GASZ is indispensable for gametogenesis in the silkworm, Bombyx mori.

Bombyx mori GASZ gametogenesis piRNA spermatogenesis

Journal

Insect molecular biology
ISSN: 1365-2583
Titre abrégé: Insect Mol Biol
Pays: England
ID NLM: 9303579

Informations de publication

Date de publication:
10 May 2024
Historique:
received: 20 01 2024
accepted: 28 04 2024
medline: 10 5 2024
pubmed: 10 5 2024
entrez: 10 5 2024
Statut: aheadofprint

Résumé

The prominent role of the P-element induced wimpy testis (PIWI)-interacting RNA (piRNA) pathway in animals is to silence transposable elements and maintain genome stability, ensuring proper gametogenesis in gonads. GASZ (Germ cell protein with Ankyrin repeats, Sterile alpha motif, and leucine Zipper) is an evolutionarily conserved protein located on the outer mitochondrial membrane of germ cells and plays vital roles in the piRNA pathway and spermatogenesis in mammals. In the model insect Drosophila melanogaster, GASZ is essential for piRNA biogenesis and oogenesis, whereas its biological functions in non-drosophilid insects are still unknown. Here, we describe a comprehensive investigation of GASZ functions in the silkworm, Bombyx mori, a lepidopteran model insect, by using a binary transgenic CRISPR/Cas9 system. The BmGASZ mutation did not affect growth and development, but led to sterility in both males and females. Eupyrene sperm bundles of mutant males exhibited developmental defects, while the apyrene sperm bundles were normal, which were further confirmed through double copulation experiments with sex-lethal mutants, which males possess functional eupyrene sperm and abnormal apyrene sperm. In female mutant moths, ovarioles were severely degenerated and the eggs in ovarioles were deformed compared with that of wild type (WT). Further RNA-seq and RT-qPCR analysis revealed that amounts of piRNAs and transposon expression were dysregulated in gonads of mutants. In summary, this study has demonstrated vital roles of BmGASZ in gametogenesis through regulating the piRNA pathway in B. mori.

Identifiants

pubmed: 38728119
doi: 10.1111/imb.12921
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Natural Science Foundation of Jiangsu Province
ID : BK20210880
Organisme : National Natural Science Foundation of China
ID : 31925007
Organisme : National Natural Science Foundation of China
ID : 32102611

Informations de copyright

© 2024 Royal Entomological Society.

