Skip to main content
SpringerLink
Log in

Genomic organization, phylogenetic comparison and differential expression of the SBP-box family of transcription factors in tomato

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

SBP-box genes represent transcription factors ubiquitously found in the plant kingdom and recognized as important regulators of many different aspects of plant development. In this study, 15 SBP-box gene family members were identified in tomato and analyzed with respect to their genomic organization and other structural features. Phylogenetic reconstruction based on the DNA-binding SBP-domain, allowed the classification of the SlySBP proteins into eight groups representing clear orthologous relationships to family members of other flowering plants and the moss Physcomitrella. In order to have a better understanding of their possible function in the development of a fleshy-fruit species like tomato, the mRNA expression levels of all SlySBP genes were quantified in vegetative and reproductive organs of plants, at different stages of growth. As transcripts of ten SlySBP genes were found to carry putative miR156- and miR157-response elements, the expression levels of the corresponding microRNAs were determined as well, revealing different patterns of expression. In addition, eight putative miR156 and four miR157 encoding loci could be identified in the tomato genome, four of them forming a polycistronic cluster. Whereas miR156 and miR157 levels were highest in seedlings, leaves and anthers of young flowers, most miR156-targeted SlySBP genes were found to be expressed in young inflorescences and during fruit development and ripening, suggesting a particularly important role during tomato reproductive growth. The data presented provide a basis for future clarification of the various functions that SBP-box gene family members play in tomato growth and development.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

aa:

Amino acid(s)

cDNA:

DNA complementary to RNA

EST:

Expressed sequence tag

miRNA:

MicroRNA

MRE:

MicroRNA responsive element

Myr:

Million years

SBP:

SQUAMOSA promoter binding protein

SPL:

SQUAMOSA promoter binding protein-like

UTR:

Untranslated region

References

  • Arazi T, Talmor-Neiman M, Stav R, Riese M, Huijser P, Baulcombe DC (2005) Cloning and characterization of micro-RNAs from moss. Plant J 43:837–848

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Blanc G, Wolfe K (2004) Widespread paleopolyploidy in model plant species inferred from age distributions of duplicate genes. Plant Cell 16:1667–1678

    Article  PubMed  CAS  Google Scholar 

  • Bombarely A, Menda N, Tecle IY, Buels RM, Strickler S, Fischer-York T, Pujar A, Leto J, Gosselin J, Mueller LA (2011) The Sol Genomics Network (solgenomics.net): growing tomatoes using Perl. Nucleic Acids Res 39:D1149–D1155

    Article  PubMed  Google Scholar 

  • Brukhin V, Hernould M, Gonzalez N, Chevalier C, Mouras A (2003) Flower development schedule in tomato Lycopersicon esculentum cv. sweet cherry. Sex Plant Reprod 15:311–320

    Google Scholar 

  • 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 12:367–377

    Article  PubMed  CAS  Google Scholar 

  • Cardon G, Höhmann S, Klein J, Nettesheim K, Saedler H, Huijser P (1999) Molecular characterisation of the Arabidopsis SBP-box genes. Gene 237:91–104

    Article  PubMed  CAS  Google Scholar 

  • Chaw SM, Chang CC, Chen HL, Li WH (2004) Dating the monocot-dicot divergence and the origin of core eudicots using whole chloroplast genomes. J Mol Evol 58:424–441

    Article  PubMed  CAS  Google Scholar 

  • Chuck G, Whipple C, Jackson D, Hake S (2010) The maize SBP-box transcription factor encoded by tasselsheath4 regulates bract development and the establishment of meristem boundaries. Development 137:1243–1250

    Article  PubMed  CAS  Google Scholar 

  • De Martino G, Pan I, Emmanuel E, Levy A, Irish VF (2006) Functional analyses of two tomato APETALA3 genes demonstrate diversification in their roles in regulating floral development. Plant Cell 18:1833–1845

    Article  PubMed  Google Scholar 

  • Eriksson EM, Bovy A, Manning K, Harrison L, Andrews J, De Silva J, Tucker GA, Seymour GB (2004) Effect of the colorless non-ripening mutation on cell wall biochemistry and gene expression during tomato fruit development and ripening. Plant Physiol 136:4184–4197

    Article  PubMed  CAS  Google Scholar 

  • Exposito-Rodriguez M, Borges AA, Borges-Perez A, Perez JA (2008) Selection of internal control genes for quantitative real-time RT-PCR studies during tomato development process. BMC Plant Biol 8:131. doi:10.1186/1471-2229-8-131

