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Genome-wide CRISPR screening reveals key genes and pathways associated with 20-hydroxyecdysone signal transduction in the silkworm(Bombyx mori)

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Insect Science 2024年第1期31卷 47-58页

作者： Hao Sun Jingya Chen Ruolin Wang Dan Liu Na Zhang Tong Zhang Ling Jia Sanyuan Ma Qingyou Xia State Key Laboratory of silkworm Genome Biology Southwest UniversityChongqingChina Biological Science Research Center Southwest UniversityChongqingChina

Metamorphosis is a complex developmental process involving multiple pathways and a large number of genes that are regulated by juvenile hormone(JH)and 20-hydroxyecdysone(20E).Despite important progress in understanding various aspects of silkworm biology,the hormone signaling pathway in the silkworm remains poorly understood.Genome-wide screening using clustered regularly interspaced short palindromic repeats(CRISPR)/CRISPR-associated protein 9(Cas9)-based libraries has recently emerged as a novel method for analyzing genome function,enabling further research into essential genes,drug targets,and virus-host interaction.Previously,we constructed a genome-wide CRISPR/Cas9-based library of the silkworm(Bombyx mori)and successfully revealed the genes involved in biotic or abiotic stress factor responses.In this study,we used our silkworm CRISPR library and large-scale genome-wide screening to analyze the key genes in the silkworm 20E signaling pathway and their mechanisms of action.Functional annotation showed that 20E regulates key proteins in processes that mainly occur in the cytoplasm and nucleus.Pathway enrichment analysis showed that 20E can activate phosphorylation and may affect innate immunity,interfere with intracellular nutrition and energy metabolism,and eventually cause cell apoptosis.The screening results were experimentally validated by generating cells with knockout alleles of the relevant genes,which had increased tolerance to 20E.Our findings provide a panoramic overview of signaling in response to 20E in the silkworm,underscoring the utility of genome-wide CRISPR mutant libraries in deciphering hormone signaling pathways and the mechanisms that regulate metamorphosis in insects.

关键词： CRISPR/Cas9 CRISPR library screening ecdysone 20E signal transduction silkworm whole genome editing

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破译pH值和金属离子编程的家蚕纺丝机制

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Science Bulletin 2024年第6期69卷 792-802页

作者：宋凯王叶菁董文杰李珍珍夏庆友朱平何华伟 Integrative Science Center of Germplasm Creation in Western China(CHONGQING)Science City Biological Science Research CenterSouthwest UniversityChongqing 400715China National Laboratory of Biomacromolecules CAS Center for Excellence in BiomacromoleculesInstitute of BiophysicsChinese Academy of SciencesBeijing 100101China Chongqing Key Laboratory of Sericultural Science Chongqing Engineering and Technology Research Center for Novel Silk MaterialsSouthwest UniversityChongqing 400715China University of Chinese Academy of Sciences Beijing 100049China Chongqing Key Laboratory of Soft-Matter Material Chemistry and Function Manufacturing Chongqing 400715China

Silk is one of the toughest fibrous materials known despite spun at ambient temperature and pressure with water as a solvent.It is a great challenge to reproduce high-performance artificial fibers comparable to natural silk by bionic for the incomplete understanding of silkworm spinning in vivo.Here,we found that amphipol and digitonin stabilized the structure of natural silk fibroin(NSF)by a large-scale screening in vitro,and then studied the close-to-native ultrastructure and hierarchical assembly of NSF in the silk gland lumen.Our study showed that NSF formed reversible flexible nanofibrils mainly composed of random coils with a sedimentation coefficient of 5.8 S and a diameter of about 4 nm,rather than a micellar or rod-like structure assembled by the aggregation of globular NSF molecules.Metal ions were required for NSF nanofibril formation.The successive p H decrease from posterior silk gland(PSG)to anterior silk gland(ASG)resulted in a gradual increase in NSF hydrophobicity,thus inducing the sol-gelation transition of NSF nanofibrils.NSF nanofibrils were randomly dispersed from PSG to ASG-1,and self-assembled into anisotropic herringbone patterns at ASG-2 near the spinneret ready for silkworm spinning.Our findings reveal the controlled self-assembly mechanism of the multi-scale hierarchical architecture of NSF from nanofibrils to herringbone patterns programmed by metal ions and p H gradient,which provides novel insights into the spinning mechanism of silk-secreting animals and bioinspired design of high-performance fibers.