Références

Aliyari, R. & Ding, S.W. (2009) RNA‐based viral immunity initiated by the Dicer family of host immune receptors. Immunological Reviews, 227, 176–188. Available from: https://doi.org/10.1111/j.1600-065X.2008.00722.x
Carmell, M.A., Girard, A., van de Kant, H.J., Bourc'his, D., Bestor, T.H., de Rooij, D.G. et al. (2007) MIWI2 is essential for spermatogenesis and repression of transposons in the mouse male germline. Developmental Cell, 12, 503–514. Available from: https://doi.org/10.1016/j.devcel.2007.03.001
Chak, L.L. & Okamura, K. (2014) Argonaute‐dependent small RNAs derived from single‐stranded, non‐structured precursors. Frontiers in Genetics, 5, 172. Available from: https://doi.org/10.3389/fgene.2014.00172
Chen, K., Chen, S., Xu, J., Yu, Y., Liu, Z., Tan, A. et al. (2019) Maelstrom regulates spermatogenesis of the silkworm, Bombyx mori. Insect Biochemistry and Molecular Biology, 109, 43–51. Available from: https://doi.org/10.1016/j.ibmb.2019.03.012
Chen, K., Yang, X., Yang, D. & Huang, Y. (2023) Spindle‐E is essential for gametogenesis in the silkworm, Bombyx mori. Insect Science, 30, 293–304. Available from: https://doi.org/10.1111/1744-7917.13096
Chen, K., Yu, Y., Yang, D., Yang, X., Tang, L., Liu, Y. et al. (2020) Gtsf1 is essential for proper female sex determination and transposon silencing in the silkworm, Bombyx mori. PLoS Genetics, 16, e1009194. Available from: https://doi.org/10.1371/journal.pgen.1009194
Chen, K., Yu, Y., Zhang, Z., Hu, B., Liu, X., James, A.A. et al. (2023) Engineering a complex, multiple enzyme‐mediated synthesis of natural plant pigments in the silkworm, Bombyx mori. Proceedings of the National Academy of Sciences of the United States of America, 120, e2306322120. Available from: https://doi.org/10.1073/pnas.2306322120
Chen, K., Yu, Y., Zhang, Z., Hu, B., Liu, X. & Tan, A. (2023) The morphogen Hedgehog is essential for proper adult morphogenesis in Bombyx mori. Insect Biochemistry and Molecular Biology, 153, 103906. Available from: https://doi.org/10.1016/j.ibmb.2022.103906
Chen, S., Liu, Y., Yang, X., Liu, Z., Luo, X., Xu, J. et al. (2020) Dysfunction of dimorphic sperm impairs male fertility in the silkworm. Cell Discovery, 6, 60. Available from: https://doi.org/10.1038/s41421-020-00194-6
Chuma, S. & Nakano, T. (2013) piRNA and spermatogenesis in mice. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 368, 20110338. Available from: https://doi.org/10.1098/rstb.2011.0338
Chuong, E.B., Elde, N.C. & Feschotte, C. (2017) Regulatory activities of transposable elements: from conflicts to benefits. Nature Reviews Genetics, 18, 71–86. Available from: https://doi.org/10.1038/nrg.2016.139
Clark, J.P. & Lau, N.C. (2014) Piwi proteins and piRNAs step onto the systems biology stage. Advances in Experimental Medicine and Biology, 825, 159–197. Available from: https://doi.org/10.1007/978-1-4939-1221-6_5
Czech, B., Munafò, M., Ciabrelli, F., Eastwood, E.L., Fabry, M.H., Kneuss, E. et al. (2018) piRNA‐guided genome defense: from biogenesis to silencing. Annual Review of Genetics, 52, 131–157. Available from: https://doi.org/10.1146/annurev-genet-120417-031441
Friedländer, M. & Hauschteck‐Jungen, E. (1982) Differential basic nucleoprotein kinetics in the two kinds of Lepidoptera spermatids: nucleate (eupyrene) and anucleate (apyrene). Chromosoma, 85, 387–398. Available from: https://doi.org/10.1007/BF00330361
Friedländer, M., Seth, R.K. & Reynolds, S.E. (2005) Eupyrene and Apyrene sperm: dichotomous spermatogenesis in Lepidoptera. Advances in insect physiology, 32, 206–308. Available from: https://doi.org/10.1016/S0065-2806(05)32003-0
Hirakata, S. & Siomi, M.C. (2019) Assembly and function of gonad‐specific non‐membranous organelles in Drosophila piRNA biogenesis. Noncoding RNA, 5, 52. Available from: https://doi.org/10.3390/ncrna5040052
