WUSCHEL-related homeobox ( WOX) transcription factors: key regulators in combating abiotic stresses in plants

Abstract

The WUSCHEL-related homeobox ( WOX) transcription factors (TFs) belong to the homeodomain (HD) family. WOX TFs are involved in various regulatory pathways related to plant growth and development. In addition to their recognized role in various development processes, many reports suggest that they play a key role in abiotic stress perception in plants. However, their underlying molecular mechanisms have rarely been studied in horticultural crops. WOXs govern the transcription of the target genes through specific binding to the cis-regulatory elements present in their promoters. Additionally, they associate with other factors to form a specific pathway regulating numerous abiotic stress responses. Here, we review the recent advances in the multifaceted functions of WOXs in the complex, developmental, and abiotic stress-sensing networks, with particular emphasis on regulating the related genes and other TFs. In addition, we suggest that WOXs are essential components of the gene regulatory networks involved in the response of plants to abiotic stress tolerance and aim to provide a reference for future research.

Keywords

Abiotic stress / WOX / Transcription factors / Gene regulation / Tolerance

References

[1]	Akbulut SE, Okay A, Aksoy T, Aras ES, Büyük I. The genome-wide characterization of WOX gene family in Phaseolus vulgaris L. during salt stress. Physiol Mol Biol Plants. 2022;28:1297–309. https://doi.org/10.1007/s12298-022-01208-1.
[2]	Alvarez JM, Bueno N, Ca?as RA, Avila C, Cánovas FM, Ordás RJ. Analysis of the WUSCHEL-RELATED HOMEOBOX gene family in Pinus pinaster: new insights into the gene family evolution. Plant Physiol Bioch. 2018;123:304–18. https://doi.org/10.1016/j.plaphy.2017.12.031.
[3]	Arroyo-Herrera A, Ku Gonzalez A, Canche Moo R, Quiroz-Figueroa FR, Loyola-Vargas V, Rodriguez-Zapata L, et al. Expression of WUSCHEL in Coffea canephora causes ectopic morphogenesis and increases somatic embryogenesis. Plant Cell Tissue Organ Cult. 2008;94:171–80. https://doi.org/10.1007/s11240-008-9401-1.
[4]	Baesso B, Chiatante D, Terzaghi M, Zenga D, Nieminen K, Mahonen A, et al. Transcription factors PRE3 and WOX11 are involved in the formation of new lateral roots from secondary growth taproot in A. thaliana. Plant Biol. 2018;20:426–32. https://doi.org/10.1111/plb.12711.
[5]	Banerjee A, Roychoudhury A. Abscisic-acid-dependent basic leucine zipper (bZIP) transcription factors in plant abiotic stress. Protoplasma. 2017;254:3–16. https://doi.org/10.1007/s00709-015-0920-4.
[6]	Breuninger H, Rikirsch E, Hermann M, Ueda M, Laux T. Differential expression of WOX genes mediates apical-basal axis formation in the Arabidopsis embryo. Dev Cell. 2008;14:867–76. https://doi.org/10.1016/j.devcel.2008.03.008.
[7]	Bürglin TR, Affolter M. Homeodomain proteins: an update. Chromosoma. 2016;125:497–521. https://doi.org/10.1007/s00412-015-0543-8.
[8]	Cao Y, Han Y, Meng D, Li G, Li D, Abdullah M, et al. 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. 2017;8:78. https://doi.org/10.3389/fgene.2017.00078.
[9]	Chang Y, Song X, Li M, Zhang Q, Zhang P, Lei X, et al. Characterization of walnut JrWOX11 and its overexpression provide insights into adventitious root formation and development and abiotic stress tolerance. Front Plant Sci. 2022;13(13):951737. https://doi.org/10.3389/fpls.2022.951737.
[10]	Chang Y, Song X, Zhang Q, Liu H, Bai Y, Lei X, et al. Genome-wide identification of WOX gene family and expression analysis during rejuvenational rhizogenesis in walnut (Juglans regia L.). Forests. 2019;11:16. https://doi.org/10.3390/f11010016.
[11]	Chaudhary R, Singh S, Kaur K, Tiwari S. Genome-wide identification and expression profiling of WUSCHEL-related homeobox (WOX) genes confer their roles in somatic embryogenesis, growth and abiotic stresses in banana. 3 Biotech. 2022;12:321. https://doi.org/10.1007/s11738-015-1964-y.
