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Transcriptome analysis reveals the role of Zelda in the regulation of embryonic and wing development of Tribolium castaneum

Published online by Cambridge University Press:  21 July 2023

Shanshan Gao
Affiliation:
Department of Food and Bioengineering, Anyang Institute of Technology, Anyang, Henan 455000, China
Shuang Xue
Affiliation:
Department of Food and Bioengineering, Anyang Institute of Technology, Anyang, Henan 455000, China
Tian Gao
Affiliation:
Department of Food and Bioengineering, Anyang Institute of Technology, Anyang, Henan 455000, China
Ruixue Lu
Affiliation:
Department of Food and Bioengineering, Anyang Institute of Technology, Anyang, Henan 455000, China
Xinyi Zhang
Affiliation:
Department of Food and Bioengineering, Anyang Institute of Technology, Anyang, Henan 455000, China
Yonglei Zhang
Affiliation:
College of Life Sciences, Nanjing Normal University, Nanjing, Jiangsu 210023, China
Kunpeng Zhang*
Affiliation:
Department of Food and Bioengineering, Anyang Institute of Technology, Anyang, Henan 455000, China
Ruimin Li*
Affiliation:
Department of Food and Bioengineering, Anyang Institute of Technology, Anyang, Henan 455000, China
*
Corresponding author: Kunpeng Zhang; Email: zhangkunpengag@163.com; Ruimin Li; Email: liruimin920130@163.com
Corresponding author: Kunpeng Zhang; Email: zhangkunpengag@163.com; Ruimin Li; Email: liruimin920130@163.com

Abstract

Zinc finger protein (Zelda) of Tribolium castaneum (TcZelda) has been showed to play pivotal roles in embryonic development and metamorphosis. However, the regulatory mechanism of TcZelda associated with these physiology processes is unclear. Herein, the developmental expression profile showed that Zelda of T. castaneum was highly expressed in early eggs. Tissue expression profiling revealed that TcZelda was mainly expressed in the larval head and adult ovary of late adults and late larvae. TcZelda knockdown led to a 95% mortality rate in adults. These results suggested that TcZelda is related to the activation of the zygote genome in early embryonic development. Furthermore, 592 differentially expressed genes were identified from the dsZelda treated group. Compared with the control group, altered disjunction (ALD) and AGAP005368-PA (GAP) in the dsZelda group were significantly down-regulated, while TGF-beta, propeptide (TGF) was significantly up-regulated, suggesting that TcZelda may be involved in insect embryonic development. In addition, the expression of Ubx ultrabithorax (UBX), Cx cephalothorax (CX), En engrailed (EN), and two Endocuticle structural glycoprotein sgabd (ABD) genes were significantly down-regulated, suggesting that they may cooperate with TcZelda to regulate the development of insect wings. Additionally, Elongation (ELO), fatty acid synthase (FAS), and fatty acyl-CoA desaturase (FAD) expression was inhibited in dsZelda insects, which could disturb the lipase signaling pathways, thus, disrupting the insect reproductive system and pheromone synthesis. These results may help reveal the function of TcZelda in insects and the role of certain genes in the gene regulatory network and provide new ideas for the prevention and control of T. castaneum.

Type
Research Paper
Copyright
Copyright © The Author(s), 2023. Published by Cambridge University Press