Hiroyoshi, S., Yoshimura, J., Iwabuchi, K., Reddy, G.V.P. & Mitsuhashi, J. (2017) Effects of pre‐overwintering conditions on eupyrene and apyrene spermatogenesis after overwintering in Polygonia c‐aureum (Lepidoptera: Nymphalidae). Journal of Insect Physiology, 100, 1–8. Available from: https://doi.org/10.1016/j.jinsphys.2017.04.008
Honda, S., Kirino, Y. & Kirino, Y. (2014) Analysis of sDMA modifications of PIWI proteins. Methods in Molecular Biology, 1093, 137–148. Available from: https://doi.org/10.1007/978-1-62703-694-8_11
Huang, X., Fejes Toth, K. & Aravin, A.A. (2017) piRNA biogenesis in Drosophila melanogaster. Trends in Genetics, 33, 882–894. Available from: https://doi.org/10.1016/j.tig.2017.09.002
Katsuma, S., Kiuchi, T., Kawamoto, M., Fujimoto, T. & Sahara, K. (2018) Unique sex determination system in the silkworm, Bombyx mori: current status and beyond. Proceedings of the Japan Academy. Series B, Physical and Biological Sciences, 94, 205–216. Available from: https://doi.org/10.2183/pjab.94.014
Kawamura, N., Yamashiki, N., Saitoh, H. & Sahara, K. (2000) Peristaltic squeezing of sperm bundles at the late stage of spermatogenesis in the silkworm, Bombyx mori. Journal of Morphology, 246, 53–58. Available from: https://doi.org/10.1002/1097-4687(200011)246:2<53::AID-JMOR1>3.0.CO;2-P
Kawamura, N., Yamashiki, N., Saitoh, H. & Sahara, K. (2001) Significance of peristaltic squeezing of sperm bundles in the silkworm, Bombyx mori: elimination of irregular eupyrene sperm nuclei of the triploid. Zygote, 9, 159–166. Available from: https://doi.org/10.1002/1097-4687(200011)246:2<53::AID-JMOR1>3.0.CO;2-P
Kiuchi, T., Shoji, K., Izumi, N., Tomari, Y. & Katsuma, S. (2023) Non‐gonadal somatic piRNA pathways ensure sexual differentiation, larval growth, and wing development in silkworms. PLoS Genetics, 19, e1010912. Available from: https://doi.org/10.1371/journal.pgen.1010912
Li, Z., You, L., Yan, D., James, A.A., Huang, Y. & Tan, A. (2018) Bombyx mori histone methyltransferase BmAsh2 is essential for silkworm piRNA‐mediated sex determination. PLoS Genetics, 14, e1007245. Available from: https://doi.org/10.1371/journal.pgen.1007245
Ma, L., Buchold, G.M., Greenbaum, M.P., Roy, A., Burns, K.H., Zhu, H. et al. (2009) GASZ is essential for male meiosis and suppression of retrotransposon expression in the male germline. PLoS Genetics, 5, e1000635. Available from: https://doi.org/10.1371/journal.pgen.1000635
Munafo, M., Manelli, V., Falconio, F.A., Sawle, A., Kneuss, E., Eastwood, E.L. et al. (2019) Daedalus and Gasz recruit Armitage to mitochondria, bringing piRNA precursors to the biogenesis machinery. Genes & Development, 33, 844–856. Available from: https://doi.org/10.1101/gad.325662.119
Sakai, H., Oshima, H., Yuri, K., Gotoh, H., Daimon, T., Yaginuma, T. et al. (2019) Dimorphic sperm formation by sex‐lethal. Proceedings of the National Academy of Sciences of the United States of America, 116, 10412–10417. Available from: https://doi.org/10.1073/pnas.1820101116
Sato, K. & Siomi, M.C. (2020) The piRNA pathway in Drosophila ovarian germ and somatic cells. Proceedings of the Japan Academy. Series B, Physical and Biological Sciences, 96, 32–42. Available from: https://doi.org/10.2183/pjab.96.003
Shi, L.Z., Nascimento, J.M., Chandsawangbhuwana, C., Botvinick, E.L. & Berns, M.W. (2008) An automatic system to study sperm motility and energetics. Biomedical Microdevices, 10, 573–583. Available from: https://doi.org/10.1007/s10544-008-9169-4
Siomi, M.C., Sato, K., Pezic, D. & Aravin, A.A. (2011) PIWI‐interacting small RNAs: the vanguard of genome defence. Nature Reviews Molecular Cell Biology, 12, 246–258. Available from: https://doi.org/10.1038/nrm3089
