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.

Genomic divergences between the two polyphagous Spodoptera relatives provide cues for successful invasion of the fall armyworm

“…In the brown planthopper, knockdown of one type of chorion protein resulted in oocyte malformation and the inability to perform oviposition (Lou et al ., 2018). In the silkworm, lack of nitrogen resource protein (SP1) led to significant repression of chorion gene expression and reduced hatchability (Zhu et al ., 2019). These findings suggest the role of these proteins in laying and hatching processes.…”

The acetylation modification regulates the stability of Bm30K‐15 protein and its mechanism in silkworm, Bombyx mori

“…Studies have shown that silkworm hemolymph contains many nutrient storage proteins, including apolipophorins, storage proteins, vitellogenin, and 30K proteins (Zhang et al, 2014), many of which show antiapoptotic and catalytic activities or serve as sources of nitrogen and amino acids in insect cells (Kang & Rhee, 2019; Rhee et al, 2002; Zhang et al, 2014; Zhu, Wang, et al, 2019). During larval‐pupal metamorphosis, the degenerated silk gland cells shift to the function of synthesizing a large amount of 30K proteins (Wang et al, 2016).…”

Genetic Mapping of Climbing and Mimicry: Two Behavioral Traits Degraded During Silkworm Domestication

“…Genes related to domesticated behaviors are usually under selection. Based on the published genome-wide SNPs of 137 domestic silkworm and 7 wild silkworm strains ( Xiang et al, 2018 ), we calculated the selection signatures ( Fst and π) of the chromosomes harboring the candidate regions related to climbing and mimicry to screen candidate domesticated genes as described previously ( Zhu et al, 2019a ). The allele frequency for each site was calculated with the reads supporting the reference genotype divided by the total covered reads.…”