Abstract
Background The animal sperm shows high diversity in morphology, components, and motility. In the lepidopteran model insect, the silkworm Bombyx mori, two types of sperm, including nucleate fertile eupyrene sperm and anucleate unfertile apyrene sperm, are generated. Apyrene sperm assists fertilization by facilitating the migration of eupyrene spermatozoa from the bursa copulatrix to the spermatheca. During spermatogenesis, eupyrene sperm bundles extrude the cytoplasm by peristaltic squeezing, while the nuclei of the apyrene sperm bundles are discarded with the same process, forming matured sperm.
Results In this study, we describe that a mechanoreceptor BmPiezo, the sole Piezo ortholog in B. mori, plays key roles in larval feeding behavior and, more importantly, is essential for eupyrene spermatogenesis and male fertility. CRISPR/ Cas9-mediated loss of BmPiezo function decreases larval appetite and subsequent body size and weight. Immunofluorescence analyses reveal that BmPiezo is intensely localized in the inflatable point of eupyrene sperm bundle induced by peristaltic squeezing. BmPiezo is also enriched in the middle region of apyrene sperm bundle before peristaltic squeezing. Cytological analyses of dimorphic sperm reveal developmental arrest of eupyrene sperm bundles in BmPiezo mutants, while the apyrene spermatogenesis is not affected. RNA-seq analysis and q-RT-PCR analyses demonstrate that eupyrene spermatogenic arrest is associated with the dysregulation of the actin cytoskeleton. Moreover, we show that the deformed eupyrene sperm bundles fail to migrate from the testes, resulting in male infertility due to the absence of eupyrene sperm in the bursa copulatrix and spermatheca.
Conclusions In conclusion, our studies thus uncover a new role for Piezo in regulating spermatogenesis and male fertility in insects.
Document Type
Article
Publication Date
2024
Digital Object Identifier (DOI)
https://doi.org/10.1186/s12915-024-01916-y
Funding Information
This work was supported by the National Science Foundation of China (31925007, 32000336, and 32000339), the Natural Science Foundation of Jiangsu Province (BK20231249), and the Jiangsu Provincial Association for Sci- ence and Technology Young Scientific and Technological Talents Trusteeship Project (T-2022-045).
Repository Citation
Zhang, Zhongjie; Liu, Xiaojing; Hu, Bo; Chen, Kai; Yu, Ye; Sun, Chenxin; Zhu, Dalin; Bai, Hua; Palli, Subba Reddy; and Tan, Anjiang, "The mechanoreceptor Piezo is required for spermatogenesis in Bombyx mori" (2024). Entomology Faculty Publications. 259.
https://uknowledge.uky.edu/entomology_facpub/259
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Notes/Citation Information
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