Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Genomic organization, differential expression, and functional analysis of the SPL gene family in Gossypium hirsutum

Abstract

SQUAMOSA promoter binding protein-like (SPL) genes encode plant-specific transcription factors that are involved in many fundamental developmental processes. Certain SPL genes contain sequences complementary to miR156, a microRNA (miRNA) that plays a role in modulating plant gene expression. In this study, 30 SPL genes were identified in the reference genome of Gossypium raimondii and 24 GhSPLs were cloned from Gossypium hirsutum. G. raimondii is regarded as the putative contributor of the D-subgenome of G. hirsutum. Comparative analysis demonstrated sequence conservation between GhSPLs and other plant species. GhSPL genes could be classified into seven subclades based on phylogenetic analysis, diverse intron–exon structure, and motif prediction. Within each subclade, genes shared a similar structure. Sequence and experimental analysis predicted that 18 GhSPL genes are putative targets of GhmiR156. Additionally, tissue-specific expression analysis of GhSPL genes showed that their spatiotemporal expression patterns during development progressed differently, with most genes having high transcript levels in leaves, stems, and flowers. Finally, overexpression of GhSPL3 and GhSPL18 in Arabidopsis plants demonstrated that these two genes are involved in the development of leaves and second shoots and play an integral role in promoting flowering. The flowering integrator GhSOC1 may bind to the promoter of GhSPL3 but not GhSPL18 to regulate flowering. In conclusion, our analysis of GhSPL genes will provide some gene resources and a further understanding of GhSPL3 and GhSPL18 function in flowering promotion. Furthermore, the comparative genomics and functional analysis deepened our understanding of GhSPL genes during upland cotton vegetative and reproductive growth.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

References

  1. 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

  2. Bernal M, Casero D, Singh V, Wilson GT, Grande A, Yang HJ, Dodani SC, Pellegrini M, Huijser P, Connolly EL, Merchant SS, Kramer U (2012) Transcriptome sequencing identifies SPL7-regulated copper acquisition genes FRO4/FRO5 and the copper dependence of iron homeostasis in Arabidopsis. Plant Cell 24:738–761

  3. 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 12:367–377

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

  5. 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 (vol 137, pg 1243, 2009). Development 137:1585

  6. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

  7. Dai XB, Zhao PX (2011) psRNATarget: a plant small RNA target analysis server. Nucleic Acids Res 39:W155–W159

  8. Eriksson M, Moseley JL, Tottey S, del Campo JA, Quinn J, Kim Y, Merchant S (2004) Genetic dissection of nutritional copper signaling in chlamydomonas distinguishes regulatory and target genes. Genetics 168:795–807

  9. Fornara F, Coupland G (2009) Plant phase transitions make a SPLash. Cell 138:625–627

  10. Gendrel AV, Lippman Z, Martienssen R, Colot V (2005) Profiling histone modification patterns in plants using genomic tiling microarrays. Nat Methods 2:213–218

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

  12. Hou HM, Li J, Gao M, Singer SD, Wang H, Mao LY, Fei ZJ, Wang XP (2013) Genomic organization, phylogenetic comparison and differential expression of the SBP-Box family genes in grape. PLoS One 8:e59358

  13. Jorgensen SA, Preston JC (2014) Differential SPL gene expression patterns reveal candidate genes underlying flowering time and architectural differences in Mimulus and Arabidopsis. Mol Phylogenet Evol 73:129–139

  14. Jung JH, Seo PJ, Kang SK, Park CM (2011) miR172 signals are incorporated into the miR156 signaling pathway at the SPL3/4/5 genes in Arabidopsis developmental transitions. Plant Mol Biol 76:35–45

  15. 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 69:577–588

  16. Kim JJ, Lee JH, Kim W, Jung HS, Huijser P, Ahn JH (2012) The microRNA156-SQUAMOSA PROMOTER BINDING PROTEIN-LIKE3 module regulates ambient temperature-responsive flowering via FLOWERING LOCUS T in Arabidopsis. Plant Physiol 159:461–478

  17. 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

  18. Lannenpaa M, Janonen I, Holtta-Vuori M, Gardemeister M, Porali I, Sopanen T (2004) A new SBP-box gene BpSPL1 in silver birch (Betula pendula). Physiol Plantarum 120:491–500

  19. Li J, Fan SL, Song MZ, Pang CY, Wei HL, Li W, Ma JH, Wei JH, Jing JG, Yu SX (2013a) Cloning and characterization of a FLO/LFY ortholog in Gossypium hirsutum L. Plant Cell Rep 32:1675–1686

  20. Li J, Hou HM, Li XQ, Xiang J, Yin XJ, Gao H, Zheng Y, Bassett CL, Wang XP (2013b) Genome-wide identification and analysis of the SBP-box family genes in apple (Malus × domestica Borkh.). Plant Physiol Bioch 70:100–114

  21. Li F, Fan G, Wang K, Sun F, Yuan Y, Song G, Li Q, Ma Z, Lu C, Zou C, Chen W, Liang X, Shang H, Liu W, Shi C, Xiao G, Gou C, Ye W, Xu X, Zhang X, Wei H, Li Z, Zhang G, Wang J, Liu K, Kohel RJ, Percy RG, Yu JZ, Zhu YX, Yu S (2014) Genome sequence of the cultivated cotton Gossypium arboreum. Nat Genet 46:567–572

