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Artificial selection on storage protein 1 possibly contributes to increase of hatchability during silkworm domestication.

ABSTRACT: Like other domesticates, the efficient utilization of nitrogen resources is also important for the only fully domesticated insect, the silkworm. Deciphering the way in which artificial selection acts on the silkworm genome to improve the utilization of nitrogen resources and to advance human-favored domestication traits, will provide clues from a unique insect model for understanding the general rules of Darwin's evolutionary theory on domestication. Storage proteins (SPs), which belong to a hemocyanin superfamily, basically serve as a source of amino acids and nitrogen during metamorphosis and reproduction in insects. In this study, through blast searching on the silkworm genome and further screening of the artificial selection signature on silkworm SPs, we discovered a candidate domestication gene, i.e., the methionine-rich storage protein 1 (SP1), which is clearly divergent from other storage proteins and exhibits increased expression in the ova of domestic silkworms. Knockout of SP1 via the CRISPR/Cas9 technique resulted in a dramatic decrease in egg hatchability, without obvious impact on egg production, which was similar to the effect in the wild silkworm compared with the domestic type. Larval development and metamorphosis were not affected by SP1 knockout. Comprehensive ova comparative transcriptomes indicated significant higher expression of genes encoding vitellogenin, chorions, and structural components in the extracellular matrix (ECM)-interaction pathway, enzymes in folate biosynthesis, and notably hormone synthesis in the domestic silkworm, compared to both the SP1 mutant and the wild silkworm. Moreover, compared with the wild silkworms, the domestic one also showed generally up-regulated expression of genes enriched in the structural constituent of ribosome and amide, as well as peptide biosynthesis. This study exemplified a novel case in which artificial selection could act directly on nitrogen resource proteins, further affecting egg nutrients and eggshell formation possibly through a hormone signaling mediated regulatory network and the activation of ribosomes, resulting in improved biosynthesis and increased hatchability during domestication. These findings shed new light on both the understanding of artificial selection and silkworm breeding from the perspective of nitrogen and amino acid resources.

SUBMITTER: Zhu YN

PROVIDER: S-EPMC6358105 | biostudies-literature | 2019 Jan

REPOSITORIES: biostudies-literature

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Artificial selection on storage protein 1 possibly contributes to increase of hatchability during silkworm domestication.

Zhu Ya-Nan YN Wang Li-Zhi LZ Li Cen-Cen CC Cui Yong Y Wang Man M Lin Yong-Jian YJ Zhao Ruo-Ping RP Wang Wen W Xiang Hui H

PLoS genetics 20190122 1

Like other domesticates, the efficient utilization of nitrogen resources is also important for the only fully domesticated insect, the silkworm. Deciphering the way in which artificial selection acts on the silkworm genome to improve the utilization of nitrogen resources and to advance human-favored domestication traits, will provide clues from a unique insect model for understanding the general rules of Darwin's evolutionary theory on domestication. Storage proteins (SPs), which belong to a hem ...[more]

PMID: 30668559

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Project description: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.

Project description:Early domestication and the following improvement are two important processes in the cocoon silk evolution of silkworms. In contrast to early domestication, understanding of the improvement process is still fuzzy. By systematically comparing the larval silk gland transcriptomes of the wild, early domestic, and improved silkworms, we highlighted a novel landscape of transcriptome in the silk glands of improved ones. We first clarified that silk cocoon protein genes were up-regulated in modern breeding but not in early domestication. Furthermore, we found that differentially expressed genes (DEGs) between improved and early domestic silkworms (2711), as well as between improved and wild silkworms (2264), were obviously more than those between the early domestic and wild silkworms (158), with 1671 DEGs specific in the improved silkworm (IS-DEGs). Hierarchical clustering of all the DEGs consistently indicated that improved silkworms were significantly diverged from the early domestic and wild silkworms, suggesting that modern breeding might cause prompt and drastic dynamic changes of gene expression in the silk gland. We further paid attention to these 1671 IS-DEGs and were surprised to find that down-regulated genes were enriched in basic organonitrogen compound biosynthesis, RNA biosynthesis, and ribosome biogenesis processes, which are generally universally expressed, whereas those up-regulated genes were enriched in organonitrogen compound catabolic processes and functions involving in the dynamic regulation of protein post-translation of modification. We finally highlighted one candidate improvement gene among these up-regulated IS-DEGs, i.e., GDAP2, which may play roles in silk behavior and the overall robustness of the improved silkworm. The findings strongly suggest that modern breeding may facilitate effective control of the basic consumption of nitrogen and a stronger switch of nitrogen resources from other tissues to the silk glands, for an efficient supply for silk production, and implies the importance of brain behavior and robustness in silk yield improvement of modern breeding.

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Artificial selection on storage protein 1 possibly contributes to increase of hatchability during silkworm domestication.

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Artificial selection on storage protein 1 possibly contributes to increase of hatchability during silkworm domestication.

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