关键词： Natural silk fibroin Nanofibril Self-assembly silkworm Cryo-EM

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

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Zoological Research 2022年第4期43卷 585-596页

作者： Han Xu Lei Chen Xiao-Ling Tong Hai Hu Li-Yuan Liu Gui-Chun Liu Ya-Nan Zhu Ruo-Ping Zhao Wen Wang Fang-Yin Dai Xin Li Hui Xiang School of Medicine Shenzhen Campus of Sun Yat-Sen UniversityShenzhenGuangdong 518107China Guangdong Provincial Key Laboratory of Insect Developmental Biology and Applied Technology Guangzhou Key Laboratory of Insect Development Regulation and Application ResearchInstitute of Insect Science and TechnologySchool of Life SciencesSouth China Normal UniversityGuangzhouGuangdong 510631China School of Ecology and Environment Northwestern Polytechnical UniversityXi’anShaanxi 710072China State Key Laboratory of silkworm Genome Biology Key Laboratory of Sericultural Biology and Genetic BreedingMinistry of Agriculture and Rural AffairsCollege of BiotechnologySouthwest UniversityChongqing 400715China State Key Laboratory of Genetic Resources and Evolution Kunming Institute of ZoologyChinese Academy of SciencesKunmingYunnan 650223China

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 upregulated genes and the parent-dominant upregulated 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.

关键词： Heterosis silkworm Hybrid systems Multi-omics Silk production

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U1 small nuclear ribonucleoprotein is essential for early larval development in silkworm, Bombyx mori

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Insect Science 2022年第2期29卷 379-387页

作者： Xiaoqian Zhang Dehong Yang Xu Yang Xinran Zhang Yong Zhang Yongping Huang Shengxiang Zhang Zulian Liu College Forestry Shangdong Agriculture UniversityShangdong ProvinceTaianChina Key Laboratory of Insect Developmental and Evolutionary Biology Center for Excellence in Molecular Plant SciencesShanghai Institute of Plant Physiology and EcologyChinese Academy of SciencesShanghaiChina CAS Center for Excellence in Biotic Interactions University of Chinese Academy of SciencesBeijingChina Soochow University SuzhouJiangsu ProvinceChina

U1 small nuclear ribonucleoproteins(U1 snRNP)associates with 5ʹsplice sites in the form of ribonucleoprotein particles and is highly conserved among species.The physiological functions of U1 snRNP in a lepidopteran model insect Bombyx mori is mostly unknown.Here,we showed that U1 snRNP plays an important role in the development of silkworm.Knockout of U1 snRNP in silkworm showed either delayed or stationary 1st instar larva development compared with the wild-type group.U1 snRNP deletion mutants exhibited abnormal cellular phenotypes with enlarged cell nucleus,scant cytoplasm and enlarged nuclei.RNA-seq analysis revealed that genes involved in metabolic pathway,biosynthesis of secondary metabolites and steroid hormone biosynthesis were significantly affected by U1 snRNP depletion.Taken together,our study suggests that U1 snRNP homeostasis plays an important role in silkworm development.

关键词： CRISPR/Cas9 development ecdysone silkworm U1 snRNP

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A secreted phospholipase A_(2) (BmsPLA_(2)) regulates melanization of immunity through BmDDC in the silkworm Bombyx mori

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Insect Science 2023年第6期30卷 1579-1594页

作者： Tian Li Gemin Wang Wei He Guiqin Li Chunyang Wang Jiamei Zhao Pan Chen Meiwei Guo Ping Chen College of Sericulture Textile and Biomass SciencesSouthwest UniversityChongqingChina Drug Discovery Research Center Southwest Medical UniversityLuzhouChina State Key Laboratory of silkworm Genome Biology Southwest UniversityChongqingChina