    Article  PubMed  Google Scholar 

  • Fernandez AI, Viron N, Alhagdow M, Karimi M, Jones M, Amsellem Z, Sicard A, Czerednik A, Angenent G, Grierson D, May S, Seymour G, Eshed Y, Lemaire-Chamley M, Rothan C, Hilson P (2009) Flexible tools for gene expression and silencing in tomato. Plant Physiol 151:1729–1740

    Article  PubMed  CAS  Google Scholar 

  • Frazier TP, Xie FL, Freistaedter A, Burklew CE, Zhang BH (2010) Identification and characterization of microRNAs and their target genes in tobacco (Nicotiana tabacum). Planta 232:1289–1308

    Article  PubMed  CAS  Google Scholar 

  • Fridman E, Zamir D (2003) Functional divergence of a syntenic invertase gene family in tomato, potato, and Arabidopsis. Plant Physiol 131:603–609

    Article  PubMed  CAS  Google Scholar 

  • Gandikota M, Birkenbihl RP, Höhmann S, Cardon GH, Saedler H, Huijser P (2007) The miRNA156/157 recognition element in the 3′ UTR of the Arabidopsis SBP box gene SPL3 prevents early flowering by translational inhibition in seedlings. Plant J 49:683–693

    Article  PubMed  CAS  Google Scholar 

  • Gilchrist DG (1998) Programmed cell death in plant disease: the purpose and promise of cellular suicide. Annu Rev Phytopathol 36:393–414

    Article  PubMed  CAS  Google Scholar 

  • Gou JY, Felippes FF, Liu CJ, Weigel D, Wang J (2011) Negative regulation of anthocyanin biosynthesis in Arabidopsis by a miR156-targeted SPL transcription factor. Plant Cell 23:1512–1522

    Article  PubMed  CAS  Google Scholar 

  • Griffiths-Jones S (2004) The microRNA registry. Nucleic Acids Res 32:D109–D111

    Article  PubMed  CAS  Google Scholar 

  • Huijser P, Schmid M (2011) The control of developmental phase transitions in plants. Development 138:4117–4129

    Article  PubMed  CAS  Google Scholar 

  • Hultquist JF, Dorweiler JE (2008) Feminized tassels of maize mop1 and ts1 mutants exhibit altered levels of miR156 and specific SBP-box genes. Planta 229:99–113

    Article  PubMed  CAS  Google Scholar 

  • Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23:254–267

    Article  PubMed  CAS  Google Scholar 

  • Jaakola L, Mervin Poole M, Jones MO, Kämäräinen-Karppinen T, Janne J, Koskimäki JJ, Hohtola A, Häggman H, Fraser PD, Manning K, King GJ, Thomson H, Graham B, Seymour GB (2010) A SQUAMOSA MADS box gene involved in the regulation of anthocyanin accumulation in bilberry fruits. Plant Physiol 153:1619–1629

    Article  PubMed  CAS  Google Scholar 

  • Jones-Rhoades MW, Bartel DP (2004) Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol Cell 14:787–799

    Article  PubMed  CAS  Google Scholar 

  • Karlova R, Rosin FM, Busscher-Lange J, Parapunovaa V, Doc PT, Ferniec AR, Fraserd PD, Baxtere C, Angenent GC, de Maagd RA (2011) Transcriptome and metabolite profiling show that APETALA2a is a major regulator of tomato fruit ripening. Plant Cell 23:923–941

    Article  PubMed  CAS  Google Scholar 

  • Kinet JM, Peet MM (1997) Tomato. In: Wien HC (ed) The physiology of vegetable crops. CAB International, Wallingford, pp 207–258

    Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Kropat J, Tottey S, Birkenbihl RP, Depege N, Huijser P, Merchant S (2005) A regulator of nutritional copper signaling in Chlamydomonas is an SBP domain protein that recognizes the GTAC core of copper response element. Proc Natl Acad Sci USA 102:18730–18735

    Article  PubMed  CAS  Google Scholar 

  • Ku H-M, Vision T, Liu J, Tanksley SD (2000) Comparing sequenced segments of the tomato and Arabidopsis genomes: Large-scale duplication followed by selective gene loss creates a network of synteny. Proc Natl Acad Sci USA 97:9121–9126

    Article  PubMed  CAS  Google Scholar 

  • Lifschitz E, Eviatar T, Rozman A, Shalit A, Goldshmidt A, Amsellem Z, Alvarez JP, Eshed Y (2006) The tomato FT ortholog triggers systemic signals that regulate growth and flowering and substitute for diverse environmental stimuli. Proc Natl Acad Sci USA 103:6398–6403