[12]	Chen S, Yang H, Zhang Y, Chen C, Ren T, et al. Global Analysis of the WOX Transcription Factor Family in Akebia trifoliata. 2023. https://doi.org/10.20944/preprints202311.0138.v1.
[13]	Cheng S, Zhou D-X, Zhao Y. WUSCHEL-related homeobox gene WOX11 increases rice drought resistance by controlling root hair formation and root system development. Plant Signal Behav. 2016;11:1130198. https://doi.org/10.1080/15592324.2015.1130198.
[14]	da Silva MB, Dornelas MC, Carrara S, Gioppato HA. Identification and characterization of the WUSCHEL-related homeobox (WOX) genes family in Passiflora organensis. Rev Trab Inic Cient. 2018; 26. https://doi.org/10.20396/revpibic262018981.
[15]	Daude MM, Dos Santos Silva TW, Freitas NC, Ságio SA, Paiva LV, Barreto HG. Transcriptional analysis of WUSCHEL-related HOMEOBOX (WOX) genes in Coffea arabica L. Biologia. 2020;75:1483–95. https://doi.org/10.2478/s11756-020-00460-8.
[16]	Denis E, Kbiri N, Mary V, Claisse G, Conde e Silva N, Kreis M, et al. WOX 14 promotes bioactive gibberellin synthesis and vascular cell differentiation in Arabidopsis. Plant J. 2017;90:560–72. https://doi.org/10.1111/tpj.13513.
[17]	Devireddy AR, Zandalinas SI, Fichman Y, Mittler R. Integration of reactive oxygen species and hormone signaling during abiotic stress. Plant J. 2021;105:459–76. https://doi.org/10.1111/tpj.15010.
[18]	Dong H, Zheng Q, Zhou Y, Zhou Y, Bao Z, Lan Q, et al. MdWOX4–2 modulated MdLBD41 functioning in adventitious shoot of apple (Malus domestica). Plant Physiol Bioch. 2022;186:11–8. https://doi.org/10.1016/j.plaphy.2022.06.026.
[19]	Duan X, Zhang W, Huang J, Hao L, Wang S, Wang A, et al. PbWoxT1 mRNA from pear (Pyrus betulaefolia) undergoes long-distance transport assisted by a polypyrimidine tract binding protein. New Phytol. 2016;210:511–24. https://doi.org/10.1111/nph.13793.
[20]	Estravis-Barcala M, Mattera MG, Soliani C, Bellora N, Opgenoorth L, Heer K, et al. Molecular bases of responses to abiotic stress in trees. J Exp Bot. 2020;71:3765–79. https://doi.org/10.1093/jxb/erz532.
[21]	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;140:2224–34. https://doi.org/10.1242/dev.091314.
[22]	Fang Y, Xie K, Xiong L. Conserved miR164-targeted NAC genes negatively regulate drought resistance in rice. J Exp Bot. 2014;65:2119–35. https://doi.org/10.1093/jxb/eru072.
[23]	FAO I. The state of food insecurity in the world. 2015;1-62.
[24]	Feng C, Zou S, Gao P, Wang Z. In silico identification, characterization expression profile of WUSCHEL-Related Homeobox (WOX) gene family in two species of kiwifruit. PeerJ. 2021;9:e12348. https://doi.org/10.7717/peerj.12348.
[25]	Francini A, Sebastiani L. Abiotic stress effects on performance of horticultural crops. Horticulturae. 2019;5:67. https://doi.org/10.3390/horticulturae5040067.
[26]	Galibina NA, Moshchenskaya YL, Tarelkina TV, Nikerova KM, Korzhenevskii MA, Serkova AA, et al. Identification and Expression Profile of CLE41/44-PXY-WOX Genes in Adult Trees Pinus sylvestris L. Trunk Tissues during Cambial Activity. Plants. 2023;12:835. https://doi.org/10.3390/plants12040835.
[27]	Gambino G, Minuto M, Boccacci P, Perrone I, Vallania R, Gribaudo I. Characterization of expression dynamics of WOX homeodomain transcription factors during somatic embryogenesis in Vitis vinifera. J Exp Bot. 2011;62:1089–101. https://doi.org/10.1093/jxb/erq349.
[28]	Gao B, Wen C, Fan L, Kou Y, Ma N, Zhao L. A Rosa canina WUSCHEL-related homeobox gene, RcWOX1, is involved in auxin-induced rhizoid formation. Plant Mol Biol. 2014;86:671–9. https://doi.org/10.1007/s11103-014-0255-0.