Insect immune-associated phospholipase A_(2) (PLA_(2)) is an important target of pathogen invasion. Melanization, an effective defense response, has significant correlations with other immune responses to coordinate immune attack against invaders. However, the effect of PLA_(2) on melanization has not yet been reported in insects or other arthropods. In this work, we cloned a PLA_(2) gene (BmsPLA_(2)), and its protein had characteristic features of secreted PLA_(2) (sPLA_(2)). After injection of bacteria, BmsPLA_(2) expression and sPLA_(2) activity in hemolymph significantly increased. BmsPLA_(2) fluorescence was transferred from the cytoplasm to the cell membranes of circulating hemocytes. These results indicated that BmsPLA_(2) was related to hemolymph immunity in silkworms. Interestingly, reducing BmsPLA_(2) by RNA interference decreased melanosis (melanistic hemocytes) levels in vivo and in vitro, while BmsPLA_(2) overexpression had the opposite effect. The larval survival and melanization rate in the hemocoel both slowed depending on the PLA_(2) inhibitor dosage. These results demonstrated that BmsPLA_(2) plays a role in melanization during the immune process of silkworms. Surprisingly, the level of BmDDC matched the degree of melanization in various observations. BmDDC expression showed a significant increase, with the peak occurring later than that of BmsPLA_(2) after injection of bacteria, implying that BmsPLA_(2) was activated prior to BmDDC. Moreover, the alteration of BmsPLA_(2) by RNA interference or overexpression led to altered BmDDC levels. These results suggested that BmsPLA_(2) regulates the melanization response in silkworms through BmDDC. Our study proposes a new regulatory mechanism of the melanization response and new directions for understanding the complex immune networks of insects.

关键词： DOPA decarboxylase immunity melanization phospholipase A_(2) silkworm

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Super-strong and Intrinsically Fluorescent silkworm Silk from Carbon Nanodots Feeding

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Nano-Micro Letters 2019年第4期11卷 326-336页

作者： Suna Fan Xiaoting Zheng Qi Zhan Huihui Zhang Huili Shao Jiexin Wang Chengbo Cao Meifang Zhu Dan Wang Yaopeng Zhang State Key Laboratory for Modification of Chemical Fibers and Polymer Materials Shanghai Belt and Road Joint Laboratory of Advanced Fiber and Low-Dimension MaterialsCollege of Materials Science and EngineeringDonghua UniversityShanghai 201620People’s Republic of China State Key Laboratory of Organic-Inorganic Composites Beijing University of Chemical TechnologyBeijing 100029People’s Republic of China School of Chemistry and Chemical Engineering Shandong UniversityJinan 250100People’s Republic of China School of Chemistry and Chemical Engineering Yantai UniversityYantai 264005People’s Republic of China

Fluorescent silk is fundamentally important for the development of future tissue engineering scaffolds.Despite great progress in the preparation of a variety of colored silks,fluorescent silk with enhanced mechanical properties has yet to be explored.In this study,we report on the fabrication of intrinsically super-strong fluorescent silk by feeding Bombyx mori silkworm carbon nanodots(CNDs).The CNDs were incorporated into silk fibroin,hindering the conformation transformation,confining crystallization,and inducing orientation of mesophase.The resultant silk exhibited super-strong mechanical properties with breaking strength of 521.9±82.7 MPa and breaking elongation of 19.2±4.3%,improvements of 55.1%and 53.6%,respectively,in comparison with regular silk.The CNDs-reinforced silk displayed intrinsic blue fluorescence when exposed to 405 nm laser and exhibited no cytotoxic effect on cells,suggesting that multi-functional silks would be potentially useful in bioimaging and other applications.