  22. Lin M, Lai DY, Pang CY, Fan SL, Song MZ, Yu SX (2013) Generation and analysis of a large-scale expressed sequence tag database from a full-length enriched cDNA library of developing leaves of Gossypium hirsutum L. PLoS One 8:e76443

  23. Luo L, Li WQ, Miura K, Ashikari M, Kyozuka J (2012) Control of tiller growth of rice by OsSPL14 and Strigolactones, which work in two independent pathways. Plant Cell Physiol 53:1793–1801

  24. 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

  25. Martin RC, Asahina M, Liu PP, Kristof JR, Coppersmith JL, Pluskota WE, Bassel GW, Goloviznina NA, Nguyen TT, Martinez-Andujar C, Kumar MBA, 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

  26. Mei M, Syed NH, Gao W, Thaxton PM, Smith CW, Stelly DM, Chen ZJ (2004) Genetic mapping and QTL analysis of fiber-related traits in cotton (Gossypium). Theor Appl Genet 108:280–291

  27. Paterson AH, Wendel JF, Gundlach H, Guo H, Jenkins J, Jin DC, Llewellyn D, Showmaker KC, Shu SQ, Udall J, Yoo MJ, Byers R, Chen W, Doron-Faigenboim A, Duke MV, Gong L, Grimwood J, Grover C, Grupp K, Hu GJ, Lee TH, Li JP, Lin LF, Liu T, Marler BS, Page JT, Roberts AW, Romanel E, Sanders WS, Szadkowski E, Tan X, Tang HB, Xu CM, Wang JP, Wang ZN, Zhang D, Zhang L, Ashrafi H, Bedon F, Bowers JE, Brubaker CL, Chee PW, Das S, Gingle AR, Haigler CH, Harker D, Hoffmann LV, Hovav R, Jones DC, Lemke C, Mansoor S, Rahman MU, Rainville LN, Rambani A, Reddy UK, Rong JK, Saranga Y, Scheffler BE, Scheffler JA, Stelly DM, Triplett BA, Van Deynze A, Vaslin MFS, Waghmare VN, Walford SA, Wright RJ, Zaki EA, Zhang TZ, Dennis ES, Mayer KFX, Peterson DG, Rokhsar DS, Wang XY, Schmutz J (2012) Repeated polyploidization of Gossypium genomes and the evolution of spinnable cotton fibres. Nature 492:423–427

  28. Poethig RS (2013) Vegetative phase change and shoot maturation in plants. Curr Top Dev Biol 105:125–152

  29. 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

  30. Preston JC, Hileman LC (2013) Functional evolution in the plant SQUAMOSA-PROMOTER BINDING PROTEIN-LIKE (SPL) gene family. Front Plant Sci 4:80

  31. Salinas M, Xing SP, 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

  32. Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3:1101–1108

  33. 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

  34. 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

  35. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

  36. 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

  37. 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

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

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

  40. Wang KB, Wang ZW, Li FG, Ye WW, Wang JY, Song GL, Yue Z, Cong L, Shang HH, Zhu SL, Zou CS, Li Q, Yuan YL, Lu CR, Wei HL, Gou CY, Zheng ZQ, Yin Y, Zhang XY, Liu K, Wang B, Song C, Shi N, Kohel RJ, Percy RG, Yu JZ, Zhu YX, Wang J, Yu SX (2012a) The draft genome of a diploid cotton Gossypium raimondii. Nat Genet 44:1098–1104

  41. Wang SK, Wu K, Yuan QB, Liu XY, Liu ZB, Lin XY, Zeng RZ, Zhu HT, Dong GJ, Qian Q, Zhang GQ, Fu XD (2012b) Control of grain size, shape and quality by OsSPL16 in rice. Nat Genet 44:950–955

  42. Wei S, Gruber MY, Yu BY, Gao MJ, Khachatourians GG, Hegedus DD, Parkin IAP, Hannoufa A (2012) Arabidopsis mutant sk156 reveals complex regulation of SPL15 in a miR156-controlled gene network. Bmc Plant Biol 12:169

  43. Wendel JF, Cronn RC (2003) Polyploidy and the evolutionary history of cotton. Adv Agron 78:139–186

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

  45. Xie KB, Wu CQ, Xiong LZ (2006) Genomic organization, differential expression, and interaction of SQUAMOSA promoter-binding-like transcription factors and microRNA156 in rice. Plant Physiol 142:280–293

  46. Jiao YQ, Wang YH, Xue DW, Wang J, Yan MX, Liu GF, Dong GJ, Zeng DL, Lu ZF, Zhu XD, Qian Q, Li JY (2010) Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice. Nat Genet 42:U536–U541

  47. 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

  48. 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

  49. 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

  50. Yang YZ, Jack T (2004) Defining subdomains of the K domain important for protein–protein interactions of plant MADS proteins. Plant Mol Biol 55:45–59

  51. 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 63:429–439

  52. Zhang LS, Wu B, Zhao DG, Li CL, Shao FJ, Lu SF (2014) Genome-wide analysis and molecular dissection of the SPL gene family in Salvia miltiorrhiza. J Integr Plant Biol 56:38–50

Download references

Acknowledgments

This research was funded by the National High-tech Research and Development Projects of China (2013AA102601) and supported by the Earmarked Fund for China Agriculture Research System (CARS-18).

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Correspondence to Chengshe Wang or Shuxun Yu.

Additional information

Communicated by S. Hohmann.

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

Keywords

  • Gossypium hirsutum
  • SPL
  • GhmiR156
  • Phylogenetic tree
  • Expression analysis