    Article  PubMed  CAS  Google Scholar 

  • Lozano R, Gimenez E, Cara B, Capel J, Angosto T (2009) Genetic analysis of reproductive development in tomato. Int J Dev Biol 53:1635–1648

    Article  PubMed  CAS  Google Scholar 

  • Luan FL, Han YS, Zhu HL, Shao Y, Chen AJ, Tian HQ, Luo YB, Zhu BZ (2010) Computational predicting novel microRNAs in tomato and validating with RT-PCR. Russ J Plant Physiol 57:469–479

    Article  CAS  Google Scholar 

  • Manning K, Tor M, Poole M, Hong Y, Thompson AJ, King GJ, Giovannoni JJ, Seymour GB (2006) A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening. Nat Genet 38:948–952

    Article  PubMed  CAS  Google Scholar 

  • Martin RC, Asahina M, Liu P–P, Kristof JR, Coppersmith JL, Pluskota WE, Bassel GW, Goloviznina NA, Nguyen TT, Martínez-Andújar C, Arun Kumar MB, Pupel P, Nonogaki H (2010) The regulation of post-germinative transition from the cotyledon- to vegetative-leaf stages by microRNA-targeted SQUAMOSA PROMOTER-BINDING PROTEIN LIKE13 in Arabidopsis. Seed Sci Res 20:89–96

    Article  CAS  Google Scholar 

  • Miura K, Ikeda M, Matsubara A, Song XJ, Ito M, Asano K, Matsuoka M, Kitano H, Ashikari M (2010) OsSPL14 promotes panicle branching and higher grain productivity in rice. Nat Genet 42:545–549

    Article  PubMed  CAS  Google Scholar 

  • Moreno MA, Harper LC, Krueger RW, Dellaporta SL, Freeling M (1997) liguleless1 encodes a nuclear-localized protein required for induction of ligules and auricles during maize leaf organogenesis. Genes Dev 11:616–628

    Article  PubMed  CAS  Google Scholar 

  • Moxon S, Jing R, Szittya G, Schwach F, Rusholme Pilcher R, Moulton V, Dalmay T (2008) Deep sequencing of tomato short RNAs identifies microRNAs targeting genes involved in fruit ripening. Genome Res 18:1602–1609

    Article  PubMed  CAS  Google Scholar 

  • Nickrent DL, Parkinson CL, Palmer JD, Duff RJ (2000) Multigene phylogeny of land plants with special reference to bryophytes and the earliest land plants. Mol Biol Evol 17:1885–1895

    Article  PubMed  CAS  Google Scholar 

  • Nodine MD, Bartel DP (2010) MicroRNAs prevent precocious gene expression and enable pattern formation during plant embryogenesis. Genes Dev 24:2678–2692

    Article  PubMed  CAS  Google Scholar 

  • Pilcher RR, Moxon S, Pakseresht N, Moulton V, Manning K, Seymour G, Dalmay T (2007) Identification of novel small RNAs in tomato (Solanum lycopersicum). Planta 226:709–717

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Riese M, Höhmann S, Saedler H, Münster T, Huijser P (2007) Comparative analysis of the SBP-box gene families in P. patens and seed plants. Gene 401:28–37

    Article  PubMed  CAS  Google Scholar 

  • Shen Y, Zhang ZM, Lin HJ, Liu HL, Chen J, Peng H, Cao MJ, Rong TZ, Pan GT (2010) Cytoplasmic male sterility-regulated novel microRNAs from maize. Funct Integr Genomics 11:179–191

    Article  PubMed  Google Scholar 

  • 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 50:2133–2145

    Article  PubMed  CAS  Google Scholar 

  • Stone JM, Liang X, Nekl ER, Stiers JJ (2005) Arabidopsis AtSPL14, a plant-specific SBP-domain transcription factor, participates in plant development and sensitivity to fumonisin B1. Plant J 41:744–754

    Article  PubMed  CAS  Google Scholar 

  • Thompson AJ, Tor M, Barry CS, Vrebalov J, Orfila C, Jarvis MC, Giovannoni JJ, Grierson D, Seymour GB (1999) Molecular and genetic characterization of a novel pleiotropic tomato-ripening mutant. Plant Physiol 120:383–390

    Article  PubMed  CAS  Google Scholar 

  • Unte US, Sorensen AM, Pesaresi P, Gandikota M, Leister D, Saedler H, Huijser P (2003) SPL8, an SBP-box gene that affects pollen sac development in Arabidopsis. Plant Cell 15:1009–1019