关键词： silkworm silk Carbon nanodot Mechanical property Fluorescent silk Feeding method

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Structural Analysis of Fibroin Heavy Chain Signal Peptide of silkworm Bombyx mori

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Acta Biochimica et Biophysica Sinica 2006年第7期38卷 507-513页

作者： Sheng-Peng WANG~(1,2)Ting-Qing GUO~1 Xiu-Yang GUO~1 Jun-Ting HUANG~2 Chang-De LU~(1*) 1 Institute of Biochemistry and Cell Biology,Shanghai Institutes for Biological Sciences,Chinese Academy of Sciences,Shanghai 200031,China 2 Sericultural Research Institute,Chinese Academy of Agricultural Sciences,Zhenjiang 212018,China Institute of Biochemistry and Cell Biology Shanghai Institutes for Biological Sciences Chinese Academy of SciencesShanghai 200031 China Sericultural Research Institute Chinese Academy of Agricultural SciencesZhenjiang 212018 China

To study the minimal length required for the secretion of recombinant proteins and silkproteins in posterior silk gland,the signal peptide(SP)of the fibroin heavy chain(FibH)of silkwormBombyx mori was systematically shortened from the C-terminal.Its effect on the secretion of protein wasobserved using enhanced green fluorescent protein(EGFP)as a reporter.Secretion of EGFP fusion proteinswas examined under fluorescence microscope.FibH SPs with lengths of 20,18,16 and 12 a.***.can directthe secretion of the reporter,yet those with lengths of 11, 10, 9, 8 and 1 a.a. can not. When the FibH SP wasshortened to 12a.a., the secretion efficiency was decreased slightly and cleavage occurred within EGFP.When 16a.***.of the FibH SP were used,the secretion of fusion protein was normal and the cleavage sitewas between the Gly-Ser linker and Met,the starting amino acid of EGFP. These findings are applicable forthe expression of foreign proteins in silkworm silk gland.The cleavage site of the SP is discussed andcompared with the predictive results of the SignalP 3.0 online prediction program.

关键词： signal peptide fibroin heavy chain silkworm Bombyx mori rAcMNPV

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Genome-wide identification of target genes for transcription factor BR-C in the silkworm,Bombyx mori

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Insect Science 2021年第6期28卷 1530-1540页

作者： Meng-Pei Guo Wen-Liang Qian Xue-Chuan He Jian Peng Peng Wang Wei-Na Wang Qing-You Xia Dao-Jun Cheng State Key Laboratory of silkworm Genome Biology Biological Science Research CenterSouthwest UniversityChongqing400715China Chongqing Key Laboratory of Sericultural Science Southwest UniversityChongqing400715China

Transcription factor Broad Complex(BR-C)is an ecdysone primary response gene in insects and participates in the regulation of insect growth and development.In this study,we performed a genome-wide identification of BR-C target genes in silkworm(Bombyx mori)using chromatin immunoprecipitation followed by high-throughput sequencing(ChIP-seq).As a result,a total of 1006 BR-C ChIP peaks were identified,and 15%of peaks were located in the promoter regions of 133 protein-coding genes.Functional annotation revealed that these ChIP peak-associated genes,as potential BR-C targets,were enriched in pathways related to biosynthetic process,metabolic process,and development.Transcriptome analysis and quantitative real-time polymerase chain reaction(PCR)examination revealed that developmental changes in expression patterns of a portion of potential BR-C targets,including HR96 and GC-otl,were similar to those of BR-C.ChIP-PCR examination confirmed that BR-C could directly bind to the promoters of potential targets.Further,dual luciferase assays demonstrated that HR96 promoter activity was significantly upregulated following BR-C overexpression,and this upregu-lation was abolished when the binding motif in the promoter was truncated.This study will be helpful for deciphering the regulatory roles of BR-C during insect growth and development.

关键词： BR-C ChIP-seq direct binding silkworm target genes transcriptional regulation

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BmPLA2 containing conserved domain WD40 affects the metabolic functions of fat body tissue in silkworm, Bombyx moil

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Insect Science 2016年第1期23卷 28-36页

作者： Chabungbam Orville Singh Hu-Hu Xin Rui-Ting Chen Mei-Xian Wang Shuang Liang Yan Lu Zi-Zheng Cai Yun-Gen Miao Institute of Sericulture and Apiculture College of Animal Sciences Zhejiang University Hangzhou 310058 China

