Skip to main content
Log in

Genome-wide identification and characterization of WUSCHEL-related homeobox (WOX) genes in Salix suchowensis

  • Original Paper
  • Published:
Journal of Forestry Research Aims and scope Submit manuscript

Abstract

Members of the WUSCHEL-related homeobox (WOX) transcription factor family are essential for determining cell fate and regulating diverse developmental processes in plants. Many WOX genes have been systematically investigated in woody plants such as Populus trichocarpa, but not in Salix suchowensis. Whole-genome sequence data for S. suchowensis is now available for comprehensive study of WOX genes in S. suchowensis. We thus surveyed the genome of S. suchowensis and demonstrated active expression of 15 WOX genes. In a phylogenetic analysis of WOX genes, the 15 SsWOX genes clustered among the modern/WUS, intermediate and ancient clades similar to the WOX genes of Arabidopsis thaliana. Based on the conserved intron/exon structure, SsWOX genes in the same subgroup had similar conserved exon–intron structures and motif domains. Furthermore, among several SsWOX subgroups, WUS (Wuschel)-box and EAR (the ERF-associated amphiphilic repression)-like motifs were conserved. Expression profiles of WOX genes in roots, stems and leaves indicate that SsWOX genes have various conserved roles in the tissues. Comparative analysis of the expression patterns in Salix suchowensis with that of Arabidopsis suggests that different shoot regeneration abilities are controlled by different WOX genes in plants. The analysis provide an overview of differentially expressed SsWOX genes during shoot regeneration, but also contribute to understanding the evolution of WOX genes in Salicaceae and the interrelations of WOX genes and other transcription factors, providing targets for further study.

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

Access this article

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

Instant access to the full article PDF.

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

Similar content being viewed by others

References

  • Bailey TL, Williams N, Misleh C (2006) MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Res 34(Web Server issue):W369

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bi C, Xu Y, Ye Q (2016) Genome-wide identification and characterization of WRKY gene family in Salix suchowensis. Peer J 4(9):e2437

    Article  PubMed  PubMed Central  Google Scholar 

  • Breuninger H et al (2008) Differential expression of WOX genes mediates apical-basal axis formation in the Arabidopsis embryo. Dev Cell 14(6):867–876

    Article  CAS  PubMed  Google Scholar 

  • Cao Y, Han Y, Meng D (2017) Genome-wide analysis suggests the relaxed purifying selection affect the evolution of WOX genes in Pyrus bretschneideri, Prunus persica, Prunus mume, and Fragaria vesca. Front Genet 8:78

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dai X, Hu Q, Cai Q (2014) The willow genome and divergent evolution from poplar after the common genome duplication. Cell Res 24(10):1274

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dolzblasz A, Nardmann J, Clerici E (2016) Stem cell regulation by arabidopsis WOX genes. Mol Plant 9(7):1028–1039

    Article  CAS  PubMed  Google Scholar 

  • Etchells JP, Provost CM, Mishra L (2013) WOX4 and WOX14 act downstream of the PXY receptor kinase to regulate plant vascular proliferation independently of any role in vascular organisation. Development 140(10):2224

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Finn RD, Bateman A, Clements J (2016) The Pfam protein families database. Nucleic Acids Res 42(Database issue):D222–230

    Google Scholar 

  • Gambino G, Minuto M, Boccacci P (2011) Characterization of expression dynamics of WOX homeodomain transcription factors during somatic embryogenesis in Vitis vinifera. J Exp Bot 62(3):1089

    Article  CAS  PubMed  Google Scholar 

  • Ge Y, Liu J, Zeng M (2016) Identification of WOX family genes in Selaginella kraussiana for studies on stem cells and regeneration in lycophytes. Front Plant Sci 7(291):93

    PubMed  PubMed Central  Google Scholar 

  • Graaff EVD, Laux T, Rensing SA (2009) The WUS homeobox-containing (WOX) protein family. Genome Biol 10(12):248

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gu Z, Cavalcanti A, Chen FC, Bouman P, Li WH (2002) Extent of gene duplication in the genomes of Drosophila, nematode, and yeast. Mol Biol Evol 19(3):256–262

    Article  CAS  PubMed  Google Scholar 

  • Haecker A, Grosshardt R, Geiges B (2004) Expression dynamics of WOX genes mark cell fate decisions during early embryonic patterning in Arabidopsis thaliana. Development 131(3):657–668

    Article  CAS  PubMed  Google Scholar 

  • Hirakawa Y, Kondo Y, Fukuda H (2010) TDIF peptide signaling regulates vascular stem cell proliferation via the wox4 homeobox gene in Arabidopsis. Plant Cell 22(8):2618–2629

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu B, Jin J, Guo A (2015) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31(8):1296

    Article  PubMed  Google Scholar 

  • Ikeda M, Ohme-Takagi M (2009) Arabidopsis WUSCHEL is a bifunctional transcription factor that acts as a repressor in stem cell regulation and as an activator in floral patterning. Plant Cell 21(11):3493–3505

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ji J, Shimizu R, Sinha N, Scanlon MJ (2010a) Analyses of WOX4 transgenics provide further evidence for the evolution of the gene family during the regulation of diverse stem cell functions. Plant Signal Behav 5(7):916–920

