The nuclear hormone receptor family transcription factor Dd-NHR-1 is required for embryonic development in Ditylenchus destructor

Ziwen Cong , Guoqiang Huang , Shitian Huo , Xueling Liao , Si Gao , Jinshui Zheng , Ming Sun , Donghai Peng

New Plant Protection ›› 2025, Vol. 2 ›› Issue (2) : e70009

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New Plant Protection ›› 2025, Vol. 2 ›› Issue (2) :e70009 DOI: 10.1002/npp2.70009
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The nuclear hormone receptor family transcription factor Dd-NHR-1 is required for embryonic development in Ditylenchus destructor

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Abstract

Plant-parasitic nematodes can diminish global food production by approximately 12.3%, leading to annual economic losses of nearly $173 billion. Unfortunately, implementing effective preventive and control strategies for plant-parasitic nematodes remains challenging. In this study, we identified and characterized a transcription factor, Dd-NHR-1, which belongs to the nuclear hormone receptor (NHR) family. The NHR domain and zinc finger domain are both present in the structure of Dd-NHR-1. Phylogenetic analysis reveals that the Dd-nhr-1 gene exhibits the closest evolutionary distance to NHRs of other nematodes. Our findings demonstrate that the colonization numbers of Ditylenchus destructor in storage roots treated with Dd-nhr-1 dsRNA are reduced by 65.70%. Additionally, silencing the expression of the Dd-nhr-1 gene in eggs resulted in a 66.83% decrease in the egg hatching rate. RT-qPCR data indicate that Dd-nhr-1 is highly expressed in the second-stage juveniles and eggs, whereas in situ hybridization reveals its localization in the anterior region of the nematodes. The ChIP-seq experiment confirmed its role as an upstream transcription factor, regulating numerous target genes and playing a crucial role in embryonic development. In summary, Dd-NHR-1 is a critical regulatory factor in embryonic development and serves as a potential target for D. destructor prevention with significant economic importance.

Keywords

Ditylenchus destructor / embryonic development / infectivity / nuclear hormone receptor / plant-parasitic nematode

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Ziwen Cong, Guoqiang Huang, Shitian Huo, Xueling Liao, Si Gao, Jinshui Zheng, Ming Sun, Donghai Peng. The nuclear hormone receptor family transcription factor Dd-NHR-1 is required for embryonic development in Ditylenchus destructor. New Plant Protection, 2025, 2(2): e70009 DOI:10.1002/npp2.70009

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References

[1]

Qiao, Y., Yu, Q., Badiss, A., Zaidi, M. A., Ekaterina, P., Hu, Y., & Ye, W. (2016). Paraphyletic genus Ditylenchus filipjev (Nematoda, tylenchida), corresponding to the D. triformis-group and the D. dipsaci-group scheme. ZooKeys, 568, 1-12. https://doi.org/10.3897/zookeys.568.5965

[2]

Song, W., Dai, M., Shi, Q., Liang, C., Duan, F., & Zhao, H. (2023). Diagnosis and characterization of Ditylenchus destructor isolated from Mazus japonicus in China. Life (Basel), 13(8), 1758. https://doi.org/10.3390/life13081758

[3]

Xu, Z., Zhao, Y. Q., Yang, D. J., Sun, H. J., Zhang, C. L., & Xie, Y. P. (2015). Attractant and repellent effects of sweet potato root exudates on the potato rot nematode, Ditylenchus destructor. Nematology, 17(1), 117-124. https://doi.org/10.1163/15685411-00002856

[4]

Pan, F., Li, F., Mao, Y., Liu, D., Chen, A., Zhao, D., & Hu, Y. (2021). First detection of Ditylenchus destructor parasitizing maize in Northeast China. Life (Basel), 11(12), 1303. https://doi.org/10.3390/life11121303

[5]

Ni, C., Zhang, S., Li, H., Liu, Y., Li, W., Xu, X., & Xu, Z. (2020). First report of potato rot nematode, Ditylenchus destructor Thorne, 1945 infecting Codonopsis pilosula in Gansu Province, China. Journal of Nematology, 52(1), e2020-e2087. https://doi.org/10.21307/jofnem-2020-087

[6]

Eves-van den Akker, S., Stojilković, B., & Gheysen, G. (2021). Recent applications of biotechnological approaches to elucidate the biology of plant-nematode interactions. Current Opinion in Biotechnology, 70, 122-130. https://doi.org/10.1016/j.copbio.2021.03.008

[7]

Xia, Y., Xie, S., Ma, X., Wu, H., Wang, X., & Gao, X. (2011). The purL gene of Bacillus subtilis is associated with nematicidal activity. FEMS Microbiology Letters, 322(2), 99-107. https://doi.org/10.1111/j.1574-6968.2011.02336.x

[8]

Gao, D. L., Yu, W. L., Miao, J. Q., & Liu, F. (2011). Toxicity and bioactivity of several alternative nematocides against Ditylenchus destructor. Yingyong Shengtai Xuebao, 22(11), 3026-3032.

