wu MF, Kanno Y, Yamaguchi A, Seo M, Wagner D (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
Yamaguchi-Shinozaki K, Shinozaki K (2005) Organization of cis-acting regulatory elements in osmotic- and cold-stress-responsive promoters. Trends Plant Sci 10(2):88–94. https://doi.org/10.1016/j.tplants.2004.12.012
Yang Y, Wang S, Huang L, Ma H, Shu Y, He X, Ma H (2014) Characterization and subcellular localization of two SBP genes and their response to abiotic stress in soybean (Glycine max (L.) Merr.). Sheng Wu Gong Cheng Xue Bao 30(11):1709–1719
Yang K, Tian Z, Chen C, Luo L, Zhao B, Wang Z, Yu L, Li Y, Sun Y, Li W, Chen Y, Li Y, Zhang Y, Ai D, Zhao J, Shang C, Ma Y, Wu B, Wang M, Gao L, Sun D, Zhang P, Guo F, Wang W, Li Y, Wang J, Varshney RK, Wang J, Ling HQ, Wan P (2015) Genome sequencing of adzuki bean (Vigna angularis) provides insight into high starch and low fat accumulation and domestication. Proc Natl Acad Sci U S A 112(43):13213–13218. https://doi.org/10.1073/pnas.1420949112
Yun J, Sun Z, Jiang Q, Wang Y, Wang C, Luo Y, Zhang F, Li X (2021) The miR156b-GmSPL9d module modulates nodulation by targeting multiple core nodulation genes in soybean. New Phytol 233(4):1881–1899. https://doi.org/10.1111/nph.17899
Zhang Y, Schwarz S, Saedler H, Huijser P (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
Zhang SD, Ling LZ, Yi TS (2015) Evolution and divergence of SBP-box genes in land plants. BMC Genomics 16:787. https://doi.org/10.1186/s12864-015-1998-y
Zhang Q, Liang Z, Cui X, Ji C, Li Y, Zhang P, Liu J, Riaz A, Yao P, Liu M, Wang Y, Lu T, Yu H, Yang D, Zheng H, Gu X (2018) N(6)-methyladenine DNA methylation in Japonica and Indica rice genomes and its association with gene expression, plant development, and stress responses. Mol Plant 11(12):1492–1508. https://doi.org/10.1016/j.molp.2018.11.005
Zhou XB, Chen C, Li ZC, Zou XY (2007) Using Chou’s amphiphilic pseudo-amino acid composition and support vector machine for prediction of enzyme subfamily classes. J Theor Biol 248(3):546–551. https://doi.org/10.1016/j.jtbi.2007.06.001
Acknowledgements
This research was supported by the Program for Scientific Research Innovation Team of Young Scholar in Colleges and Universities of Shandong Province, China (2021KJ029), Science & Technology Specific Projects in Agricultural High-tech Industrial Demonstration Area of the Yellow River Delta (2022SZX36).
Funding
All data supporting the findings of this study are available within the paper and within its supplementary materials.
Author information
Authors and Affiliations
Contributions
XX and HZ (Hong Zhu) designed the research; HZ (Huiying Zhang), XG, ZW, ZY, KN, and MH performed the experiments and analyzed the data; HZ (Hong Zhu), HZ (Huiying Zhang) and XG wrote the manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Zhang, H., Guo, X., Wang, Z. et al. Identification and expression analysis of SQUAMOSA promoter-binding protein (SBP) genes in mungbean. Plant Biotechnol Rep 17, 401–413 (2023). https://doi.org/10.1007/s11816-023-00833-w
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11816-023-00833-w