PLA2 enzyme hydrolyzes arachidonic acid, and other polyunsaturated fatty acids, from the sn-2 position to release free arachidonic acid and a lysophospholipid. Previous studies reported that the PLA2 in invertebrate organisms participates in lipid signaling molecules like arachidonic acid release in immune-associated tissues like hemo- cytes and fat bodies. In the present study, we cloned the BmPLA2 gene from fat body tissue of silkworm Bombyx mori, which has a total sequence of 1.031 kb with a 31.90 kDa pro- tein. In silico results of BmPLA2 indicated that the protein has a putative WD40 conserved domain and its phylogeny tree clustered with Danaus plexippus species. We investigated the transcriptional expression in development stages and tissues. The highest expression of BmPLA2 was screened in fat body among the studied tissues of third day fifth instar larva, with a high expression on third day fifth instar larva followed by a depression of expression in the wandering stage of the fifth instar larva. The expression of BmPLA2 in female pupa was higher than that of male pupa. Our RNAi-mediated gene silencing results showed highest reduction of BmPLA2 expression in post-24 h followed by post-48 and post-72 h. The BmPLA2-RNAi larvae and pupa could be characterized by pharate adult lethality and underdevelopment. The phenotypic characters of fat body cells in RNAi-induced larva im- plied that BmPLA2 affects the metabolic functions of fat body tissue in silkworm Bombyx mori.

关键词： BmPLA2 cloning and expression dsRNA interference fat body tissue silkworm

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Role of juvenile hormone receptor Methoprene-tolerant 1 in silkworm larval brain development and domestication

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Zoological Research 2021年第5期42卷 637-649页

作者： Yong Cui Zu-Lian Liu Cen-Cen Li Xiang-Min Wei Yong-Jian Lin Lang You Zi-Dan Zhu Hui-Min Deng Qi-Li Feng Yong-Ping Huang Hui Xiang Guangdong Provincial Key Laboratory of Insect Developmental Biology and Applied Technology Guangzhou Key Laboratory of Insect Development Regulation and Application ResearchInstitute of Insect Science and TechnologySchool of Life SciencesSouth China Normal UniversityGuangzhouGuangdong 510631China Key Laboratory of Insect Developmental and Evolutionary Biology Institute of Plant Physiology and EcologyShanghai Institutes for Biological SciencesChinese Academy of SciencesShanghai 200032China College of Life Sciences Xinyang Normal UniversityXinyangHenan 464000China

The insect brain is the central part of the neurosecretory system,which controls morphology,physiology,and behavior during the insect’s lifecycle.Lepidoptera are holometabolous insects,and their brains develop during the larval period and metamorphosis into the adult form.As the only fully domesticated insect,the Lepidoptera silkworm Bombyx mori experienced changes in larval brain morphology and certain behaviors during the domestication process.Hormonal regulation in insects is a key factor in multiple processes.However,how juvenile hormone(JH)signals regulate brain development in Lepidoptera species,especially in the larval stage,remains elusive.We recently identified the JH receptor Methoprene tolerant 1(Met1)as a putative domestication gene.How artificial selection on Met1 impacts brain and behavioral domestication is another important issue addressing Darwin’s theory on domestication.Here,CRISPR/Cas9-mediated knockout of Bombyx Met1 caused developmental retardation in the brain,unlike precocious pupation of the cuticle.At the whole transcriptomelevel,theecdysteroid(20-hydroxyecdysone,20 E)signaling and downstream pathways were overactivated in the mutant cuticle but not in the brain.Pathways related to cell proliferation and specialization processes,such as extracellular matrix(ECM)-receptor interaction and tyrosine metabolism pathways,were suppressed in the brain.Molecular evolutionary analysis and in vitro assay identified an amino acid replacement located in a novel motif under positive selection in B.mori,which decreased transcriptional binding activity.The B.mori MET1 protein showed a changed structure and dynamic features,as well as a weakened co-expression gene network,compared with B.mandarina.Based on comparative transcriptomic analyses,we proposed a pathway downstream of JH signaling(i.e.,tyrosine metabolism pathway)that likely contributed to silkworm larval brain development and domestication and highlighted the importance of the biogenic amine system in larval evolution during silkworm domesticat

关键词： Met1 Brain Artificial selection Tyrosine metabolism pathway silkworm

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