Abstract
SQUAMOSA promoter-binding protein (SBP)-box genes regulate plant-specific transcription factors that play vital roles in diverse biological processes. In this study, we identified 48 SBP-box genes from Juglans regia (JrSBPs) based on the transcriptome dataset. Nineteen of these JrSBPs were predicted to be putative target genes of jre-miR156/157. Phylogenetic tree based on the conserved SBP domains divided the JrSBPs into nine groups, analogous to those from Arabidopsis. JrSBP members within the same group shared similar motifs. Cis-elements analysis implied that JrSBP genes were regulated by light, phytohormones, and stresses. Functions of JrSBP genes were predicted and analyzed by comparing the proteins of JrSBPs and SPLs from Arabidopsis. Expression profile of JrSBPs was analyzed based on RNA-seq and RT-qPCR. The results should provide fundamental information for understanding the roles of JrSBPs during floral induction.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abdullah M, Cao Y, Cheng X, Shakoor A, Su X, Gao J, Cai Y (2018) Genome-wide analysis characterization and evolution of SBP genes in Fragaria vesca, Pyrusbretschneideri, Prunus persica and Prunus mume. Front Plant Sci 9:64. https://doi.org/10.3389/fgene.2018.00064
Al-Khayri JM, Jain SM, Johnson DV (2015) Advances in plant breeding strategies: breeding. Tools, Biotechnology and Molecular
Aoki K, Ogata Y, Shibata D (2007) Approaches for Extracting Practical Information from Gene Co-expression Networks in Plant Biology. Plant Cell Physiol 48:381–390. https://doi.org/10.1093/pcp/pcm013
Aukerman MJ, Sakai H (2003) Regulation of flowering time and floral organ identity by a MicroRNA and its APETALA2-like target genes. Plant Cell 15:2730–2741. https://doi.org/10.1105/tpc.016238
Barker D, Pagel M (2005) Predicting functional gene links from phylogenetic-statistical analyses of whole genomes. PLoS Comput Biol 1:e3e. https://doi.org/10.1371/journal.pcbi.0010003
Birkenbihl RP, Jach G, Saedler H, Huijser P (2005) Functional dissection of the plant-specific SBP-domain: overlap of the DNA-binding and nuclear localization domains. J Mol Biol 352:585–596. https://doi.org/10.1016/j.jmb.2005.07.013
Borner R, Kampmann G, Chandler J (2000) A MADS domain gene involved in the transition to flowering in Arabidopsis. Plant J 24:591–599. https://doi.org/10.1046/j.1365-313x.2000.00906.x
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(12):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 237:91. https://doi.org/10.1016/s0378-1119(99)00308-x
Chao L-M, Liu Y-Q, Chen D-Y, Xue X-Y, Mao Y-B, Chen X-Y (2017) Arabidopsis transcription factors SPL1 and SPL12 confer plant thermotolerance at reproductive stage. Mol Plant 10:735–748. https://doi.org/10.1016/j.molp.2017.03.010
Chen G et al (2019) Roles of the GA-mediated SPL gene family and miR156 in the floral development of Chinese chestnut (Castanea mollissima). Int J Mol Sci:20. https://doi.org/10.3390/ijms20071577
Cheng H, Hao M, Wang W, Mei D, Tong C, Wang H, Liu J, Fu L, Hu Q (2016) Genomic identification, characterization and differential expression analysis of SBP-box gene family in Brassica napus. BMC Plant Biol 16:16–17. https://doi.org/10.1186/s12870-016-0852-y
Hassankhah A, Rahemi M, Mozafari MR, Vahdati K (2018) Flower development in walnut: altering the flowering pattern by Gibberellic acid application. Notulae Botanicae Horti Agrobotanici Cluj-Napoca 46:700–706. https://doi.org/10.15835/nbha46211183
Hassankhah A, Vahdati K, Rahemi M, Hassani D, Khorami SS (2019) Persian walnut phenology: effect of chilling and heat requirements on budbreak and flowering date. Int J Horticult Sci Technol. https://doi.org/10.22059/ijhst.2018.260944.249
Hou H, Li J, Gao M, Singer SD, Wang H, Mao L, Fei Z, Wang X (2013) Genomic organization, Phylogenetic Comparison and Differential Expression of the SBP-Box Family Genes in Grape. PLoS One 8(3). https://doi.org/10.1371/journal.pone.0059358
Hou H, Yan X, Sha T, Yan Q, Wang X (2017) The SBP-box gene VpSBP11 from Chinese wild Vitis is involved in floral transition and affects leaf development. Int J Mol Sci 18(7):1493. https://doi.org/10.3390/ijms18071493
Kim JJ, Lee JH, Kim W, Jung HS, Huijser P, Ahn JH (2012) The microRNA156-SQUAMOSA promoter binding protein-like 3 module regulates ambient temperature-responsive flowering via flowering locus T in Arabidopsis. Plant Physiol 159:461–478. https://doi.org/10.1104/pp.111.192369
