Functional analysis of WOX family genes in Dendrobium catenatum during growth and development
Received date: 2023-02-28
Revised date: 2023-07-13
Online published: 2023-07-24
Supported by
Major Scientific and Technological R&D Projects of Yunnan Province(202102AE090042);Major Scientific and Technological Projects for New Agricultural Varieties Breeding in Zhejiang Province(2021C02074);National Natural Science Foundation of China(31870310)
The WUSCHEL-Related Homeobox (WOX) family is a group of transcription factors unique to plants that play an important role in regulating key developmental processes such as stem cell maintenance and organ morphogenesis. As a rare and valuable Chinese herb, Dendrobium catenatum has a unique epiphytic lifestyle and growth and developmental characteristics, and a functional investigation of its WOX family genes can help to further understand the conserved and specific development of D. catenatum. In this study, we analyzed the phylogeny, spatio-temporal expression pattern and heterologous expression function of D. catenatum WOX family genes (DcWOX). The results showed that members of the D. catenatum WOX gene family could be divided into three evolutionary branches with significantly different tissue expression profiles. In transgenic Arabidopsis, overexpression of DcWOX4 resulted in significant dwarfism, pinnately leaf margins, and delayed flowering for 2 weeks; overexpression of DcWOX9 resulted in plant dwarfing, serrated leaf margin, delayed flowering for 1 week, and even male and female sterility in strong phenotype plants; overexpression of DcWOX11 caused curl downward leaf. The abnormal morphogenesis of DcWOX4/9/11 overexpression Arabidopsis leaves are related to the down-regulation of TCP family genes, CUC family genes and the up-regulation of KNOX family genes; Postponement of flowering is related to down-regulation of early flowering genes such as FT, SOC1 and CO. Therefore, this study showed that D. catenatum WOX family genes have important functions in regulating plant morphogenesis, leaf development, flowering time and fertility, further expanding the understanding of the WOX gene family function, and providing clues for the conservation and specificity during orchid development and evolution.
Key words: Dendrobium catenatum; WOX gene family; transgenic Arabidopsis
Kai Chen, Hao Wang, Yiting Chen, Ke Fu, Zhigang Han, Cong Li, Jinping Si, Donghong Chen . Functional analysis of WOX family genes in Dendrobium catenatum during growth and development[J]. Hereditas(Beijing), 2023 , 45(8) : 700 -714 . DOI: 10.16288/j.yczz.22-392
| [1] | van der Graaff E, Laux T, Rensing SA. The WUS homeobox-containing (WOX) protein family. Genome Biol, 2009, 10(12): 248. |
| [2] | Laux T, Mayer KF, Berger J, Jürgens G. The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. Development, 1996, 122(1): 87-96. |
| [3] | Lian GB, Ding ZW, Wang Q, Zhang DB, Xu J.Origins and evolution of WUSCHEL-related homeobox protein family in plant kingdom. Scientific World J, 2014, 2014: 534140. |
| [4] | Mukherjee K, Brocchieri L, Bürglin TR. A comprehensive classification and evolutionary analysis of plant homeobox genes. Mol Biol Evol, 2009, 26(12): 2775-2794. |
| [5] | Romera-Branchat M, Ripoll JJ, Yanofsky MF, Pelaz S. The WOX13 homeobox gene promotes replum formation in the Arabidopsis thaliana fruit. Plant J, 2013, 73(1): 37-49. |
| [6] | 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 Evol Biol, 2008, 8: 291. |
| [7] | Denis E, Kbiri N, Mary V, Claisse G, Conde E Silva N, Kreis M, Deveaux Y.WOX14 promotes bioactive gibberellin synthesis and vascular cell differentiation in Arabidopsis. Plant J, 2017, 90(3): 560-572. |
| [8] | Wu XL, Dabi T, Weigel D. Requirement of homeobox gene STIMPY/WOX9 for Arabidopsis meristem growth and maintenance. Curr Biol, 2005, 15(5): 436-440. |
| [9] | Lie C, Kelsom C, Wu XL.WOX2 and STIMPY-LIKE/ WOX8 promote cotyledon boundary formation in Arabidopsis. Plant J, 2012, 72(4): 674-682. |
| [10] | Sheng LH, Hu XM, Du YJ, Zhang GF, Huang H, Scheres B, Xu L. Non-canonical WOX11-mediated root branching contributes to plasticity in Arabidopsis root system architecture. Development, 2017, 144(17): 3126-3133. |
