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Comprehensive silk gland multi-omics comparison illuminates two alternative mechanisms in silkworm heterosis.

ABSTRACT: Heterosis is a common phenomenon in plants and animals with diverse underlying mechanisms. Here, we applied two widely used silkworm hybrid systems and performed multi-omics analysis to identify possible intrinsic associations between different hybrid strategies and epigenetic mechanisms with silkworm heterosis. We found significant differences in the silk gland transcriptomic landscape between the two systems, including differentially expressed genes and expression patterns in the hybrid offspring compared to their parents. In the quaternary hybrid system, hybrid vigor was primarily due to up-regulated genes and the parent-dominant up-regulated expression pattern, involving multiple transport processes, cellular nitrogen compound catabolism, glucose metabolism, and tricarboxylic acid cycle. In the binary system, hybrid vigor was mainly due to the down-regulated genes and transgressively down-regulated expression pattern, mainly involving basic nitrogen synthesis metabolism and body function. We also demonstrated that DNA methylation may affect hybrid vigor by regulating the expression of several heterosis-related genes. Thus, this study revealed two alternative mechanisms that may contribute to silkworm heterosis, both of which facilitate the efficient utilization of energy and nitrogen for silk production.

SUBMITTER: Xu H

PROVIDER: S-EPMC9336454 | biostudies-literature | 2022 Jul

REPOSITORIES: biostudies-literature

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Comprehensive silk gland multi-omics comparison illuminates two alternative mechanisms in silkworm heterosis.

Xu Han H Chen Lei L Tong Xiao-Ling XL Hu Hai H Liu Li-Yuan LY Liu Gui-Chun GC Zhu Ya-Nan YN Zhao Ruo-Ping RP Wang Wen W Dai Fang-Yin FY Li Xin X Xiang Hui H

Zoological research 20220701 4

Heterosis is a common phenomenon in plants and animals with diverse underlying mechanisms. Here, we applied two widely used silkworm hybrid systems and performed multi-omics analysis to identify possible intrinsic associations between different hybrid strategies and epigenetic mechanisms with silkworm heterosis. We found significant differences in the silk gland transcriptomic landscape between the two systems, including differentially expressed genes and expression patterns in the hybrid offspr ...[more]

PMID: 35726584

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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.

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.

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Comprehensive silk gland multi-omics comparison illuminates two alternative mechanisms in silkworm heterosis.

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Comprehensive silk gland multi-omics comparison illuminates two alternative mechanisms in silkworm heterosis.

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