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 250:7–16
Lännenpää M, Jänönen I, Hölttä-Vuori M, Gardemeister M, Porali I, Sopanen T (2010) A new SBP-box gene BpSPL1 in silver birch (Betula pendula). Physiol Plant 120:491–500
Li J et al (2013) Genome-wide identification and analysis of the SBP-box family genes in apple (Malus × domestica Borkh.). Plant Physiol Biochem 70:100–114. https://doi.org/10.1016/j.plaphy.2013.05.021
Li X-Y, Lin E-P, Huang H-H, Niu M-Y, Tong Z-K, Zhang J-H (2018) Molecular Characterization of SQUAMOSA promoter binding protein-like (SPL) gene family in Betula luminifera. Front Plant Sci:9. https://doi.org/10.3389/fpls.2018.00608
Liang YT (1981) Study on early fruiting characteristics of superior varieties of walnut in Xinjiang. Journal of Shandong Agricultural College 2:35–44
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
Mandel MA, Yanofsky MF (1995) The Arabidopsis AGL8 MADS box gene is expressed in inflorescence meristems and is negatively regulated by APETALA1. Plant Cell 7:1763–1771. https://doi.org/10.2307/3870185
Mandel MA, Gustafson-Brown C, Savidge B, Yanofsky MF (1992) Molecular characterization of the Arabidopsis floral homeotic gene APETALA1. Nature 360:273–277. https://doi.org/10.1038/360273a0
Marchler-Bauer A et al (2015) CDD: NCBI's conserved domain database. Nucleic Acids Res 43:D222–D226. https://doi.org/10.1093/nar/gku1221
Martínez-García PJ et al (2016) The walnut ( Juglans regia ) genome sequence reveals diversity in genes coding for the biosynthesis of non-structural polyphenols. Plant J 87:507–532. https://doi.org/10.1111/tpj.13207/full
Preston JC, Hileman LC (2010) SQUAMOSA-promoter binding protein 1 initiates flowering in Antirrhinum majus through the activation of meristem identity genes. Plant J 62:704–712. https://doi.org/10.1111/j.1365-313X.2010.04184.x
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
Salinas M, Xing S, Hohmann S, Berndtgen R, Huijser P (2012) Genomic organization, phylogenetic comparison and differential expression of the SBP-box family of transcription factors in tomato. Planta 235:1171–1184. https://doi.org/10.1007/s00425-011-1565-y
Schultz EA, Haughn GW (1991) LEAFY, a homeotic gene that regulates inflorescence development in Arabidopsis. Plant Cell 3:771–781
Schwarz S, Grande AV, Bujdoso N, Saedler H, Huijser P (2008) The microRNA regulated SBP-box genes SPL9 and SPL15 control shoot maturation in Arabidopsis. Plant Mol Biol 67:183–195. https://doi.org/10.1007/s11103-008-9310-z
Shikata M, Koyama T, Mitsuda N, Ohme-Takagi M (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
Si L et al (2016) OsSPL13 controls grain size in cultivated rice. Nat Genet 48:447. https://doi.org/10.1038/ng.3518
Song A et al (2016) Transcriptome-wide identification and expression analysis of chrysanthemum SBP-like transcription factors. Plant Physiol Biochem 102:10–16. https://doi.org/10.1016/j.plaphy.2016.02.009
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 18:1734. https://doi.org/10.3390/ijms18081734
Stone JM, Liang XY, Nekl ER, Stiers JJ (2010) Arabidopsis AtSPL14, a plant-specific SBP-domain transcription factor, participates in plant development and sensitivity to fumonisin B1. Plant J 41:744–754. https://doi.org/10.1111/j.1365-313X.2005.02334.x
Trapnell C et al (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28:511–515. https://doi.org/10.1038/nbt.1621
Trepathi RK, Goel R, Kumari S, Dahuja A (2017) Genomic organization, phylogenetic comparison, and expression profiles of the SPL family genes and their regulation in soybean. Dev Genes Evol 227:1–19. https://doi.org/10.1007/s00427-017-0574-7
Unte US, Sorensen A-M, Pesaresi P, Gandikota M, Leister D, Saedler H (2003) SPL8, an SBP-box gene that affects pollen sac development in Arabidopsis. Plant Cell 15:1009–1019. https://doi.org/10.1105/tpc.010678
Usami T, Horiguchi G, Yano S, Tsukaya H (2009) The more and smaller cells mutants of Arabidopsis thaliana identify novel roles for SQUAMOSA promoter binding protein-like genes in the control of heteroblasty. Development 136:955–964. https://doi.org/10.1242/dev.028613
Wang JW, Czech B, Weigel D (2009) miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 138:738–749. https://doi.org/10.1016/j.cell.2009.06.014
Wang S et al (2012) Control of grain size, shape and quality by OsSPL16 in rice. Nat Genet 44:950–954. https://doi.org/10.1038/ng.2327