    Article  PubMed  CAS  Google Scholar 

  • Voinnet O (2009) Origin, biogenesis, and activity of plant microRNAs. Cell 136:669–687

    Article  PubMed  CAS  Google Scholar 

  • Wang H, Nussbaum-Wagler T, Li B, Zhao Q, Vigouroux Y, Faller M, Bomblies K, Lukens L, Doebley JF (2005) The origin of the naked grains of maize. Nature 436:714–719

    Article  PubMed  CAS  Google Scholar 

  • Wang JW, Schwab R, Czech B, Mica E, Weigel D (2008) Dual effects of miR156-targeted SPL genes and CYP78A5/KLUH on plastochron length and organ size in Arabidopsis thaliana. Plant Cell 20:1231–1243

    Article  PubMed  CAS  Google Scholar 

  • Wang JW, Czech B, Weigel D (2009) miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 138:738–749

    Article  PubMed  CAS  Google Scholar 

  • Wu G, Poethig RS (2006) Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3. Development 133:3539–3547

    Article  PubMed  CAS  Google Scholar 

  • Wu G, Park MY, Conway SR, Wang JW, Weigel D, Poethig RS (2009) The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell 138:750–759

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Yamaguchi A, Wu MF, Yang L, Wu G, Poethig RS, Wagner D (2009) The microRNA-regulated SBP-Box transcription factor SPL3 is a direct upstream activator of LEAFY, FRUITFULL, and APETALA1. Dev Cell 17:268–278

    Article  PubMed  CAS  Google Scholar 

  • Yamasaki K, Kigawa T, Inoue M, Tateno M, Yamasaki T, Yabuki T, Aoki M, Seki E, Matsuda T, Nunokawa E, Ishizuka Y, Terada T, Shirouzu M, Osanai T, Tanaka A, Seki M, Shinozaki K, Yokoyama S (2004) A novel zinc-binding motif revealed by solution structures of DNA-binding domains of Arabidopsis SBP-family transcription factors. J Mol Biol 337:49–63

    Article  PubMed  CAS  Google Scholar 

  • Yamasaki H, Hayashi 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

    Article  PubMed  CAS  Google Scholar 

  • Yin Z, Li C, Han X, Shen F (2008) Identification of conserved microRNAs and their target genes in tomato (Lycopersicon esculentum). Gene 414:60–66

    Article  PubMed  CAS  Google Scholar 

  • Yu N, Cai WJ, Wang S, Shan CM, Wang LJ, Chen XY (2010) Temporal control of trichome distribution by microRNA156-targeted SPL genes in Arabidopsis thaliana. Plant Cell 22:2322–2335

    Article  PubMed  CAS  Google Scholar 

  • Zhang B, Pan X, Anderson TA (2006) Identification of 188 conserved maize microRNAs and their targets. FEBS Lett 580:3753–3762

    Article  PubMed  CAS  Google Scholar 

  • Zhang Y, Schwarz S, Saedler S, Huijser P (2007) SPL8, a local regulator in a subset of gibberellin-mediated developmental processes in Arabidopsis. Plant Mol Biol 63:429–439

    Article  PubMed  CAS  Google Scholar 

  • Zhang J, Zeng R, Chen J, Liu X, Liao Q (2008) Identification of conserved microRNAs and their targets from Solanum lycopersicum Mill. Gene 423:1–7

    Article  PubMed  CAS  Google Scholar 

  • Zhang X, Zou Z, Zhang J, Zhang Y, Han Q, Hua T, Xu X, Liu H, Li H, Ye Z (2010) Over-expression of sly-miR156a in tomato results in multiple vegetative and reproductive trait alterations and partial phenocopy of the sft mutant. FEBS Lett 585:435–439

    Article  PubMed  Google Scholar 

  • Zuker M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31:3406–3415

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Molecular Plant Genetics, Max Planck Institute for Plant Breeding Research, Carl-von-Linné-Weg 10, 50829, Cologne, Germany

    María Salinas, Shuping Xing, Susanne Höhmann, Rita Berndtgen & Peter Huijser

  2. Departamento de Biología Aplicada, Área de Genética, Universidad de Almería, 04120, Almería, Spain

    María Salinas

Authors
  1. María Salinas
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shuping Xing
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Susanne Höhmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Rita Berndtgen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Peter Huijser
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Peter Huijser.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 1301 kb)

Supplementary material 2 (TXT 209 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-011-1565-y

Keywords

Search

Navigation