[29]	Gao Y, Li K, Yin Y, Li Y, Zong Y, Liu X, et al. Genome-wide Analysis of the WUSCHEL-related Homeobox Gene Family and Functional Characterization of VcWOX4b Regarding the Inhibition of Adventitious Root Formation in Blueberry (Vaccinium Spp.). Res Seq. 2021. https://doi.org/10.21203/rs.3.rs-849933/v1
[30]	Gu R, Song X, Liu X, Yan L, Zhou Z, Zhang X. Genome-wide analysis of CsWOX transcription factor gene family in cucumber (Cucumis sativus L.). Sci Rep. 2020;10:6216. https://doi.org/10.1038/s41598-020-63197-z.
[31]	Guan C, Wu B, Yu T, Wang Q, Krogan NT, Liu X, et al. Spatial auxin signaling controls leaf flattening in Arabidopsis. Curr Biol. 2017;27:2940–50. https://doi.org/10.1016/j.cub.2017.08.042.
[32]	Haecker A, Gro?-Hardt R, Geiges B, Sarkar A, Breuninger H, Herrmann M, et al. Expression dynamics of WOX genes mark cell fate decisions during early embryonic patterning in Arabidopsis thaliana. Development. 2004;131:657–68. https://doi.org/10.1242/dev.00963.
[33]	He G, Cao Y, Wang J, Song M, Bi M, Tang Y, et al. WUSCHEL-related homeobox genes cooperate with cytokinin to promote bulbil formation in Lilium lancifolium. Plant Physiol. 2022;190:387–402. https://doi.org/10.1093/plphys/kiac259.
[34]	Hu Q, Dong J, Ying J, Wang Y, Xu L, Ma Y, et al. Functional analysis of RsWUSb with Agrobacterium-mediated in planta transformation in radish (Raphanus sativus L.). Sci Horti. 2024;323:112504. https://doi.org/10.1016/j.scienta.2023.112504.
[35]	Jain M, Tyagi AK, Khurana JP. Genome-wide identification, classification, evolutionary expansion and expression analyses of homeobox genes in rice. FEBS J. 2008;275:2845–61. https://doi.org/10.1111/j.1742-4658.2008.06424.x.
[36]	Jiang S, An H, Luo J, Wang X, Shi C, Xu F. Comparative analysis of transcriptomes to identify genes associated with fruit size in the early stage of fruit development in Pyrus pyrifolia. Int J Mol Sci. 2018;19:2342. https://doi.org/10.1093/jxb/erx153.
[37]	Jiang W, Zhou S, Zhang Q, Song H, Zhou DX, Zhao Y. Transcriptional regulatory network of WOX11 is involved in the control of crown root development, cytokinin signals, and redox in rice. J Exp Bot. 2017;68:2787–98. https://doi.org/10.1093/jxb/erx153.
[38]	Khan FS, Zeng RF, Gan ZM, Zhang JZ, Hu CG. Genome-wide identification and expression profiling of the WOX gene family in Citrus sinensis and functional analysis of a CsWUS member. Int J Mol Sci. 2021;22:4919. https://doi.org/10.3390/ijms22094919.
[39]	Khan FS, Goher F, Paulsmeyer MN, Hu CG, Zhang JZ. Calcium (Ca2+) sensors and MYC2 are crucial players during jasmonates-mediated abiotic stress tolerance in plants. Plant Biol. 2023a;25:1025–34. https://doi.org/10.1111/plb.13560.
[40]	Khan FS, Li Z, Shi P, Zhang D, Htwe YM, Yu Q, et al. Transcriptional regulations and hormonal signaling during somatic embryogenesis in the coconut tree: an insight. Forests. 2023b;14:1800. https://doi.org/10.3390/f14091800.
[41]	Khan FS, Gan ZM, Li EQ, Ren MK, Hu CG, Zhang JZ. Transcriptomic and physiological analysis reveals interplay between salicylic acid and drought stress in citrus tree floral initiation. Planta. 2022a;255:1–22. https://doi.org/10.1007/s00425-021-03801-2.