[9]

Zasada, I. A., Halbrendt, J. M., Kokalis-Burelle, N., LaMondia, J., McKenry, M. V., & Noling, J. W. (2010). Managing nematodes without methyl bromide. Annual Review of Phytopathology, 48(1), 311-328. https://doi.org/10.1146/annurev-phyto-073009-114425

[10]

Da Rocha, M., Bournaud, C., Dazenière, J., Thorpe, P., Bailly-Bechet, M., Pellegrin, C., Péré, A., Grynberg, P., Perfus-Barbeoch, L., Eves-van den Akker, S., & Danchin, E. G. J. (2021). Genome expression dynamics reveal the parasitism regulatory landscape of the root-knot nematode Meloidogyne incognita and a promoter motif associated with effector genes. Genes, 12(5), 771. https://doi.org/10.3390/genes12050771

[11]

Montarry, J., Mimee, B., Danchin, E. G. J., Koutsovoulos, G. D., Ste-Croix, D. T., & Grenier, E. (2021). Recent advances in population genomics of plant-parasitic nematodes. Phytopathology, 111(1), 40-48. https://doi.org/10.1094/PHYTO-09-20-0418-RVW

[12]

Banerjee, S., Banerjee, A., Gill, S. S., Gupta, O. P., Dahuja, A., Jain, P. K., & Sirohi, A. (2017). RNA interference: A novel source of resistance to combat plant parasitic nematodes. Frontiers in Plant Science, 8, 834. https://doi.org/10.3389/fpls.2017.00834

[13]

Dinh, P. T., Zhang, L., Mojtahedi, H., Brown, C. R., & Elling, A. A. (2015). Broad Meloidogyne resistance in potato based on RNA interference of effector gene 16D10. Journal of Nematology, 47(1), 71-78.

[14]

Moreira, V. J. V., Lourenço-Tessutti, I. T., Basso, M. F., Lisei-de-Sa, M. E., Morgante, C. V., Paes-de-Melo, B., Arraes, F. B. M., Martins-de-Sa, D., Silva, M. C. M., de Almeida Engler, J., & Grossi-de-Sa, M. F. (2022). Minc03328 effector gene downregulation severely affects Meloidogyne incognita parasitism in transgenic Arabidopsis thaliana. Planta, 255(2), 44. https://doi.org/10.1007/s00425-022-03823-4

[15]

Shivakumara, T. N., Somvanshi, V. S., Phani, V., Chaudhary, S., Hada, A., Budhwar, R., Shukla, R. N., & Rao, U. (2019). Meloidogyne incognita sterol-binding protein Mi-SBP-1 as a target for its management. International Journal for Parasitology, 49(13-14), 1061-1073. https://doi.org/10.1016/j.ijpara.2019.09.002

[16]

Lu, C. J., Tian, B. Y., Cao, Y., Zou, C. G., & Zhang, K. Q. (2016). Nuclear receptor nhr-48 is required for pathogenicity of the second stage (J2) of the plant parasite Meloidogyne incognita. Scientific Reports, 6(1), 34959. https://doi.org/10.1038/srep34959

[17]

Dong, L., Xu, J., Chen, S., Li, X., & Zuo, Y. (2016). Mi-flp-18 and Mi-mpk-1 genes are potential targets for Meloidogyne incognita control. The Journal of Parasitology, 102(2), 208-213. https://doi.org/10.1645/15-768

[18]

Wang, M., Wang, D., Zhang, X., Wang, X., Liu, W., Hou, X., Huang, X., Xie, B., & Cheng, X. (2016). Double-stranded RNA-mediated interference of dumpy genes in Bursaphelenchus xylophilus by feeding on filamentous fungal transformants. International Journal for Parasitology, 46(5-6), 351-360. https://doi.org/10.1016/j.ijpara.2016.01.008

[19]

Chen, L., Xu, M., Wang, C., Zheng, J., Huang, G., Chen, F., Peng, D., & Sun, M. (2020). Multi-copy alpha-amylase genes are crucial for Ditylenchus destructor to parasitize the plant host. PLoS One, 15(10), e0240805. https://doi.org/10.1371/journal.pone.0240805

[20]

Urwin, P. E., Lilley, C. J., & Atkinson, H. J. (2002). Ingestion of double-stranded RNA by preparasitic juvenile cyst nematodes leads to RNA interference. Molecular Plant-Microbe Interactions, 15(8), 747-752. https://doi.org/10.1094/MPMI.2002.15.8.747