| [11] | Wan QH, Zhai N, Xie DX, Liu W, Xu L. WOX11: the founder of plant organ regeneration. Cell Regen, 2023, 12(1): 1. |
| [12] | Liu JC, Sheng LH, Xu YQ, Li JQ, Yang ZN, Huang H, Xu L.WOX11 and 12 are involved in the first-step cell fate transition during de novo root organogenesis in Arabidopsis. Plant Cell, 2014, 26(3): 1081-1093. |
| [13] | Nardmann J, Reisewitz P, Werr W. Discrete shoot and root stem cell-promoting WUS/WOX5 functions are an evolutionary innovation of angiosperms. Mol Biol Evol, 2009, 26(8): 1745-1755. |
| [14] | 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): 805-815. |
| [15] | Zhang ZJ, Tucker E, Hermann M, Laux T. A molecular framework for the embryonic initiation of shoot meristem stem cells. Dev Cell, 2017, 40(3): 264-277.e4. |
| [16] | Chung K, Sakamoto S, Mitsuda N, Suzuki K, Ohme- Takagi M, Fujiwara S. WUSCHEL-RELATED HOMEOBOX2 is a transcriptional repressor involved in lateral organ formation and separation in Arabidopsis. Plant Biotechnol (Tokyo), 2016, 33(4): 245-253. |
| [17] | Matsumoto N, Okada K. A homeobox gene, PRESSED FLOWER, regulates lateral axis-dependent development of Arabidopsis flowers. Genes Dev, 2001, 15(24): 3355-3364. |
| [18] | Suer S, Agusti J, Sanchez P, Schwarz M, Greb T.WOX4 imparts auxin responsiveness to cambium cells in Arabidopsis. Plant Cell, 2011, 23(9): 3247-3259. |
| [19] | Brackmann K, Qi JY, Gebert M, Jouannet V, Schlamp T, Grünwald K, Wallner ES, Novikova DD, Levitsky VG, Agustí J, Sanchez P, Lohmann JU, Greb T. Spatial specificity of auxin responses coordinates wood formation. Nat Commun, 2018, 9(1): 875. |
| [20] | Gonzali S, Novi G, Loreti E, Paolicchi F, Poggi A, Alpi A, Perata P.A turanose-insensitive mutant suggests a role for WOX5 in auxin homeostasis in Arabidopsis thaliana. Plant J, 2005, 44(4): 633-645. |
| [21] | Sarkar AK, Luijten M, Miyashima S, Lenhard M, Hashimoto T, Nakajima K, Scheres B, Heidstra R, Laux T. Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature, 2007, 446(7137): 811-814. |
| [22] | Tian HY, Wabnik K, Niu TT, Li HB, Yu QQ, Pollmann S, Vanneste S, Govaerts W, Rolcík J, Geisler M, Friml J, Ding ZJ. WOX5-IAA17 feedback circuit-mediated cellular auxin response is crucial for the patterning of root stem cell niches in Arabidopsis. Mol Plant, 2014, 7(2): 277-289. |
| [23] | Wang W, Li G, Zhao J, Chu H, Lin W, Zhang D, Wang Z, Liang WJPG. DWARF TILLER1, a WUSCHEL-related homeobox transcription factor, is required for tiller growth in rice. PLoS Genet, 2014, 10(3): e1004154-e1004154. |
| [24] | Hendelman A, Zebell S, Rodriguez-Leal D, Dukler N, Robitaille G, Wu XL, Kostyun J, Tal L, Wang PP, Bartlett ME, Eshed Y, Efroni I, Lippman ZB. Conserved pleiotropy of an ancient plant homeobox gene uncovered by cis- regulatory dissection. Cell, 2021, 184(7): 1724-1739.e16. |
| [25] | Cheng SF, Tan F, Lu Y, Liu XY, Li TT, Yuan WJ, Zhao Y, Zhou DX. WOX11 recruits a histone H3K27me3 demethylase to promote gene expression during shoot development in rice. Nucleic Acids Res, 2018, 46(5): 2356-2369. |
| [26] | Sun WQ, Gao DW, Xiong Y, Tang XX, Xiao XF, Wang CR, Yu SB. Hairy leaf 6, an AP2/ERF transcription factor, interacts with OsWOX3B and regulates trichome formation in rice. Mol Plant, 2017, 10(11): 1417-1433. |
| [27] | Ji JB, Shimizu R, Sinha N, Scanlon MJ. Analyses of WOX4 transgenics provide further evidence for the evolution of the WOX gene family during the regulation of diverse stem cell functions. Plant Signal Behav, 2010, 5(7): 916-920. |
| [28] | Si JP, Zhang Y, Luo YB, Liu JJ, Liu ZJ. Herbal textual research on relationship between Chinese medicine“Shihu” (Dendrobium spp.)and “Tiepi Shihu” (D. catenatum). China J Chin Mater Med, 2017, 42(10):191-195. |
| [28] | 斯金平, 张媛, 罗毅波, 刘京晶, 刘仲健. 石斛与铁皮石斛关系的本草考证. 中国中药杂志, 2017, 42(10): 191-195. |
| [29] | Lin YK, Zhu YQ, SI JP, Qin L, Zhu Y, Wu LS, Liu JJ. Effects of cultivation environments on Dendrobium catenatum. China J Chin Mater Med, 2017, 42(16): 62-67. |
| [29] | 林弋凯, 朱玉球, 斯金平, 秦朗, 诸燕, 吴令上, 刘京晶. 栽培环境对铁皮石斛生长与代谢成分的影响. 中国中药杂志, 2017, 42(16): 62-67. |