[42]	Khan FS, Goher F, Zhang D, Shi P, Li Z, Htwe YM, et al. Is CRISPR/Cas9 a way forward to fast-track genetic improvement in commercial palms? Prospects and limits. Front Plant Sci. 2022b;13 https://doi.org/10.3389/fpls.2022.1042828
[43]	Klimaszewska K, Overton C, Stewart D, Rutledge RG. Initiation of somatic embryos and regeneration of plants from primordial shoots of 10-year-old somatic white spruce and expression profiles of 11 genes followed during the tissue culture process. Planta. 2011;233:635–47. https://doi.org/10.1007/s00425-010-1325-4.
[44]	Kong D, Hao Y, Cui H. The WUSCHEL related homeobox protein WOX7 regulates the sugar response of lateral root development in Arabidopsis thaliana. Mol Plant. 2016;9:261–70. https://doi.org/10.1016/j.molp.2015.11.006.
[45]	Kumar V, Kumar Srivastava A, Wani SH, Shriram V, Penna S. Transcriptional and post-transcriptional mechanisms regulating salt tolerance in plants. Physiol Plant. 2021;173:1291–4. https://doi.org/10.1111/ppl.13592.
[46]	Laux T, Mayer KF, Berger J, Jürgens G. The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. Development. 1996;122:87–96. https://doi.org/10.1242/dev.122.1.87.
[47]	Leonardo B, Emanuela T, Letizia MM, Antonella M, Marco M, Fabrizio A, et al. Cadmium affects cell niches maintenance in Arabidopsis thaliana post-embryonic shoot and root apical meristem by altering the expression of WUS/WOX homolog genes and cytokinin accumulation. Plant Physiol Biochem. 2021;167:785–94. https://doi.org/10.1016/j.plaphy.2021.09.014.
[48]	Li Y, Zhu Y, Yao J, Zhang S, Wang L, Guo C, et al. Genome-wide identification and expression analyses of the homeobox transcription factor family during ovule development in seedless and seeded grapes. Sci Rep. 2017;7:12638. https://doi.org/10.1038/s41598-017-12988-y.
[49]	Li Y, Zhang D, An N, Fan S, Zuo X, Zhang X, et al. Transcriptomic analysis reveals the regulatory module of apple (Malus× domestica) floral transition in response to 6-BA. BMC Plant Biol. 2019;19:93. https://doi.org/10.1186/s12870-019-1695-0.
[50]	Li Z, Liu D, Xia Y, Li Z, Jing D, Du J, et al. Identification of the WUSCHEL-related homeobox (WOX) gene family, and interaction and functional analysis of TaWOX9 and TaWUS in wheat. Int J Mol Sci. 2020;21:1581. https://doi.org/10.3390/ijms21051581.
[51]	Li Y, Jin C, Liu Y, Wang L, Li F, Wang B, et al. Global Analysis of the WOX Transcription Factor Gene Family in Populus× xiaohei TS Hwang et Liang Reveals Their Stress?Responsive Patterns. Forests. 2022;13:122. https://doi.org/10.3390/f13010122.
[52]	Li WX, Oono Y, Zhu J, He XJ, Wu JM, Iida K, et al. The Arabidopsis NFYA5 transcription factor is regulated transcriptionally and posttranscriptionally to promote drought resistance. Plant Cell. 2008;20:2238–51. https://doi.org/10.1105/tpc.108.059444.
[53]	Li H, Li X, Sun M, Chen S, Ma H, Lin J, et al. Molecular characterization and gene expression analysis of tomato WOX transcription factor family under abiotic stress and phytohormone treatment. J Plant Biochem Biotechnol. 2021;30:973–86. https://doi.org/10.1007/s13562-021-00723-8.
[54]	Li C, He Z, Liang G, Yang N, Cai P, Liang Y, et al. Genome-wide identification and evolutionary analysis of WOX gene family in cucurbit crops. Horti. Environ. Biotechnol. 2023;1–14. https://doi.org/10.1007/s13580-023-00550-x
[55]	Liao Q, Cheng X, Lan T, Guo X, Su Z, An X, et al. OsSPL10 controls trichome development by interacting with OsWOX3B at both transcription and protein levels in rice (Oryza sativa L.). Crop J. 2023. https://doi.org/10.1016/j.cj.2023.05.012.
[56]	Lin H, Niu L, McHale NA, Ohme-Takagi M, Mysore KS, et al. Evolutionarily conserved repressive activity of WOX proteins mediates leaf blade outgrowth and floral organ development in plants. Proceed Nat Acad Sci. 2013;110(1):366–71. https://doi.org/10.1073/pnas.1215376110.
