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

Zool Res. 2022 Jul 18;43(4):585-596. doi: 10.24272/j.issn.2095-8137.2022.065.

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.

杂种优势是动物和植物中的普遍存在的一种现象,其潜在机制复杂多样。该研究以两种常用的家蚕杂交系统为模型,利用多组学技术,以回答两个问题:不同杂交策略之间是否存在可能的内在关联;表观遗传机制对家蚕杂种优势的贡献。我们证明了两个杂交系统之间的丝腺转录组格局存在显著差异,表现在杂交优势后代与亲本相比的基因表达水平差异和表达模式差异。四元杂交系统的杂交优势主要是由上调基因和亲本显性上调表达模式基因引起,这些基因主要参与多种转运过程、细胞氮化合物分解代谢、葡萄糖代谢过程以及三羧酸循环(TCA循环)。与此相反,二元系统的杂种优势则是由下调基因和超亲下调表达模式基因引起,这些基因主要参与机体基本的氮合成代谢和运作。该研究还证明了 DNA 甲基化可以通过调节一些杂种优势相关基因的表达来促进杂种优势。总的来说,我们阐明了两种可能有助于蚕杂种优势形成的备选机制,这两种机制都是有利于提高能源和氮的利用效率来提高蚕丝产量。.

Keywords: Heterosis; hybrid systems; multi-omics; silk production; silkworm.

MeSH terms

  • Animals
  • Bombyx* / genetics
  • Gene Expression Profiling / veterinary
  • Gene Expression Regulation, Plant
  • Hybrid Vigor* / genetics
  • Nitrogen
  • Silk / genetics

Substances

  • Silk
  • Nitrogen

Associated data

  • BioProject/PRJNA770282

Grants and funding

This work was supported by the National Natural Science Foundation of China (31371286, 32070411, 81872299, 31830094, U20A2058), Guangzhou Science Technology Project (201904010007), Shenzhen Science and Technology Program (JCYJ20190807160011600, JCYJ20210324124808023), and Guangdong Provincial Key Laboratory of Insect Developmental Biology and Applied Technology (GDKCFY2101)