[21]

Fanelli, E., Di Vito, M., Jones, J. T., & De Giorgi, C. (2005). Analysis of chitin synthase function in a plant parasitic nematode, Meloidogyne artiellia, using RNAi. Gene, 349, 87-95. https://doi.org/10.1016/j.gene.2004.11.045

[22]

Li, Y., Wang, K., Xie, H., Wang, D. W., Xu, C. L., Huang, X., Wu, W. J., & Li, D. L. (2015). Cathepsin B cysteine proteinase is essential for the development and pathogenesis of the plant parasitic nematode Radopholus similis. International Journal of Biological Sciences, 11(9), 1073-1087. https://doi.org/10.7150/ijbs.12065

[23]

Huang, G., Cong, Z., Liu, Z., Chen, F., Bravo, A., Soberón, M., Zheng, J., Peng, D., & Sun, M. (2024). Silencing Ditylenchus destructor cathepsin l-like cysteine protease has negative pleiotropic effect on nematode ontogenesis. Scientific Reports, 14(1), 10030. https://doi.org/10.1038/s41598-024-60018-5

[24]

Ercan, S., Giresi, P. G., Whittle, C. M., Zhang, X., Green, R. D., & Lieb, J. D. (2007). X chromosome repression by localization of the C. elegans dosage compensation machinery to sites of transcription initiation. Nature Genetics, 39(3), 403-408. https://doi.org/10.1038/ng1983

[25]

Peng, H., Peng, D. L., & Huang, W. K. (2009). Molecular cloning and sequence analysis of a new β-1, 4-endoglucanase gene (Dd-eng-1b) from migratory plant-parasitic nematode Ditylenchus destructor on sweetpotato in China. Journal of Agricultural Biotechnology, 17, 1035-1041.

[26]

Zheng, J., Peng, D., Chen, L., Liu, H., Chen, F., Xu, M., Ju, S., Ruan, L., & Sun, M. (2016). The Ditylenchus destructor genome provides new insights into the evolution of plant parasitic nematodes. Proceedings of the Royal Society B, 283(1835), 20160942. https://doi.org/10.1098/rspb.2016.0942

[27]

Katafuchi, T., & Makishima, M. (2022). Molecular basis of bile acid-FXR-FGF15/19 signaling axis. International Journal of Molecular Sciences, 23(11), 6046. https://doi.org/10.3390/ijms23116046

[28]

Shapiro, H., Kolodziejczyk, A. A., Halstuch, D., & Elinav, E. (2018). Bile acids in glucose metabolism in health and disease. Journal of Experimental Medicine, 215(2), 383-396. https://doi.org/10.1084/jem.20171965

[29]

Watterson, A., Tatge, L., Wajahat, N., Arneaud, S. L. B., Solano Fonseca, R., Beheshti, S. T., Metang, P., Mihelakis, M., Zuurbier, K. R., Corley, C. D., Dehghan, I., McDonald, J. G., & Douglas, P. M. (2022). Intracellular lipid surveillance by small G protein geranylgeranylation. Nature, 605(7911), 736-740. https://doi.org/10.1038/s41586-022-04729-7

[30]

Font-Díaz, J., Jiménez-Panizo, A., Caelles, C., Vivanco, M. D., Pérez, P., Aranda, A., Estébanez-Perpiñá, E., Castrillo, A., Ricote, M., & Valledor, A. F. (2021). Nuclear receptors: Lipid and hormone sensors with essential roles in the control of cancer development. Seminars in Cancer Biology, 73, 58-75. https://doi.org/10.1016/j.semcancer.2020.12.007

[31]

Cai, H., Dhondt, I., Vandemeulebroucke, L., Vlaeminck, C., Rasulova, M., & Braeckman, B. P. (2019). CBP-1 acts in GABAergic neurons to double life span in axenically cultured Caenorhabditis elegans. The Journals of Gerontology: Series A, 74(8), 1198-1205. https://doi.org/10.1093/gerona/glx206

[32]

Witze, E. S., Field, E. D., Hunt, D. F., & Rothman, J. H. (2009). C. elegans pur alpha, an activator of end-1, synergizes with the Wnt pathway to specify endoderm. Developmental Biology, 327(1), 12-23. https://doi.org/10.1016/j.ydbio.2008.11.015

[33]

Vishnupriya, R., Thomas, L., Wahba, L., Fire, A., & Subramaniam, K. (2020). PLP-1 is essential for germ cell development and germline gene silencing in Caenorhabditis elegans. Development, 147(22), dev195578. https://doi.org/10.1242/dev.195578

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2025 The Author(s). New Plant Protection published by John Wiley & Sons Australia, Ltd on behalf of Institute of Plant Protection, Chinese Academy of Agricultural Sciences.

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