[57]	Liu D, Chen X, Liu J, Ye J, Guo Z. The rice ERF transcription factor OsERF922 negatively regulates resistance to Magnaporthe oryzae and salt tolerance. J Exp Bot. 2012;63:3899–911. https://doi.org/10.1093/jxb/ers079.
[58]	Liu J, Sheng L, Xu Y, Li J, Yang Z, Huang H, et al. WOX11 and 12 are involved in the first-step cell fate transition during de novo root organogenesis in Arabidopsis. Plant Cell. 2014;26:1081–93. https://doi.org/10.1105/tpc.114.122887.
[59]	Liu R, Wen SS, Sun TT, Wang R, Zuo WT, Yang T, et al. PagWOX11/12a positively regulates the PagSAUR36 gene that enhances adventitious root development in poplar. J Exp Bot. 2022;73:7298–311. https://doi.org/10.1093/jxb/erac345.
[60]	Lu Y, Liu Z, Lyu M, Yuan Y, Wu B. Characterization of JsWOX1 and JsWOX4 during callus and root induction in the shrub species Jasminum sambac. Plants. 2019;8:79. https://doi.org/10.3390/plants8040079.
[61]	Lv J, Feng Y, Jiang L, Zhang G, Wu T, Zhang X, et al. Genome-wide identification of WOX family members in nine Rosaceae species and a functional analysis of MdWOX13-1 in drought resistance. Plant Sci. 2023;328:111564. https://doi.org/10.1016/j.plantsci.2022.111564.
[62]	Ma S, Bohnert HJ. Integration of Arabidopsis thaliana stress-related transcript profiles, promoter structures, and cell-specific expression. Genom Biol. 2007;8:R49. https://doi.org/10.1186/gb-2007-8-4-r49.
[63]	Mao J, Ma D, Niu C, Ma X, Li K, Tahir MM, et al. Transcriptome analysis reveals the regulatory mechanism by which MdWOX11 suppresses adventitious shoot formation in apple. Hort Res. 2022;9:uhac080. https://doi.org/10.1093/hr/uhac080.
[64]	Mao J, Niu C, Li K, Fan L, Liu Z, Li S, et al. Cytokinin-responsive MdTCP17 interacts with MdWOX11 to repress adventitious root primordium formation in apple rootstocks. Plant Cell. 2023;35:1202–21. https://doi.org/10.1093/plcell/koac369.
[65]	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;95:805–15. https://doi.org/10.1016/S0092-8674(00)81703-1.
[66]	Minh-Thu PT, Kim JS, Chae S, Jun KM, Lee GS, Kim DE, et al. A WUSCHEL homeobox transcription factor, OsWOX13, enhances drought tolerance and triggers early flowering in rice. Mol Cells. 2018;41:781–98. https://doi.org/10.14348/molcells.2018.0203.
[67]	Mukherjee K, Brocchieri L, Bürglin TR. A comprehensive classification and evolutionary analysis of plant homeobox genes. Mol Biol. 2009;26:2775–94. https://doi.org/10.1093/molbev/msp201.
[68]	Nakata MT, Tameshige T, Takahara M, Mitsuda N, Okada K. The functional balance between the WUSCHEL-RELATED HOMEOBOX1 gene and the phytohormone auxin is a key factor for cell proliferation in Arabidopsis seedlings. Plant Biotechnol. 2018;35:141–54. https://doi.org/10.5511/plantbiotechnology.18.0427a.
[69]	Niu H, Liu X, Tong C, Wang H, Li S, Lu L, et al. The WUSCHEL-related homeobox1 gene of cucumber regulates reproductive organ development. J Exp Bot. 2018;69:5373–87. https://doi.org/10.1093/jxb/ery329.
[70]	Park SO, Zheng Z, Oppenheimer DG, Hauser BA. The PRETTY FEW SEEDS2 gene encodes an Arabidopsis homeodomain protein that regulates ovule development. Development. 2005;132:841–9. https://doi.org/10.1242/dev.01654.
[71]	Peng X, Wu Q, Teng L, Tang F, Pi Z, Shen S. Transcriptional regulation of the paper mulberry under cold stress as revealed by a comprehensive analysis of transcription factors. BMC Plant Biol. 2015;15:108. https://doi.org/10.1186/s12870-015-0489-2.