Story, B., Ma, X., Ishihara, K., Li, H., Hall, K., Peak, A. et al. (2019) Defining the expression of piRNA and transposable elements in Drosophila ovarian germline stem cells and somatic support cells. Life Science Alliance, 2, e201800211. Available from: https://doi.org/10.26508/lsa.201800211
Tan, A., Fu, G., Jin, L., Guo, Q., Li, Z., Niu, B. et al. (2013) Transgene‐based, female‐specific lethality system for genetic sexing of the silkworm, Bombyx mori. Proceedings of the National Academy of Sciences of the United States of America, 110, 6766–6770. Available from: https://doi.org/10.1073/pnas.1221700110
Teng, X., Zhang, Z., He, G., Yang, L. & Li, F. (2012) Validation of reference genes for quantitative expression analysis by real‐time rt‐PCR in four lepidopteran insects. Journal of Insect Science, 12, 60. Available from: https://doi.org/10.1673/031.012.6001
Tóth, K.F., Pezic, D., Stuwe, E. & Webster, A. (2016) The piRNA pathway guards the germline genome against transposable elements. Advances in Experimental Medicine and Biology, 886, 51–77. Available from: https://doi.org/10.1007/978-94-017-7417-8_4
Vagin, V.V., Sigova, A., Li, C., Seitz, H., Gvozdev, V. & Zamore, P.D. (2006) A distinct small RNA pathway silences selfish genetic elements in the germline. Science, 313, 320–324. Available from: https://doi.org/10.26508/lsa.202000912
Vrettos, N., Maragkakis, M., Alexiou, P., Sgourdou, P., Ibrahim, F., Palmieri, D. et al. (2021) Modulation of Aub‐TDRD interactions elucidates piRNA amplification and germplasm formation. Life Science Alliance, 4, e202000912. Available from: https://doi.org/10.26508/lsa.202000912
Wyrwoll, M.J., Gaasbeek, C.M., Golubickaite, I., Stakaitis, R., Oud, M.S., Nagirnaja, L. et al. (2022) The piRNA‐pathway factor FKBP6 is essential for spermatogenesis but dispensable for control of meiotic LINE‐1 expression in humans. American Journal of Human Genetics, 109, 1850–1866. Available from: https://doi.org/10.1016/j.ajhg.2022.09.002
Yamashiki, N. & Kawamura, N. (1998) Behavior of centrioles during meiosis in the male silkworm, Bombyx mori (Lepidoptera). Development, Growth & Differentiation, 40, 619–630. Available from: https://doi.org/10.1046/j.1440-169X.1998.t01-4-00006.x
Yan, W., Rajkovic, A., Viveiros, M.M., Burns, K.H., Eppig, J.J. & Matzuk, M.M. (2002) Identification of Gasz, an evolutionarily conserved gene expressed exclusively in germ cells and encoding a protein with four ankyrin repeats, a sterile‐alpha motif, and a basic leucine zipper. Molecular Endocrinology, 16, 1168–1184. Available from: https://doi.org/10.1210/mend.16.6.0864
Yang, D., Xu, J., Chen, K., Liu, Y., Yang, X., Tang, L. et al. (2022) BmPMFBP1 regulates the development of eupyrene sperm in the silkworm, Bombyx mori. PLoS Genetics, 18, e1010131. Available from: https://doi.org/10.1371/journal.pgen.1010131
Yang, X., Chen, D., Zheng, S., Yi, M., Liu, Z., Liu, Y. et al. (2022) BmHen1 is essential for eupyrene sperm development in Bombyx mori but PIWI proteins are not. Insect Biochemistry and Molecular Biology, 151, 103874. Available from: https://doi.org/10.1016/j.ibmb.2022.103874
Yang, X., Chen, D., Zheng, S., Yi, M., Wang, S., Liu, Y. et al. (2023) The Prmt5‐Vasa module is essential for spermatogenesis in Bombyx mori. PLoS Genetics, 19, e1010600. Available from: https://doi.org/10.1371/journal.pgen.1010600
Zhang, J., Chen, S. & Liu, K. (2022) Structural insights into piRNA biogenesis. Biochimica et Biophysica Acta‐Gene Regulatory Mechanisms, 1865, 194799. Available from: https://doi.org/10.1016/j.bbagrm.2022.194799
Zhang, J., Wang, Q., Wang, M., Jiang, M., Wang, Y., Sun, Y. et al. (2016) GASZ and mitofusin‐mediated mitochondrial functions are crucial for spermatogenesis. EMBO Reports, 17, 220–234. Available from: https://doi.org/10.15252/embr.201540846

