Advertisement

Journal of Forestry Research

, Volume 30, Issue 5, pp 1811–1822 | Cite as

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

  • Xuelin Wang
  • Changwei Bi
  • Chunyan Wang
  • Qiaolin Ye
  • Tongming Yin
  • Ning YeEmail author
Original Paper
  • 108 Downloads

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.

Keywords

WOX family Salicaceae Expression Evolution Duplication 

Supplementary material

11676_2018_734_MOESM1_ESM.pdf (487 kb)
Supplementary material 1 (PDF 486 kb)

References

  1. Bailey TL, Williams N, Misleh C (2006) MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Res 34(Web Server issue):W369CrossRefGoogle Scholar
  2. Bi C, Xu Y, Ye Q (2016) Genome-wide identification and characterization of WRKY gene family in Salix suchowensis. Peer J 4(9):e2437CrossRefGoogle Scholar
  3. Breuninger H et al (2008) Differential expression of WOX genes mediates apical-basal axis formation in the Arabidopsis embryo. Dev Cell 14(6):867–876CrossRefGoogle Scholar
  4. 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 8:78CrossRefGoogle Scholar
  5. Dai X, Hu Q, Cai Q (2014) The willow genome and divergent evolution from poplar after the common genome duplication. Cell Res 24(10):1274CrossRefGoogle Scholar
  6. Dolzblasz A, Nardmann J, Clerici E (2016) Stem cell regulation by arabidopsis WOX genes. Mol Plant 9(7):1028–1039CrossRefGoogle Scholar
  7. 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):2224CrossRefGoogle Scholar
  8. Finn RD, Bateman A, Clements J (2016) The Pfam protein families database. Nucleic Acids Res 42(Database issue):D222–230Google Scholar
  9. 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):1089CrossRefGoogle Scholar
  10. 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):93Google Scholar
  11. Graaff EVD, Laux T, Rensing SA (2009) The WUS homeobox-containing (WOX) protein family. Genome Biol 10(12):248CrossRefGoogle Scholar
  12. 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):256–262CrossRefGoogle Scholar
  13. 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):657–668CrossRefGoogle Scholar
  14. 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):2618–2629CrossRefGoogle Scholar
  15. Hu B, Jin J, Guo A (2015) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31(8):1296CrossRefGoogle Scholar
  16. 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):3493–3505CrossRefGoogle Scholar
  17. 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):916–920CrossRefGoogle Scholar
  18. Ji J, Strable J, Shimizu R (2010b) WOX4 promotes procambial development. Plant Physiol 152(3):1346–1356CrossRefGoogle Scholar
  19. 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–D1045CrossRefGoogle Scholar
  20. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870CrossRefGoogle Scholar
  21. Larkin MA, Blackshields G, Brown NP (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23(21):2947–2948CrossRefGoogle Scholar
  22. Laux T, Mayer KF, Berger J (1996) The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. Development 122(1):87Google Scholar
  23. 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 CrossRefGoogle Scholar
  24. Lian G, Wang Q, Ding Z (2014) Origins and evolution of WUSCHEL-related homeobox protein family in plant kingdom. Sci World J 2014(1):534140Google Scholar
  25. 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):366CrossRefGoogle Scholar
  26. 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):296CrossRefGoogle Scholar
  27. Luan F, Wang X, Shang L (2013) A highly efficient regeneration system for watermelon (Citrullus lanatus thunb.). Pak J Bot 45(1):145–150Google Scholar
  28. 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):404–420CrossRefGoogle Scholar
  29. Romera-Branchat M, Ripoll JJ, Yanofsky MF (2013) The WOX13 homeobox gene promotes replum formation in the Arabidopsis thaliana fruit. Plant J 73(1):37–49CrossRefGoogle Scholar
  30. Sarkar AK, Luijten M, Miyashima S (2007) Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature 446(7137):811CrossRefGoogle Scholar
  31. Shimizu R, Ji J, Kelsey E (2009) Tissue specificity and evolution of meristematic WOX3 function. Plant Physiol 149(2):841CrossRefGoogle Scholar
  32. Suer S, Agusti J, Sanchez P (2011) WOX4 imparts auxin responsiveness to cambium cells in Arabidopsis. Plant Cell 23(9):3247CrossRefGoogle Scholar
  33. Team RC (2004-2016) GUI 1.69. R: R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
  34. Wang X, Cheng F, Rohlsen D (2018) Organellar genome assembly methods and comparative analysis of horticultural plants. Hortic Res 5(1):3CrossRefGoogle Scholar
  35. 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):113CrossRefGoogle Scholar
  36. 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:e3148CrossRefGoogle Scholar
  37. 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):1016–1026Google Scholar
  38. 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):493–506CrossRefGoogle Scholar
  39. 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):650CrossRefGoogle Scholar
  40. 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):1–12CrossRefGoogle Scholar

Copyright information

© Northeast Forestry University and Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Xuelin Wang
    • 1
  • Changwei Bi
    • 2
  • Chunyan Wang
    • 1
  • Qiaolin Ye
    • 1
  • Tongming Yin
    • 3
  • Ning Ye
    • 1
    Email author
  1. 1.College of Information Science and TechnologyNanjing Forestry UniversityNanjingPeople’s Republic of China
  2. 2.School of Biological Science and Medical EngineeringSoutheast UniversityNanjingPeople’s Republic of China
  3. 3.College of Forest Resources and EnvironmentNanjing Forestry UniversityNanjingPeople’s Republic of China

Personalised recommendations