[72]	Rahman ZU, Azam SM, Liu Y, Yan C, Ali H, Zhao L, et al. Expression profiles of Wuschel-related homeobox gene family in pineapple (Ananas comosus L). Trop Plant Biol. 2017;10:204–15. https://doi.org/10.1007/s12042-017-9192-9.
[73]	Riccucci E, Vanni C, Vangelisti A, Fambrini M, Giordani T, Cavallini A, Mascagni F, Pugliesi C. Genome-Wide Analysis of WOX Multigene Family in Sunflower (Helianthus annuus L.). Int J Mol Sci. 2023;24:3352. https://doi.org/10.3390/ijms24043352.
[74]	Romera-Branchat M, Ripoll JJ, Yanofsky MF, Pelaz S. The WOX 13 homeobox gene promotes replum formation in the Arabidopsis thaliana fruit. Plant J. 2013;73:37–49. https://doi.org/10.1111/tpj.12010.
[75]	Ru D, JIN H, Zeng W, Avihai P, XU H, ZHANG W, et al. Cloning and characterization of WOX4 Gene from Vitis vinifera L. involved in stem cell regulation. Agri Sci China. 2011;10:1861–71. https://doi.org/10.1016/S1671-2927(11)60186-7.
[76]	Saijo Y, Loo EP. Plant immunity in signal integration between biotic and abiotic stress responses. New Phytol. 2020;225:87–104. https://doi.org/10.1111/nph.15989.
[77]	Sarkar AK, Luijten M, Miyashima S, Lenhard M, Hashimoto T, Nakajima K, et al. Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature. 2007;446:811–4. https://doi.org/10.1038/nature05703.
[78]	Song Y, Jin L, Wang X. Cadmium absorption and transportation pathways in plants. Int J Phyto. 2017;19:133–41. https://doi.org/10.1080/15226514.2016.1207598.
[79]	Sun R, Zhang X, Ma D, Liu C. Identification and Evolutionary Analysis of Cotton (Gossypium hirsutum) WOX Family Genes and Their Potential Function in Somatic Embryogenesis. Int J Mol Sci. 2023;24(13):11077. https://doi.org/10.3390/ijms241311077.
[80]	Sun W, Gao D, Xiong Y, Tang X, Xiao X, Wang C, et al. Hairy leaf 6, an AP2/ERF transcription factor, interacts with OsWOX3B and regulates trichome formation in rice. Mol Plant. 2017;10:1417–33. https://doi.org/10.1016/j.molp.2017.09.015.
[81]	Szemenyei H, Hannon M, Long JA. TOPLESS mediates auxin-dependent transcriptional repression during Arabidopsis embryogenesis. Science. 2008;319:1384–6. https://doi.org/10.1126/science.1151461.
[82]	Tahir MM, Tong L, Fan L, Liu Z, Li S, Zhang X, et al. Insights into the complicated networks contribute to adventitious rooting in transgenic MdWOX11 apple microshoots under nitrate treatments. Plant Cell Env. 2022;45:3134–56. https://doi.org/10.1111/pce.14409.
[83]	Tang F, Chen N, Zhao M, Wang Y, He R, Peng X, et al. Identification and functional divergence analysis of WOX gene family in paper mulberry. Int J Mol Sci. 2017;18:1782. https://doi.org/10.3390/ijms18081782.
[84]	Tang Y, Li H, Guan Y, Li S, Xun C, Dong Y, et al. Genome-wide identification of the physic nut WUSCHEL-related homeobox gene family and functional analysis of the abiotic stress responsive gene JcWOX5. Front Genet. 2020;11:670. https://doi.org/10.3389/fgene.2020.00670.
[85]	Tang L, He Y, Liu B, Xu Y, Zhao G. Genome-Wide Identification and Characterization Analysis of WUSCHEL-Related Homeobox Family in Melon (Cucumis melo L.). Int J Mol Sci. 2023;24:12326. https://doi.org/10.3390/ijms241512326.
[86]	Thorne SJ, Hartley SE, Maathuis FJ. Is silicon a panacea for alleviating drought and salt stress in crops? Front Plant Sci. 2020;11:1221. https://doi.org/10.3389/fpls.2020.01221.
[87]	Tiwari SB, Hagen G, Guilfoyle T. The roles of auxin response factor domains in auxin-responsive transcription. Plant Cell. 2003;15:533–43. https://doi.org/10.1105/tpc.008417.
