A molecular atlas reveals the tri-sectional spinning mechanism of spider dragline silk

Wenbo Hu, Anqiang Jia, Sanyuan Ma, Guoqing Zhang, Zhaoyuan Wei, Fang Lu, Yongjiang Luo, Zhisheng Zhang, Jiahe Sun, Tianfang Yang, TingTing Xia, Qinhui Li, Ting Yao, Jiangyu Zheng, Zijie Jiang, Zehui Xu, Qingyou Xia () and Yi Wang ()
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Wenbo Hu: Southwest University
Anqiang Jia: Southwest University
Sanyuan Ma: Southwest University
Guoqing Zhang: Southwest University
Zhaoyuan Wei: Southwest University
Fang Lu: Southwest University
Yongjiang Luo: Southwest University
Zhisheng Zhang: Southwest University
Jiahe Sun: Southwest University
Tianfang Yang: Southwest University
TingTing Xia: Southwest University
Qinhui Li: Southwest University
Ting Yao: Southwest University
Jiangyu Zheng: Southwest University
Zijie Jiang: Southwest University
Zehui Xu: Southwest University
Qingyou Xia: Southwest University
Yi Wang: Southwest University

Nature Communications, 2023, vol. 14, issue 1, 1-16

Abstract: Abstract The process of natural silk production in the spider major ampullate (Ma) gland endows dragline silk with extraordinary mechanical properties and the potential for biomimetic applications. However, the precise genetic roles of the Ma gland during this process remain unknown. Here, we performed a systematic molecular atlas of dragline silk production through a high-quality genome assembly for the golden orb-weaving spider Trichonephila clavata and a multiomics approach to defining the Ma gland tri-sectional architecture: Tail, Sac, and Duct. We uncovered a hierarchical biosynthesis of spidroins, organic acids, lipids, and chitin in the sectionalized Ma gland dedicated to fine silk constitution. The ordered secretion of spidroins was achieved by the synergetic regulation of epigenetic and ceRNA signatures for genomic group-distributed spidroin genes. Single-cellular and spatial RNA profiling identified ten cell types with partitioned functional division determining the tri-sectional organization of the Ma gland. Convergence analysis and genetic manipulation further validated that this tri-sectional architecture of the silk gland was analogous across Arthropoda and inextricably linked with silk formation. Collectively, our study provides multidimensional data that significantly expand the knowledge of spider dragline silk generation and ultimately benefit innovation in spider-inspired fibers.

Date: 2023
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DOI: 10.1038/s41467-023-36545-6

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