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References

Albre, J, Liénard, MA, Sirey, TM, Schmidt, S, Tooman, LK, Carraher, C, Greenwood, DR, Löfstedt, C and Newcomb, RD (2012) Sex pheromone evolution is associated with differential regulation of the same desaturase gene in two genera of leafroller moths. PLoS Genetics 8, e1002489.CrossRefGoogle ScholarPubMed
Begum, K, Li, B, Beeman, RW and Park, Y (2009) Functions of ion transport peptide and ion transport peptide-like in the red flour beetle Tribolium castaneum. Insect Biochemistry and Molecular Biology 39, 717725.CrossRefGoogle ScholarPubMed
Berg, JM and Shi, Y (1996) The galvanization of biology: a growing appreciation for the roles of zinc. Science 271, 10811085.CrossRefGoogle ScholarPubMed
Boos, A, Distler, J, Rudolf, H, Klingler, M and El-Sherif, E (2018) A re-inducible gap gene cascade patterns the anterior-posterior axis of insects in a threshold-free fashion. Elife 7, e41208.CrossRefGoogle Scholar
Bourgouin, C, Lundgren, SE and Thomas, JB (1992) Apterous is a Drosophila LIM domain gene required for the development of a subset of embryonic muscles. Neuron 9, 549561.CrossRefGoogle ScholarPubMed
Celniker, SE and Rubin, GM (2003) The Drosophila melanogaster genome. Annual Review of Genomics and Human Genetics 4, 89117.CrossRefGoogle ScholarPubMed
Chen, D and McKearin, D (2003) Dpp signaling silences bam transcription directly to establish asymmetric divisions of germline stem cells. Current Biology 13, 17861791.CrossRefGoogle ScholarPubMed
Dönitz, J, Schmitt-Engel, C, Grossmann, D, Gerischer, L, Tech, M, Schoppmeier, M, Klingler, M and Bucher, G (2015) iBeetle-Base: a database for RNAi phenotypes in the red flour beetle Tribolium castaneum. Nucleic Acids Research 43, D720D725.CrossRefGoogle ScholarPubMed
Frankel, AD and Pabo, CO (1988) Fingering too many proteins. Cell 53, 675.CrossRefGoogle ScholarPubMed
Guo, S, Dan, L, Li, Z, Jie, S and Entomology, DO (2017) Present status and perspectives of the researches on insect wing development. Journal of Plant Protection 44, 185195.Google Scholar
Haritos, VS, Horne, I, Damcevski, K, Glover, K and Gibb, N (2014) Unexpected functional diversity in the fatty acid desaturases of the flour beetle Tribolium castaneum and identification of key residues determining activity. Insect Biochemistry and Molecular Biology 51, 6270.CrossRefGoogle ScholarPubMed
Horn, T and Panfilio, KA (2016) Novel functions for Dorsocross in epithelial morphogenesis in the beetle Tribolium castaneum. Development 143, 30023011.Google ScholarPubMed
Iconomidou, VA, Willis, JH and Hamodrakas, SJ (2005) Unique features of the structural model of ‘hard’ cuticle proteins: implications for chitin-protein interactions and cross-linking in cuticle. Insect Biochemistry and Molecular Biology 35, 553560.CrossRefGoogle ScholarPubMed
Jakobsson, A, Westerberg, R and Jacobsson, A (2006) Fatty acid elongases in mammals: their regulation and roles in metabolism. Progress in Lipid Research 45, 237249.CrossRefGoogle ScholarPubMed
Jung, A, Hollmann, M and Schäfer, MA (2007) The fatty acid elongase NOA is necessary for viability and has a somatic role in Drosophila sperm development. Journal of Cell Science 120, 29242934.CrossRefGoogle Scholar
Kim, D, Langmead, B and Salzberg, SL (2015) HISAT: a fast spliced aligner with low memory requirements. Nature Methods 12, 357360.CrossRefGoogle ScholarPubMed
Langmead, B and Salzberg, SL (2012) Fast gapped-read alignment with Bowtie 2. Nature Methods 9, 357359.CrossRefGoogle ScholarPubMed
Lei, L, Jiang, Y, Liu, Z, You, L and Wu, J (2016) Jinggangmycin increases fecundity of the brown planthopper, Nilaparvata lugens (Stål) via fatty acid synthase gene expression. Journal of Proteomics 130, 140.CrossRefGoogle Scholar
Leonard, AE, Pereira, SL, Sprecher, H and Huang, YS (2004) Elongation of long-chain fatty acids. Progress in Lipid Research 43, 3654.CrossRefGoogle ScholarPubMed
Li, B and Dewey, CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12, 323.CrossRefGoogle ScholarPubMed
Li, HY, Lin, XW, Geng, SL and Xu, WH (2018) TGF-β and BMP signals regulate insect diapause through Smad1-POU-TFAM pathway. Biochim Biophys Acta Mol Cell Res 1865, 12391249.CrossRefGoogle ScholarPubMed
Liang, HL, Nien, CY, Liu, HY, Metzstein, MM, Kirov, N and Rushlow, C (2008 a) The zinc-finger protein Zelda is a key activator of the early zygotic genome in Drosophila. Nature 456, 400403.CrossRefGoogle ScholarPubMed
Liang, J, Song, W, Tromp, G, Kolattukudy, PE and Fu, M (2008 b) Genome-wide survey and expression profiling of CCCH-zinc finger family reveals a functional module in macrophage activation. PLoS ONE 3, e2880.CrossRefGoogle ScholarPubMed