[88]	Tvorogova VE, Krasnoperova EY, Potsenkovskaia EA, Kudriashov AA, Dodueva IE, Lutova LA. What does the WOX say? Review of regulators, targets, partners. Mol Biol. 2021;55:311–37. https://doi.org/10.1134/S002689332102031X.
[89]	Ulmasov T, Hagen G, Guilfoyle TJ. ARF1. a transcription factor that binds to auxin response elements. Science. 1997;276:1865–8. https://doi.org/10.1126/science.276.5320.1865.
[90]	van der Graaff E, Laux T, Rensing SA. The WUS homeobox-containing (WOX) protein family. Genom Biol. 2009;10:248. https://doi.org/10.1186/gb-2009-10-12-248.
[91]	Vandenbussche M, Horstman A, Zethof J, Koes R, Rijpkema AS, Gerats T. Differential recruitment of WOX transcription factors for lateral development and organ fusion in Petunia and Arabidopsis. Plant Cell. 2009;21:2269–83. https://doi.org/10.1105/tpc.109.065862.
[92]	Vandenbussche M. The role of WOX1 genes in blade development and beyond. J Exp Bot. 2021;72:1514–6. https://doi.org/10.1093/jxb/eraa599.
[93]	Wang Q, Zhu Z. Light signaling-mediated growth plasticity in Arabidopsis grown under high-temperature conditions. Stress Biol. 2022;2:53. https://doi.org/10.1007/s44154-022-00075-w.
[94]	Wang H, Wang H, Shao H, Tang X. Recent advances in utilizing transcription factors to improve plant abiotic stress tolerance by transgenic technology. Front Plant Sci. 2016;7:67. https://doi.org/10.3389/fpls.2016.00067.
[95]	Wang J, Tian C, Zhang C, Shi B, Cao X, Zhang T-Q, et al. Cytokinin signaling activates WUSCHEL expression during axillary meristem initiation. Plant Cell. 2017;29:1373–87. https://doi.org/10.1093/jxb/erz490.
[96]	Wang P, Guo Y, Chen X, Zheng Y, Sun Y, Yang J, et al. Genome-wide identification of WOX genes and their expression patterns under different hormone and abiotic stress treatments in tea plant (Camellia sinensis). Trees. 2019;33:1129–42. https://doi.org/10.1007/s00468-019-01847-0.
[97]	Wang LQ, Li Z, Wen SS, Wang JN, Zhao ST, Lu MZ. WUSCHEL-related homeobox gene PagWOX11/12a responds to drought stress by enhancing root elongation and biomass growth in poplar. J Exp Bot. 2020;71:1503–13. https://doi.org/10.1093/jxb/erz490.
[98]	Wang LQ, Wen SS, Wang R, Wang C, Gao B, Lu MZ. PagWOX11/12a activates PagCYP736A12 gene that facilitates salt toleran4ce in poplar. Plant Biotechnol J. 2021;19:2249–60. https://doi.org/10.1111/pbi.13653.
[99]	Willoughby AC, Nimchuk ZL. WOX going on: CLE peptides in plant development. Curr Opin Plant Biol. 2021;63:102056. https://doi.org/10.1016/j.pbi.2021.102056.
[100]	Wu H, Lv H, Li L, Liu J, Mu S, Li X, et al. Genome-wide analysis of the AP2/ERF transcription factors family and the expression patterns of DREB genes in Moso Bamboo (Phyllostachys edulis). PLoS ONE. 2015;10:e0126657. https://doi.org/10.1371/journal.pone.0126657.
[101]	Wu X, Chory J, Weigel D. Combinations of WOX activities regulate tissue proliferation during Arabidopsis embryonic development. Dev Biol. 2007;309:306–16. https://doi.org/10.1016/j.ydbio.2007.07.019.
[102]	Xu X, Lou Y, Yang K, Shan X, Zhu C, Gao Z. Identification of homeobox genes associated with lignification and their expression patterns in bamboo shoots. Biomolecules. 2019;9:862. https://doi.org/10.3390/biom9120862.
[103]	Xu X, Che Q, Cheng C, Yuan Y, Wang Y. Genome-wide identification of WOX gene family in apple and a functional analysis of MdWOX4b during adventitious root formation. J Integrat Agri. 2022;21:1332–45. https://doi.org/10.1016/S2095-3119(21)63768-1.
[104]	Xu Q, Wang Y, Yue Y, Chen Z, Zhou D-X, Zhao Y. Transcription factor WOX11 regulates protein translation via ribosome protein acetylation in rice roots. Plant Physiol. 2023;191:2224–8. https://doi.org/10.1093/plphys/kiad025.
