Genome wide characterization of WUSCHEL-related homeobox (WOX) gene family in Apostasia shenzhenica, a primeval orchid

Authors

  • Thakku R Ramkumar Department of Botany, Panjab University, Chandigarh 160 014, India
  • Madhvi Kanchan Department of Botany, Panjab University, Chandigarh 160 014, India
  • Jaspreet K. Sembi Department of Botany, Panjab University, Chandigarh 160 014, India

DOI:

https://doi.org/10.14719/pst.2020.7.2.703

Keywords:

WOX, WUSCHEL, Apostasia shenzhenica

Abstract

In the present study, we report identification and characterization of the plant-specific WUSCHEL-related homeobox (WOX) gene family in Apostasia shenzhenica, a primeval orchid. WOX proteins are DNA-binding WUSCHEL-related homeobox (WOX) encoding transcription factors that play critical role in zygote patterning, embryo development, organogenesis, florigenesis, stress responses etc. Ten putative AsWOX genes were predicted in the A. shenzhenica genome and were characterized by the presence of DNA-binding helix-loop-helix-turn-helix motif. AsWOX proteins were grouped into three clades, ancient, intermediate and WUS on the basis of sequence homology with Arabidopsis thaliana (AtWOX), Oryza sativa (OsWOX), Phalaenopsis equestris (PeWOX) and Dendrobium catenatum (DcWOX) and their phylogenetic relationship was established. Gene structure analysis revealed that three AsWOX genes had two introns, six genes had a single intron, and one gene was intron-less. Expression profiling in a variety of tissue (tubers, seeds and pollens) was analysed in light of the presence of specific cis-regulatory elements in the promoter region and their role in various developmental processes was discussed. Three dimensional structures were predicted for three selected AsWOX proteins representing the three clades. The present study provides insights to the role of AsWOX gene family in various vital developmental processes, establishes phylogenetic relationships with related plant species and provides a platform for functional validation of specific AsWOX genes.

Downloads

Download data is not yet available.

References

1. van der Graaff E, Laux T, Rensing SA. The WUS homeobox-containing (WOX) protein family. Genome Biology. 2009;10(12):248. https://doi.org/10.1186/gb-2009-10-12-248

2. Nic-Can GI, Lopez-Torres A, Barredo-Pool F, Wrobel K, Loyola-Vargas VM, Rojas-Herrera R, De-la-Pena C. New insights into somatic embryogenesis: LEAFY COTYLEDON1, BABY BOOM1 and WUSCHEL-RELATED HOMEOBOX4 are epigenetically regulated in Coffea canephora. PLoS One. 2013;8(8):e72160. https://doi.org/10.1371/journal.pone.0072160

3. Costanzo E, Trehin C, Vandenbussche M. The role of WOX genes in flower development. Annals of Botany. 2014; 114(7):1545-53. https://doi.org/10.1093/aob/mcu123

4. Gehring WJ, Affolter M, Bürglin T. Homeodomain proteins. Annual Review of Biochemistry. 1994;63(1):487-526. https://doi.org/10.1146/annurev.bi.63.070194.002415

5. Kamiya N, Nagasaki H, Morikami A, Sato Y, Matsuoka M. Isolation and characterization of a rice WUSCHEL?type homeobox gene that is specifically expressed in the central cells of a quiescent center in the root apical meristem. The Plant Journal. 2003;35(4):429-41. https://doi.org/10.1046/j.1365-313X.2003.01816.x

6. Laux T, Mayer KF, Berger J, Jurgens G. The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. Development. 1996;122(1):87-96. https://doi.org/10.1371/journal.pone.0038161

7. Deveaux Y, Toffano-Nioche C, Claisse G, Thareau V, Morin H, Laufs P, Moreau H, Kreis M, Lecharny A. Genes of the most conserved WOX clade in plants affect root and flower development in Arabidopsis. BMC Evolutionary Biology. 2008;8(1):291. https://doi.org/10.1186/1471-2148-8-291

8. Ge Y, Liu J, Zeng M, He J, Qin P, Huang H, Xu L. Identification of WOX family genes in Selaginella kraussiana for studies on stem cells and regeneration in lycophytes. Frontiers in Plant Science. 2016;7:93. https://doi.org/10.3389/fpls.2016.00093

9. Hedman H, Zhu T, von Arnold S, Sohlberg JJ. Analysis of the WUSCHEL-RELATED HOMEOBOX gene family in the conifer Picea abies reveals extensive conservation as well as dynamic patterns. BMC Plant Biology. 2013;13(1):89. https://doi.org/10.1186/1471-2229-13-89