Auteurs

Peilin Guo (P)

Jiangsu Key Laboratory of Sericultural Biology and Biotechnology, School of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang, China.
Key Laboratory of Silkworm and Mulberry Genetic Improvement, Ministry of Agriculture, Sericultural Scientific Research Center, Chinese Academy of Agricultural Sciences, Zhenjiang, China.

Ye Yu (Y)

Jiangsu Key Laboratory of Sericultural Biology and Biotechnology, School of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang, China.
Key Laboratory of Silkworm and Mulberry Genetic Improvement, Ministry of Agriculture, Sericultural Scientific Research Center, Chinese Academy of Agricultural Sciences, Zhenjiang, China.

Hongxia Kang (H)

Jiangsu Key Laboratory of Sericultural Biology and Biotechnology, School of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang, China.
Key Laboratory of Silkworm and Mulberry Genetic Improvement, Ministry of Agriculture, Sericultural Scientific Research Center, Chinese Academy of Agricultural Sciences, Zhenjiang, China.

Yutong Liu (Y)

Jiangsu Key Laboratory of Sericultural Biology and Biotechnology, School of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang, China.
Key Laboratory of Silkworm and Mulberry Genetic Improvement, Ministry of Agriculture, Sericultural Scientific Research Center, Chinese Academy of Agricultural Sciences, Zhenjiang, China.

Dalin Zhu (D)

Jiangsu Key Laboratory of Sericultural Biology and Biotechnology, School of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang, China.
Key Laboratory of Silkworm and Mulberry Genetic Improvement, Ministry of Agriculture, Sericultural Scientific Research Center, Chinese Academy of Agricultural Sciences, Zhenjiang, China.

Chenxin Sun (C)

Jiangsu Key Laboratory of Sericultural Biology and Biotechnology, School of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang, China.
Key Laboratory of Silkworm and Mulberry Genetic Improvement, Ministry of Agriculture, Sericultural Scientific Research Center, Chinese Academy of Agricultural Sciences, Zhenjiang, China.

Zhiping Xing (Z)

Jiangsu Key Laboratory of Sericultural Biology and Biotechnology, School of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang, China.
Key Laboratory of Silkworm and Mulberry Genetic Improvement, Ministry of Agriculture, Sericultural Scientific Research Center, Chinese Academy of Agricultural Sciences, Zhenjiang, China.

Ziyue Tang (Z)

Jiangsu Key Laboratory of Sericultural Biology and Biotechnology, School of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang, China.
Key Laboratory of Silkworm and Mulberry Genetic Improvement, Ministry of Agriculture, Sericultural Scientific Research Center, Chinese Academy of Agricultural Sciences, Zhenjiang, China.

Kai Chen (K)

Jiangsu Key Laboratory of Sericultural Biology and Biotechnology, School of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang, China.
Key Laboratory of Silkworm and Mulberry Genetic Improvement, Ministry of Agriculture, Sericultural Scientific Research Center, Chinese Academy of Agricultural Sciences, Zhenjiang, China.

Anjiang Tan (A)

Jiangsu Key Laboratory of Sericultural Biology and Biotechnology, School of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang, China.
Key Laboratory of Silkworm and Mulberry Genetic Improvement, Ministry of Agriculture, Sericultural Scientific Research Center, Chinese Academy of Agricultural Sciences, Zhenjiang, China.

Classifications MeSH