[105]	Yang X, He K, Chi X, Chai G, Wang Y, Jia C, et al. Miscanthus NAC transcription factor MlNAC12 positively mediates abiotic stress tolerance in transgenic Arabidopsis. Plant Sci. 2018;277:229–41. https://doi.org/10.1016/j.plantsci.2018.09.013.
[106]	Yang X, Zhao X, Miao Y, Wang D, Zhang Z, Liu Y. Genome-Wide Identification and Expression Profile Analysis of the WUSCHEL-Related Homeobox (WOX) Genes in Woodland Strawberry (Fragaria vesca). Horticulturae. 2022;8:1043. https://doi.org/10.3390/horticulturae8111043.
[107]	Yang W, Xu C, Han J, Zhang X, Song J, Jia H, et al. Genome-wide identification and characterization of the WOX gene family in Brassica juncea. Chin J Biotechnol. 2023;39:537–51.
[108]	Yasui Y, Ohmori Y, Takebayashi Y, Sakakibara H, Hirano H-Y. WUSCHEL-RELATED HOMEOBOX4 acts as a key regulator in early leaf development in rice. PLoS Gen. 2018;14:e1007365. https://doi.org/10.1371/journal.pgen.1007365.
[109]	Youngstrom CE, Irish EE, Cheng C-L. The crucial role of Ceratopteris richardii in understanding the evolution of the WOX gene family. In: Ferns: Biotechnology, Propagation, Medicinal Uses and Environmental Regulation. 2022. Springer, pp 135–147. https://doi.org/10.1007/978-981-16-6170-9_6
[110]	Yu Y, Yang M, Liu X, Xia Y, Hu R, Xia Q, et al. Genome-wide analysis of the WOX gene family and the role of EjWUSa in regulating flowering in loquat (Eriobotrya japonica). Front Plant Sci. 2022;13:1024515. https://doi.org/10.3389/fpls.2022.1024515.
[111]	Zhang H, Liu S, Ren T, Niu M, Liu X, Liu C, et al. Crucial Abiotic Stress Regulatory Network of NF-Y Transcription Factor in Plants. Int J Mol Sci. 2023;24:4426. https://doi.org/10.3390/ijms24054426.
[112]	Zhang X, Zong J, Liu J, Yin J, Zhang D. Genome-wide analysis of WOX gene family in rice, sorghum, maize, Arabidopsis and poplar. J Integrat Plant Biol. 2010;52:1016–26. https://doi.org/10.1111/j.1744-7909.2010.00982.x.
[113]	Zhang F, Rossignol P, Huang T, Wang Y, May A, Dupont C, et al. Reprogramming of stem cell activity to convert thorns into branches. Curr Biol. 2020;30:2951–61. https://doi.org/10.1016/j.cub.2020.05.068.
[114]	Zhang M, Chen X, Lou X, Zhang Y, Han X, Yang Q, et al. Identification of WUSCHEL-related homeobox (WOX) gene family members and determination of their expression profiles during somatic embryogenesis in Phoebe bournei. Forest Res. 2023;3:5. https://doi.org/10.48130/FR-2023-0005
[115]	Zhao Y, Cheng S, Song Y, Huang Y, Zhou S, Liu X, et al. The interaction between rice ERF3 and WOX11 promotes crown root development by regulating gene expression involved in cytokinin signaling. Plant Cell. 2015;27:2469–83. https://doi.org/10.1105/tpc.15.00227.
[116]	Zhu J, Shi H, Lee B, Damsz B, Cheng S, Stirm V, et al. An Arabidopsis homeodomain transcription factor gene, HOS9, mediates cold tolerance through a CBF-independent pathway. Proceed National Academy Sci. 2004;101:9873–8. https://doi.org/10.1073/pnas.0403166101.
[117]	Zubo YO, Blakley IC, Yamburenko MV, Worthen JM, Street IH, Franco-Zorrillaet JM, et al. Cytokinin induces genome-wide binding of the type-B response regulator ARR10 to regulate growth and development in Arabidopsis. Proceed National Academy Sci. 2017;114:E5995–6004. https://doi.org/10.1073/pnas.1620749114.

Funding

National Major Research and Development Plan(2022YPD1200503); Innovative Research Group Project of the National Natural Science Foundation of China(31872045)