10. Zhang X, Zong J, Liu J, Yin J, Zhang D. Genome?wide analysis of WOX gene family in rice, sorghum, maize, Arabidopsis and poplar. Journal of Integrative plant biology. 2010; 52(11):1016-26. https://doi.org/10.1111/j.1744-7909.2010.00982.x

11. Li XX, Liu C, Li W, Zhang ZL, Gao XM, Zhou H, Guo YF. Genome-wide identification, phylogenetic analysis and expression profiling of the WOX family genes in Solanum lycopersicum. Yi chuan= Hereditas. 2016;38(5):444-60. http://www.cnki.net/kcms/detail/11.1913.R.20160331.1108.006.html

12. Shchennikova AV, Shulga OA, Kochieva EZ, Beletsky AV, Filyushin MA, Ravin NV, Skryabin KG. Homeobox genes encoding WOX transcription factors in the flowering parasitic plant Monotropa hypopitys. Russian Journal of Genetics: Applied Research. 2017;7(7):781-88. https://doi.org/10.1134/S2079059717070085

13. Tang F, Chen N, Zhao M, Wang Y, He R, Peng X, Shen S. Identification and functional divergence analysis of WOX gene family in paper mulberry. International Journal of Molecular Sciences. 2017;18(8):1782. https://doi.org/10.3390/ijms18081782

14. Cao Y, Han Y, Meng D, Li G, Li D, Abdullah M, Jin Q, Lin Y, Cai Y. Genome-wide analysis suggests the relaxed purifying selection affect the evolution of WOX genes in Pyrus bretschneideri, Prunus persica, Prunus mume and Fragaria vesca. Frontiers in Genetics. 2017;8:78. https://doi.org/10.3389/fgene.2017.00078

15. Li Y, Zhu Y, Yao J, Zhang S, Wang L, Guo C, Van Nocker S, Wang X. Genome-wide identification and expression analyses of the homeobox transcription factor family during ovule development in seedless and seeded grapes. Scientific Reports. 2017;7(1):1-6. https://doi.org/10.1038/s41598-017-12988-y

16. Yang Z, Gong Q, Qin W, Yang Z, Cheng Y, Lu L, Ge X, Zhang C, Wu Z, Li F. Genome-wide analysis of WOX genes in upland cotton and their expression pattern under different stresses. BMC Plant Biology. 2017;17(1):113. https://doi.org/10.1186/s12870-017-1065-8

17. Zhang N, Huang X, Bao Y, Wang B, Liu L, Dai L, Chen J, An X, Sun Y, Peng D. Genome-wide identification and expression profiling of WUSCHEL-related homeobox (WOX) genes during adventitious shoot regeneration of watermelon (Citrullus lanatus). Acta physiologiae Plantarum. 2015;37(11):224. https://doi.org/10.1007/s11738-015-1964-y

18. Rahman ZU, Azam SM, Liu Y, Yan C, Ali H, Zhao L, Chen P, Yi L, Priyadarshani SV, Yuan Q. Expression profiles of Wuschel-related homeobox gene family in pineapple (Ananas comosus L.). Tropical Plant Biology. 2017;4(10):204-15. https://doi.org/10.1007/s12042-017-9192-9

19. Ramkumar TR, Kanchan M, Upadhyay SK, Sembi JK. Identification and characterization of WUSCHEL-related homeobox (WOX) gene family in economically important orchid species Phalaenopsis equestris and Dendrobium catenatum. Plant Gene. 2018;14:37-45. https://doi.org/10.1016/j.plgene.2018.04.004

20. Wang X, Bi C, Wang C, Ye Q, Yin T, Ye N. Genome-wide identification and characterization of WUSCHEL-related homeobox (WOX) genes in Salix suchowensis. Journal of Forestry Research. 2019;30(5):1811-22.https://doi.org/10.1007/s11676-018-0734-2

21. Wang P, Guo Y, Chen X, Zheng Y, Sun Y, Yang J, Ye N. Genome-wide identification of WOX genes and their expression patterns under different hormone and abiotic stress treatments in tea plant (Camellia sinensis). Trees. 2019; 33(4):1129-42. https://doi.org/10.1007/s00468-019-01847-0

22. Li M, Wang R, Liu Z, Wu X, Wang J. Genome-wide identification and analysis of the WUSCHEL-related homeobox (WOX) gene family in allotetraploid Brassica napus reveals changes in WOX genes during polyploidization. BMC Genomics. 2019; 20(1): 317. https://doi.org/10.1186/s12864-019-5684-3

23. Chang Y, Song X, Zhang Q, Liu H, Bai Y, Lei X, Pei D. Genome-Wide Identification of WOX Gene Family and Expression Analysis during Rejuvenational Rhizogenesis in Walnut (Juglans regia L.). Forests. 2020;11(1):16. https://doi.org/10.3390/f11010016