Livak, KJ and Schmittgen, TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25, 402408.CrossRefGoogle ScholarPubMed
Miller, J, McLachlan, AD and Klug, A (1985) Repetitive zinc-binding domains in the protein transcription factor IIIA from Xenopus oocytes. EMBO Journal 4, 16091614.CrossRefGoogle ScholarPubMed
O'Tousa, J (1982) Meiotic chromosome behavior influenced by mutation-altered disjunction in Drosophila melanogaster females. Genetics 102, 503524.CrossRefGoogle ScholarPubMed
Pearson, JC, Watson, JD and Crews, ST (2012) Drosophila melanogaster Zelda and single-minded collaborate to regulate an evolutionarily dynamic CNS midline cell enhancer. Developmental Biology 366, 420432.CrossRefGoogle ScholarPubMed
Pires, CV, Freitas, FC, Cristino, AS, Dearden, PK and Simões, ZL (2016) Transcriptome analysis of honeybee (Apis mellifera) haploid and diploid embryos reveals early zygotic transcription during cleavage. PLoS ONE 11, e0146447.CrossRefGoogle ScholarPubMed
Reichardt, I, Bonnay, F, Steinmann, V, Loedige, I, Burkard, TR, Meister, G and Knoblich, JA (2018) The tumor suppressor Brat controls neuronal stem cell lineages by inhibiting Deadpan and Zelda. EMBO Reports 19, 102117.CrossRefGoogle ScholarPubMed
Ribeiro, L, Tobias-Santos, V, Santos, D, Antunes, F, Feltran, G, de Souza Menezes, J, Aravind, L, Venancio, TM and Nunes da Fonseca, R (2017) Evolution and multiple roles of the Pancrustacea specific transcription factor zelda in insects. PLoS Genetics 13, e1006868.CrossRefGoogle ScholarPubMed
Rolff, J, Johnston, PR and Reynolds, S (2019) Complete metamorphosis of insects. Philosophical Transactions of the Royal Society of London B Biological Sciences 374, 20190063.CrossRefGoogle ScholarPubMed
Sánchez, L and Thieffry, D (2001) A logical analysis of the Drosophila gap-gene system. Journal of Theoretical Biology 211, 115141.CrossRefGoogle ScholarPubMed
Schulz, KN, Bondra, ER, Moshe, A, Villalta, JE, Lieb, JD, Kaplan, T, McKay, DJ and Harrison, MM (2015) Zelda is differentially required for chromatin accessibility, transcription factor binding, and gene expression in the early Drosophila embryo. Genome Research 25, 17151726.CrossRefGoogle ScholarPubMed
Shyy, W, Kang, CK, Chirarattananon, P, Ravi, S and Liu, H (2016) Aerodynamics, sensing and control of insect-scale flapping-wing flight. Proceedings. Mathematical, Physical, and Engineering Sciences/the Royal Society 472, 20150712.CrossRefGoogle ScholarPubMed
Sim, C and Denlinger, DL (2009) Transcription profiling and regulation of fat metabolism genes in diapausing adults of the mosquito Culex pipiens. Physiological Genomics 39, 202209.CrossRefGoogle ScholarPubMed
Simmonds, AJ, Liu, X, Soanes, KH, Krause, HM, Irvine, KD and Bell, JB (1998) Molecular interactions between vestigial and scalloped promote wing formation in Drosophila. Genes & Development 12, 38153820.CrossRefGoogle ScholarPubMed
Song, X, Wong, MD, Kawase, E, Xi, R, Ding, BC, McCarthy, JJ and Xie, T (2004) Bmp signals from niche cells directly repress transcription of a differentiation-promoting gene, bag of marbles, in germline stem cells in the Drosophila ovary. Development 131, 13531364.CrossRefGoogle ScholarPubMed
Tomoyasu, Y, Wheeler, SR and Denell, RE (2005) Ultrabithorax is required for membranous wing identity in the beetle Tribolium castaneum. Nature 433, 643647.CrossRefGoogle ScholarPubMed
Ventos-Alfonso, A, Ylla, G and Belles, X (2019) Zelda and the maternal-to-zygotic transition in cockroaches. FEBS Journal 286, 32063221.CrossRefGoogle ScholarPubMed
Wang, Y, da Cruz, TC, Pulfemuller, A, Grégoire, S, Ferveur, JF and Moussian, B (2016) Inhibition of fatty acid desaturases in Drosophila melanogaster larvae blocks feeding and developmental progression. Archives of Insect Biochemistry and Physiology 92, 623.CrossRefGoogle ScholarPubMed
Williams, JA, Paddock, SW, Vorwerk, K and Carroll, SB (1994) Organization of wing formation and induction of a wing-patterning gene at the dorsal/ventral compartment boundary. Nature 368, 299305.CrossRefGoogle ScholarPubMed
Wu, SY, Tong, XL, Li, CL, Ding, X, Zhang, ZL, Fang, CY, Tan, D, Hu, H, Liu, H and Dai, FY (2019) BmBlimp-1 gene encoding a C2H2 zinc finger protein is required for wing development in the silkworm Bombyx mori. International Journal of Biological Sciences 15, 26642675.CrossRefGoogle ScholarPubMed
Zhao, N and Zhao, F (2009) Advances in research on zinc finger protein. Letters in Biotechnology 20, 131134.Google Scholar
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