| [30] | Chen DH, Qiu HL, Huang Y, Zhang L, Si JP. Genome- wide identification and expression profiling of SET DOMAIN GROUP family in Dendrobium catenatum. BMC Plant Biol, 2020, 20(1): 40. |
| [31] | Xu L, Shen WH. Polycomb silencing of KNOX genes confines shoot stem cell niches in Arabidopsis. Curr Biol, 2008, 18(24): 1966-1971. |
| [32] | Clough SJ, Bent AF. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J, 1998, 16(6): 735-743. |
| [33] | Zhang GQ, Xu Q, Bian C, Tsai WC, Yeh CM, Liu KW, Yoshida K, Zhang LS, Chang SB, Chen F, Shi Y, Su YY, Zhang YQ, Chen LJ, Yin YY, Lin M, Huang HX, Deng H, Wang ZW, Zhu SL, Zhao X, Deng C, Niu SC, Huang J, Wang MN, Liu GH, Yang HJ, Xiao XJ, Hsiao YY, Wu WL, Chen YY, Mitsuda N, Ohme-Takagi M, Luo YB, Van de Peer Y, Liu ZJ. The Dendrobium catenatum Lindl. genome sequence provides insights into polysaccharide synthase, floral development and adaptive evolution. Sci Rep, 2016, 6: 19029. |
| [34] | Chen CJ, Chen H, Zhang Y, Thomas HR, Frank MH, He Y, Xia R. TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant, 2020, 13(8): 1194-1202. |
| [35] | Segatto ALA, Thompson CE, Freitas LB. Molecular evolution analysis of WUSCHEL-related homeobox transcription factor family reveals functional divergence among clades in the homeobox region. Dev Genes Evol, 2016, 226(4): 259-268. |
| [36] | Ji JB, Strable J, Shimizu R, Koenig D, Sinha N, Scanlon MJ. WOX4 promotes procambial development. Plant Physiol, 2010, 152(3): 1346-1356. |
| [37] | Hibara K, Karim MR, Takada S, Taoka K, Furutani M, Aida M, Tasaka M. Arabidopsis CUP-SHAPED COTYLEDON3 regulates postembryonic shoot meristem and organ boundary formation. Plant Cell, 2006, 18(11): 2946-2957. |
| [38] | Hasson A, Plessis A, Blein T, Adroher B, Grigg S, Tsiantis M, Boudaoud A, Damerval C, Laufs P. Evolution and diverse roles of the CUP-SHAPED COTYLEDON genes in Arabidopsis leaf development. Plant Cell, 2011, 23(1): 54-68. |
| [39] | Bresso EG, Chorostecki U, Rodriguez RE, Palatnik JF, Schommer C. Spatial control of gene expression by miR319-regulated TCP transcription factors in leaf development. Plant Physiol, 2018, 176(2): 1694-1708. |
| [40] | Song YH, Ito S, Imaizumi T. Flowering time regulation: photoperiod- and temperature-sensing in leaves. Trends Plant Sci, 2013, 18(10): 575-583. |
| [41] | Shen LS, Thong ZH, Gong XM, Shen Q, Gan YB, Yu H. The putative PRC 1 RING-finger protein AtRING1A regulates flowering through repressing MADS AFFECTING FLOWERING genes in Arabidopsis. Development, 2014, 141(6): 1303-1312. |
| [42] | Baesso B, Chiatante D, Terzaghi M, Zenga D, Nieminen K, Mahonen AP, Siligato R, Helariutta Y, Scippa GS, Montagnoli A.Transcription factors PRE3 and WOX11 are involved in the formation of new lateral roots from secondary growth taproot in A. thaliana. Plant Biol (Stuttg), 2018, 20(3): 426-432. |
| [43] | Hu X, Xu L. Transcription factors WOX11/12 directly activate WOX5/7 to promote root primordia initiation and organogenesis. Plant Physiol, 2016, 172(4): 2363-2373. |
| [44] | Kucukoglu M, Nilsson J, Zheng B, Chaabouni S, Nilsson O. WUSCHEL-RELATED HOMEOBOX4 (WOX4)-like genes regulate cambial cell division activity and seconddary growth in Populus trees. New Phytol, 2017, 215(2): 642-657. |
| [45] | Yasui Y, Ohmori Y, Takebayashi Y, Sakakibara H, Hirano HY. WUSCHEL-RELATED HOMEOBOX4 acts as a key regulator in early leaf development in rice. PLoS Genet, 2018, 14(4): e1007365. |
| [46] | Shimizu R, Ji JB, Kelsey E, Ohtsu K, Schnable PS, Scanlon MJ. Tissue specificity and evolution of meristematic WOX3 function. Plant Physiol, 2009, 149(2): 841-850. |
| [47] | Zhang ZJ, Runions A, Mentink RA, Kierzkowski D, Karady M, Hashemi B, Huijser P, Strauss S, Gan XC, Ljung K, Tsiantis M. A WOX/Auxin biosynthesis module controls growth to shape leaf form. Curr Biol, 2020, 30(24): 4857-4868.e6. |
| [48] | Wang FX, Shang GD, Wu LY, Xu ZG, Zhao XY, Wang JW. Chromatin accessibility dynamics and a hierarchical transcriptional regulatory network structure for plant somatic embryogenesis. Dev Cell, 2020, 54(6): 742-757.e8. |
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