24. Cai J, Liu X, Vanneste K, Proost S, Tsai WC, Liu KW, Chen LJ, He Y, Xu Q, Bian C, Zheng Z. The genome sequence of the orchid Phalaenopsis equestris. Nature Genetics. 2015; 47(1): 65-72. https://doi.org/10.1038/ng.3149

25. Zhang GQ, Xu Q, Bian C, Tsai WC, Yeh CM, Liu KW, Yoshida K, Zhang LS, Chang SB, Chen F, Shi Y. The Dendrobium catenatum Lindl. genome sequence provides insights into polysaccharide synthase, floral development and adaptive evolution. Scientific Reports. 2016;6(1):1-10. https://doi.org/10.1038/srep19029

26. Zhang GQ, Liu KW, Li Z, Lohaus R, Hsiao YY, Niu SC, Wang JY, Lin YC, Xu Q, Chen LJ, Yoshida K. The Apostasia genome and the evolution of orchids. Nature. 2017;549(7672):379-83. https://doi.org/10.1038/nature23897

27. Givnish TJ, Spalink D, Ames M, Lyon SP, Hunter SJ, Zuluaga A, Iles WJ, Clements MA, Arroyo MT, Leebens-Mack J, Endara L. Orchid phylogenomics and multiple drivers of their extraordinary diversification. Proceedings of the Royal Society B: Biological Sciences. 2015;282(1814):20151553. https://doi.org/10.1098/rspb.2015.1553

28. Schultz J, Copley RR, Doerks T, Ponting CP, Bork P. SMART: a web-based tool for the study of genetically mobile domains. Nucleic Acids Research. 2000;28(1):231-34. https://doi.org/10.1093/nar/28.1.231

29. Sigrist CJ, De Castro E, Cerutti L, Cuche BA, Hulo N, Bridge A, Bougueleret L, Xenarios I. New and continuing developments at PROSITE. Nucleic Acids Research. 2012;41(D1):D344-7. https://doi.org/10.1093/nar/gks1067

30. Corpet F. Multiple sequence alignment with hierarchical clustering. Nucleic Acids Research. 1988;16(22):10881-90. https://doi.org/10.1093/nar/16.22.10881

31. Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Research. 2009; 37(suppl_2):W202-8. https://doi.org/10.1093/nar/gkp335

32. Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution. 2016;33(7):1870-74. https://doi.org/10.1093/molbev/msw054

33. Gasteiger E, Hoogland C, Gattiker A, Duvaud S, Wilkins MR, Appel RD, Bairoch A. Protein identification and analysis tools on the ExPASy server. Springer. 2005:571-607. https://doi.org/10.1385/1-59259-890-0:571

34. Petersen TN, Brunak S, Von Heijne G, Nielsen H. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nature Methods. 2011; 8(10): 785. https://doi.org/10.1038/nmeth.1701.

35. Krogh A, Larsson B, Von Heijne G, Sonnhammer EL. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. Journal of Molecular Biology. 2001;305(3):567-80. https://doi.org/10.1006/jmbi.2000.4315

36. Yu CS, Chen YC, Lu CH, Hwang JK. Prediction of protein subcellular localization. Proteins: Structure, Function, and Bioinformatics. 2006;64(3):643-51. https://doi.org/10.1002/prot.21018

37. Horton P, Park KJ, Obayashi T, Fujita N, Harada H, Adams-Collier CJ, Nakai K. WoLF PSORT: protein localization predictor. Nucleic Acids Research. 2007;35(suppl_2):W585-7. https://doi.org/10.1093/nar/gkm259

38. Emanuelsson O, Nielsen H, Brunak S, Von Heijne G. Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. Journal of Molecular Biology. 2000; 300(4):1005-16. https://doi.org/10.1006/jmbi.2000.3903

39. Chou KC, Shen HB. Plant-mPLoc: a top-down strategy to augment the power for predicting plant protein subcellular localization. PLoS One. 2010;5(6). https://dx.doi.org/10.1371%2Fjournal.pone.0011335

40. Hu B, Jin J, Guo AY, Zhang H, Luo J, Gao G. GSDS 2.0: an upgraded gene features visualization server. Bioinformatics. 2015;31:1296-97. https://doi.org/10.1093/bioinformatics/btu817

41. Higo K, Ugawa Y, Iwamoto M, Korenaga T. Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Research. 1999;27(1):297-300. https://doi.org/10.1093/nar/27.1.297

42. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic acids research. 2004;32(5):1792-7. https://doi.org/10.1093/nar/gkh340

43. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nature Methods. 2008;5(7):621. https://doi.org/10.1038/nmeth.1226