Wang P, Chen D, Zheng Y, Jin S, Yang J, Ye N (2018) Identification and expression analyses of SBP-box genes reveal their involvement in abiotic stressand hormone response in tea plant (Camellia sinensis). Int J Mol Sci:19. https://doi.org/10.3390/ijms19113404
Wu G, Poethig RS (2006) Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3. Development 133:3539–3547. https://doi.org/10.1242/dev.02521
Wu D, Luo J, Chen J, Zhang L, Lim KJ, Wang Z (2019) Selection pressure causes differentiation of the SPL gene family in the Juglandaceae. Mol Gen Genomics 294:1037–1048. https://doi.org/10.1007/s00438-019-01562-y
Xia X, Xi R (1989) The periods of physiological and morphological differentiation of pistillate flower buds in walnut (Juglans regia L.) journal of Hebei agricultural university (1), 18-21
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 142:280–293. https://doi.org/10.1104/pp.106.084475
Xie LH et al (2019) Genome-wide analysis and expression profiling of the heat shock factor gene family in Phyllostachys edulis during development and in response to abiotic stresses. Forests 10:100. https://doi.org/10.3390/f10020100
Xing S, Salinas M, Höhmann S, Berndtgen R, Huijser P (2010) miR156-targeted and nontargeted SBP-box transcription factors act in concert to secure male fertility in Arabidopsis. Plant Cell 22:3935–3950. https://doi.org/10.1105/tpc.110.079343
Xing S, Salinas M, Garcia-Molina A, Höhmann S, Berndtgen R, Huijser P (2013) SPL8 and miR156-targeted SPL genes redundantly regulate Arabidopsis gynoecium differential patterning. Plant J 75:566–577. https://doi.org/10.1111/tpj.12221
Xu Z, Sun L, Zhou Y, Yang W, Cheng T, Wang J, Zhang Q (2015) Identification and expression analysis of the SQUAMOSA promoter-binding protein (SBP)-box gene family in Prunus mume. Mol Gen Genomics 290(5):1701–1715. https://doi.org/10.1007/s00438-015-1029-3
Yamasaki H, Haysshi M, Fukazawa M, Kobayashi Y, Shikanai T (2009) SQUAMOSA promoter binding protein-Like7 is a central regulator for copper homeostasis in Arabidopsis. Plant Cell 21:347–361
Yang WH (1984) Walnut of China. Journal of Hebei Agricultural University 7(2):1–9
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):0–11 doi:https://doi.org/10.1016/j.gene.2007.02.034, 1
Yuan H et al (2019) OsSPL18 controls grain weight and grain number in rice. J Genet Genomics 46:41–51. https://doi.org/10.1016/j.jgg.2019.01.003
Zeng RF, Zhou JJ, Liu SR, Gan ZM, Zhang JZ, Hu CG (2019) Genome-Wide Identification and Characterization of SQUAMOSA-Promoter-Binding Protein (SBP) Genes Involved in the Flowering Development of Citrus Clementina. Biomolecules:9. https://doi.org/10.3390/biom9020066
Zhang SX, Yu SP (1987) Observation on flowering and fruiting characteristics of early fruiting walnut in. Xinjiang Economic Forest Researchs 5(1):73–75
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 63:429. https://doi.org/10.1007/s11103-006-9099-6
Zhou L, Niu J, Quan S (2018a) Identification of appropriate reference genes for RT-qPCR analysis in Juglans regia L. PLoS One:13. https://doi.org/10.1371/journal.pone.0209424
Zhou Q et al (2018b) Genome-wide identification and characterization of the SBP-box gene family in Petunia. BMC Genomics 19(1):–193. https://doi.org/10.1186/s12864-018-4537-9
Zhu Z, Tan L, Fu Y, Liu F, Cai H, Xie D, Wu F, Wu J, Matsumoto T, Sun C (2013) Genetic control of inflorescence architecture during rice domestication. Nat Commun 4:2200. https://doi.org/10.1038/ncomms3200
Funding
The study was supported by the National Science and Technology Specific Projects of Xinjiang (No. 201130102-1-4) and the National Natural Science Foundation of China (No.30560090). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Data archiving statement
Supplementary data associated with this article can be found in the online version, Supplementary Material Table 1: The primers used in this study by RT-qPCR; Supplementary Material Table 2: The protein sequences of SBP domains of 48 JrSBP genes.
Additional information
Communicated by M. Troggio
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Zhou, L., Quan, S., Ma, L. et al. Molecular characterization of SBP-box gene family during floral induction in walnut (Juglans regia L.). Tree Genetics & Genomes 16, 12 (2020). https://doi.org/10.1007/s11295-019-1402-1
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11295-019-1402-1