Artificial selection on storage protein 1 possibly contributes to increase of hatchability during silkworm domestication
Artificial selection on storage protein 1 possibly contributes to increase of hatchability during silkworm domestication
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DOI：
10.1371/journal.pgen.1007616
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发表时间：
2019-01
期刊：
影响因子：
4.5
通讯作者：
Yanan Zhu;Lizhi Wang;Cencen Li;Yong Cui;Man Wang;Yong-Jian Lin;Ruoping Zhao;Wen Wang;
中科院分区：
文献类型：
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作者：
Yanan Zhu;Lizhi Wang;Cencen Li;Yong Cui;Man Wang;Yong-Jian Lin;Ruoping Zhao;Wen Wang;
像其他驯养动物一样，氮资源的有效利用对唯一完全驯化的昆虫——蚕也很重要。破译人工选择如何作用于家蚕基因组，以提高氮素资源的利用率和推进人类偏好的驯化性状，将为理解达尔文驯化进化理论的一般规律提供独特的昆虫模型线索。储存蛋白（Storage proteins, SPs）属于血青素超家族，在昆虫的变态和繁殖过程中主要作为氨基酸和氮的来源。本研究通过对家蚕基因组的blast搜索和家蚕SPs人工选择特征的进一步筛选，发现了一个候选驯化基因，即富蛋氨酸储存蛋白1 (SP1)，该基因与其他储存蛋白明显不同，在家蚕卵中表达增加。通过CRISPR/Cas9技术敲除SP1，导致卵的孵化率急剧下降，但对产卵没有明显影响，与家蚕相比，对野生家蚕的影响相似。敲除SP1不影响幼虫的发育和变态。综合比较转录组显示，与SP1突变体和野生家蚕相比，家蚕卵黄蛋白原、绒毛膜和细胞外基质（ECM）相互作用途径中的结构组分、叶酸生物合成酶以及激素合成酶的编码基因表达显著增加。此外，与野生家蚕相比，家蚕核糖体和酰胺结构成分丰富的基因以及多肽生物合成基因的表达也普遍上调。本研究表明，人工选择可能直接作用于氮资源蛋白，通过激素信号介导的调节网络和核糖体的激活，进一步影响鸡蛋营养和蛋壳形成，从而改善驯化过程中的生物合成和提高孵化率。这些发现从氮和氨基酸资源的角度对人工选择和家蚕育种有了新的认识。
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.