44. Seo J, Gordish-Dressman H, Hoffman EP. An interactive power analysis tool for microarray hypothesis testing and generation. Bioinformatics. 2006;22(7):808-14. https://doi.org/10.1093/bioinformatics/btk052

45. Sapay N, Guermeur Y, Deléage G. Prediction of amphipathic in-plane membrane anchors in monotopic proteins using a SVM classifier. BMC bioinformatics. 2006;7(1):255. https://dx.doi.org/10.1186%2F1471-2105-7-255

46. Yang J, Yan R, Roy A, Xu D, Poisson J, Zhang Y. The I-TASSER Suite: protein structure and function prediction. Nature Methods. 2015;12(1):7. https://doi.org/10.1038/nmeth.3213

47. Jha P, Ochatt SJ, Kumar V. WUSCHEL: a master regulator in plant growth signaling. Plant Cell Reports. 2020:1-4. https://doi.org/10.1007/s00299-020-02511-5

48. Colombo L, Battaglia R, Kater MM. Arabidopsis ovule development and its evolutionary conservation. Trends in Plant Science. 2008;13(8):444-50. https://doi.org/10.1016/j.tplants.2008.04.011

49. Mayer KF, Schoof H, Haecker A, Lenhard M, Jürgens G, Laux T. Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell. 1998;95(6):805-15. https://doi.org/10.1016/S0092-8674(00)81703-1

50. Sakakibara K, Reisewitz P, Aoyama T, Friedrich T, Ando S, Sato Y, Tamada Y, Nishiyama T, Hiwatashi Y, Kurata T, Ishikawa M. WOX13-like genes are required for reprogramming of leaf and protoplast cells into stem cells in the moss Physcomitrella patens. Development. 2014;141(8):1660-70. https://doi.org/10.1242/dev.097444

51. Romera?Branchat M, Ripoll JJ, Yanofsky MF, Pelaz S. The WOX 13 homeobox gene promotes replum formation in the Arabidopsis thaliana fruit. The Plant Journal. 2013;73(1):37-49. https://doi.org/10.1111/tpj.12010

52. Etchells JP, Provost CM, Mishra L, Turner SR. WOX4 and WOX14 act downstream of the PXY receptor kinase to regulate plant vascular proliferation independently of any role in vascular organisation. Development. 2013;140(10):2224-34. https://doi.org/10.1242/dev.091314

53. Denis E, Kbiri N, Mary V, Claisse G, Conde e Silva N, Kreis M, Deveaux Y. WOX 14 promotes bioactive gibberellin synthesis and vascular cell differentiation in Arabidopsis. The Plant Journal. 2017;90(3):560-72. https://doi.org/10.1111/tpj.13513

54. Breuninger H, Rikirsch E, Hermann M, Ueda M, Laux T. Differential expression of WOX genes mediates apical-basal axis formation in the Arabidopsis embryo. Developmental Cell. 2008;14(6):867-76. https://doi.org/10.1016/j.devcel.2008.03.008

55. Ueda M, Zhang Z, Laux T. Transcriptional activation of Arabidopsis axis patterning genes WOX8/9 links zygote polarity to embryo development. Developmental cell. 2011;20(2):264-70. https://doi.org/10.1016/j.devcel.2011.01.009

56. Ikeda M, Mitsuda N, Ohme-Takagi M. Arabidopsis WUSCHEL is a bifunctional transcription factor that acts as a repressor in stem cell regulation and as an activator in floral patterning. The Plant Cell. 2009;21(11):3493-505. https://doi.org/10.1105/tpc.109.069997

57. Zuo J, Niu QW, Frugis G, Chua NH. The WUSCHEL gene promotes vegetative?to?embryonic transition in Arabidopsis. The Plant Journal. 2002;30(3):349-59. https://doi.org/10.1046/j.1365-313X.2002.01289.x

58. Su YH, Zhao XY, Liu YB, Zhang CL, O’Neill SD, Zhang XS. Auxin?induced WUS expression is essential for embryonic stem cell renewal during somatic embryogenesis in Arabidopsis. The Plant Journal. 2009;59(3):448-60. https://doi.org/10.1111/j.1365-313X.2009.03880.x

Published

01-04-2020

How to Cite

1.
Ramkumar TR, Kanchan M, Sembi JK. Genome wide characterization of WUSCHEL-related homeobox (WOX) gene family in Apostasia shenzhenica, a primeval orchid. Plant Sci. Today [Internet]. 2020 Apr. 1 [cited 2024 Nov. 21];7(2):164-71. Available from: https://horizonepublishing.com/journals/index.php/PST/article/view/703

Issue

Section

Research Articles

Most read articles by the same author(s)