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ji J, Strable J, Shimizu R (2010b) WOX4 promotes procambial development. Plant Physiol 152(3):1346–1356

    Article  PubMed  Google Scholar 

  • Jin J, Tian F, Yang DC (2017) PlantTFDB 4.0: toward a central hub for transcription factors and regulatory interactions in plants. Nucleic Acids Res 45(Database issue):D1040–D1045

    Article  CAS  PubMed  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23(21):2947–2948

    Article  CAS  PubMed  Google Scholar 

  • Laux T, Mayer KF, Berger J (1996) The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. Development 122(1):87

    CAS  PubMed  Google Scholar 

  • Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25:1754–1760. https://doi.org/10.1093/bioinformatics/btp324

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lian G, Wang Q, Ding Z (2014) Origins and evolution of WUSCHEL-related homeobox protein family in plant kingdom. Sci World J 2014(1):534140

    Google Scholar 

  • Lin H, Niu L, McHale NA (2013) Evolutionarily conserved repressive activity of WOX proteins mediates leaf blade outgrowth and floral organ development in plants. Proc Natl Acad Sci USA 110(1):366

    Article  PubMed  Google Scholar 

  • Liu B, Wang L, Zhang J (2014) WUSCHEL-related homeobox genes in Populus tomentosa: diversified expression patterns and a functional similarity in adventitious root formation. BMC Genome 15(1):296

    Article  CAS  Google Scholar 

  • Luan F, Wang X, Shang L (2013) A highly efficient regeneration system for watermelon (Citrullus lanatus thunb.). Pak J Bot 45(1):145–150

    Google Scholar 

  • Oshchepkova EA, Omelyanchuk NA, Savina MS (2017) Systems biology analysis of the WOX5 gene and its functions in the root stem cell niche. Russ J Genet Appl Res 7(4):404–420

    Article  CAS  Google Scholar 

  • Romera-Branchat M, Ripoll JJ, Yanofsky MF (2013) The WOX13 homeobox gene promotes replum formation in the Arabidopsis thaliana fruit. Plant J 73(1):37–49

    Article  CAS  PubMed  Google Scholar 

  • Sarkar AK, Luijten M, Miyashima S (2007) Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature 446(7137):811

    Article  CAS  PubMed  Google Scholar 

  • Shimizu R, Ji J, Kelsey E (2009) Tissue specificity and evolution of meristematic WOX3 function. Plant Physiol 149(2):841

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suer S, Agusti J, Sanchez P (2011) WOX4 imparts auxin responsiveness to cambium cells in Arabidopsis. Plant Cell 23(9):3247

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Team RC (2004-2016) GUI 1.69. R: R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

  • Wang X, Cheng F, Rohlsen D (2018) Organellar genome assembly methods and comparative analysis of horticultural plants. Hortic Res 5(1):3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang Z, Gong Q, Qin W (2017) Genome-wide analysis of WOX genes in upland cotton and their expression pattern under different stresses. BMC Plant Biol 17(1):113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ye N, Wang X, Li J (2017) Assembly and comparative analysis of complete mitochondiral genome sequence of an economic plant Salix suchowensis. Peer J 5:e3148

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang X, Zong J, Liu J (2010) Genome-wide analysis of WOX gene family in rice, sorghum, maize, Arabidopsis and poplar. Bull Bot 52(11):1016–1026

    CAS  Google Scholar 

  • Zhang Y, Wu R, Qin G (2011) Over-expression of WOX1 leads to defects in meristem development and polyamine homeostasis in Arabidopsis. J Integr Plant Biol 53(6):493–506

    Article  CAS  PubMed  Google Scholar 

  • Zhang F, Wang Y, Li G (2014) Stenofolia recruits topless to repress asymmetric LEAVES2 at the leaf margin and promote leaf blade outgrowth in Medicago truncatula. Plant Cell 26(2):650

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang N, Huang X, Bao Y (2015) Genome-wide identification and expression profiling of WUSCHEL-related homeobox (WOX) genes during adventitious shoot regeneration of watermelon (Citrullus lanatus). Acta Physiol Plant 37(11):1–12

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ning Ye.

Additional information

Project funding: This study was supported by the National Key Research and Development Plan of China (2016YFD0600101), the Fundamental Research Funds for the Central Non-Profit Research Institution of CAF (CAFYBB2014QB015), the National Natural Science Foundation of China (31570662, 31500533, and 61401214), Jiangsu Provincial Department of Housing and Urban–Rural Development (2016ZD44), 2017 Graduate Research and Innovation Program Projects in Jiangsu Province (KYCY17_0827), and the PAPD (Priority Academic Program Development) program at Nanjing Forestry University.

The online version is available at http://www.springerlink.com

Corresponding editor: Yu Lei.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 486 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, X., Bi, C., Wang, C. et al. Genome-wide identification and characterization of WUSCHEL-related homeobox (WOX) genes in Salix suchowensis. J. For. Res. 30, 1811–1822 (2019). https://doi.org/10.1007/s11676-018-0734-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11676-018-0734-2

Keywords

Navigation