A Comparison of Co-expression Networks in Silk Gland Reveals the Causes of Silk Yield Increase During Silkworm Domestication.

Qiu-Zhong Zhou,Ze Zhang,Shu-Shang Li,Quan-You Yu,Hong-Bo Zhang,Chuan-Zhen Qiu,Ping Fu,Chang-Jiang Zhang

doi:10.3389/fgene.2020.00225

Abstract

Long-term domestication and selective breeding have increased the silk yield of the domestic silkworm (Bombyx mori) by several times the amount of the silk yield of its wild ancestor (Bombyx mandarina). However, little is known about the molecular mechanisms behind the increase in silk yield during domestication. Based on dynamic patterns of functional divergence in the silk gland between domestic and wild silkworms, we found that at early and intermediate stages of silk gland development, the up-regulated genes of the domestic silkworm were mainly involved in DNA integration, nucleic acid binding, and transporter activity, which are related to the division and growth of cells. This has led to the posterior silk gland (PSG) of the domestic silkworm having significantly more cells (“factories” of fibroin protein synthesis) than that of the wild silkworm. At the late stage of silk gland development, the up-regulated genes in the domestic silkworm was enriched in protein processing and ribosome pathways, suggesting protein synthesis efficiency is greatly improved during silkworm domestication. While there was an increase in fibroin protein synthesis, the production of sericin protein was simultaneously reduced in the silk gland of the domestic silkworm. This reflects that domestic and wild silkworms have been under different selection pressures. Importantly, we found that the network co-expressed with the silk-coding genes of the domestic silkworm was larger than that of the wild silkworm. Furthermore, many more genes co-expressed with silk-coding genes in the domestic silkworm were subjected to artificial selection than those in the wild silkworm. Our results revealed that the increase of silk yield during silkworm domestication is involved in improvement of a biological system which includes not only expansion of “factories” (cells of PSG) of protein synthesis, but also a high expression of silk-coding genes and silk production-related genes such as biological energy, transport, and ribosome pathway genes.

Highlights

The domestic silkworm (Bombyx mori) was domesticated from the Chinese wild silkworm (Bombyx mandarina) about 5,000 years ago (Astaurov and Rovinskaya, 1959; Shimada et al, 1995; Sun et al, 2012)
Silk fibroin consists of the fibroin heavy chain (Fib-H), fibroin light chain (Fib-L), and 25-kD polypeptide proteins (P25) with a molar ratio of 6:6:1 (Inoue et al, 2000), which are synthesized in the posterior silk gland (PSG), one of three specialized compartments of the gland
Apart from more “factories” for silk fibroins production, our results revealed that in the late stage of silk gland development, the up-regulated genes in the domestic silkworm are enriched in protein processing in the endoplasmic reticulum and ribosome pathways (Figure 2A and Supplementary Figure S4A), indicating that protein synthesis is more active in the domestic silkworm

Summary

Introduction

The domestic silkworm (Bombyx mori) was domesticated from the Chinese wild silkworm (Bombyx mandarina) about 5,000 years ago (Astaurov and Rovinskaya, 1959; Shimada et al, 1995; Sun et al, 2012). It was found that the differentially expressed genes (DEGs) were mainly involved in the processing and biosynthesis of proteins (Li et al, 2016), and silk gland development or protein synthesis (Luan et al, 2018). These studies have provided some insights into the genetic basis of silk production, no gene that regulates silk yield in silkworm has been functionally verified. This implies that the molecular mechanisms underlying silk production may be much more complex than thought before

Methods

Results

Discussion

Conclusion