Common strategies in silkworm disease resistance breeding research.

Bombyx mori CRISPR system gene editing pathogen transgenic technology

Journal

Pest management science
ISSN: 1526-4998
Titre abrégé: Pest Manag Sci
Pays: England
ID NLM: 100898744

Informations de publication

Date de publication:
Jul 2023
Historique:
revised: 09 02 2023
received: 13 09 2022
accepted: 19 03 2023
medline: 2 6 2023
pubmed: 20 3 2023
entrez: 19 3 2023
Statut: ppublish

Résumé

The silkworm, which is considered a model invertebrate organism, was the first insect used for silk production in human history and has been utilized extensively throughout its domestication. However, sericulture has been plagued by various pathogens that have  caused significant economic losses. To enhance the resistance of a host to its pathogens,numerous strategies have been developed. For instance, gene-editing techniques have been applied to a wide range of organisms, effectively solving a variety of experimental problems. This review focuses on several common silkworm pests and their pathogenic mechanisms, with a particular emphasis on breeding for disease resistance to control multiple types of silkworm diseases. The review also compares the advantages and disadvantages of transgenic technology and gene-editing systems. Finally, the paper provides a brief summary of current strategies used in breeding silkworm disease resistance, along with a discussion of the establishment of existing technologies and their future application prospects. © 2023 Society of Chemical Industry.

Identifiants

pubmed: 36935349
doi: 10.1002/ps.7454
doi:

Types de publication

Journal Article Review

Langues

eng

Sous-ensembles de citation

IM

Pagination

2287-2298

Subventions

Organisme : National Key R&D Program of China
ID : 2022YFD1601908
Organisme : Supported by the earmarked fund for CARS (CARS-18)
Organisme : Natural Science Foundation of Chongqing
ID : cstc2019jcyj-msxmX0096
Organisme : National Natural Science Foundation of China
ID : 31902214
Organisme : National Natural Science Foundation of China
ID : 31872427

Informations de copyright

© 2023 Society of Chemical Industry.

Références

Kang GPJAJB, Overview of silkworm pathology in China. African Journal of Biotechnology 10:18046-18056 (2011).
Blissard GW and Theilmann DA, Baculovirus entry and egress from insect cells. Annu Rev Virol 5:113-139 (2018).
Yang L, Sun Y, Chang M, Zhang Y, Qiao H, Huang S et al., RNA interference-mediated knockdown of Bombyx mori Haemocyte-specific Cathepsin L (cat L)-like cysteine protease gene increases bacillus thuringiensis kurstaki toxicity and reproduction in insect cadavers. Toxins 14:394 (2022).
Xu G, Tian Y, Peng Y and Zheng S, Knock down of target genes by RNA interference in the embryos of lepidopteran insect, Bombyx mori. STAR Protocols 3:101219 (2022).
Su ZH, Gao YH, Cheng S, Wen Y, Tang XD, Li MW et al., Identification of the in vitro antiviral effect of BmNedd2-like caspase in response to Bombyx mori nucleopolyhedrovirus infection. J Invertebr Pathol 183:107625 (2021).
Lee YS, Nakahara K, Pham JW, Kim K, He Z, Sontheimer EJ et al., Distinct roles for drosophila Dicer-1 and Dicer-2 in the siRNA/miRNA silencing pathways. Cell 117:69-81 (2004).
tenOever BR, The evolution of antiviral defense systems. Cell Host Microbe 19:142-149 (2016).
Kim VN, Han J and Siomi MC, Biogenesis of small RNAs in animals. Nat Rev Mol Cell Biol 10:126-139 (2009).
Marques JT and Imler JL, The diversity of insect antiviral immunity: insights from viruses. Curr Opin Microbiol 32:71-76 (2016).
Bronkhorst AW and van Rij RP, The long and short of antiviral defense: small RNA-based immunity in insects. Curr Opin Virol 7:19-28 (2014).
Kolliopoulou A, Santos D, Taning CNT, Wynant N, Vanden Broeck J, Smagghe G et al., PIWI pathway against viruses in insects. Wiley Interdiscip Rev RNA 10:e1555 (2019).
Zhao P, Xia F, Jiang L, Guo H, Xu G, Sun Q et al., Enhanced antiviral immunity against Bombyx mori cytoplasmic polyhedrosis virus via overexpression of peptidoglycan recognition protein S2 in transgenic silkworms. Dev Comp Immunol 87:84-89 (2018).
Dong Z, Zheng N, Hu C, Huang X, Chen P, Wu Q et al., Genetic bioengineering of overexpressed guanylate binding protein family BmAtlastin-n enhances silkworm resistance to Nosema bombycis. Int J Biol Macromol 172:223-230 (2021).
Xu J, Luo X, Fang G, Zhan S, Wu J, Wang D et al., Transgenic expression of antimicrobial peptides from black soldier fly enhance resistance against entomopathogenic bacteria in the silkworm, Bombyx mori. Insect Biochem Mol Biol 127:103487 (2020).
Thomas KR, Folger KR and Capecchi MR, High frequency targeting of genes to specific sites in the mammalian genome. Cell 44:419-428 (1986).
Kim YG, Cha J and Chandrasegaran S, Hybrid restriction enzymes: zinc finger fusions to Fok I cleavage domain. Proc Natl Acad Sci U S A 93:1156-1160 (1996).
Takasu Y, Kobayashi I, Beumer K, Uchino K, Sezutsu H, Sajwan S et al., Targeted mutagenesis in the silkworm Bombyx mori using zinc finger nuclease mRNA injection. Insect Biochem Mol Biol 40:759-765 (2010).
Bogdanove AJ, Schornack S and Lahaye T, TAL effectors: finding plant genes for disease and defense. Curr Opin Plant Biol 13:394-401 (2010).
Pavletich NP and Pabo CO, Zinc finger-DNA recognition: crystal structure of a Zif268-DNA complex at 2.1 a. Science (New York, NY) 252:809-817 (1991) Zinc Finger-DNA Recognition: Crystal Structure of a Zif268-DNA Complex at 2.1 Å.
Ye L, You Z, Qian Q, Zhang Y, Che J, Song J et al., TAL effectors mediate high-efficiency transposition of the piggyBac transposon in silkworm Bombyx mori L. Sci Rep 5:17172 (2015).
Jansen R, Embden JD, Gaastra W and Schouls LM, Identification of genes that are associated with DNA repeats in prokaryotes. Mol Microbiol 43:1565-1575 (2002).
Sasnauskas G and Siksnys V, CRISPR adaptation from a structural perspective. Curr Opin Struct Biol 65:17-25 (2020).
He L, St John James M, Radovcic M, Ivancic-Bace I and Bolt EL, Cas3 protein-a review of a multi-tasking machine. Genes 11:208 (2020).
Lee H and Sashital DG, Creating memories: molecular mechanisms of CRISPR adaptation. Trends Biochem Sci 47:464-476 (2022).
Tang TH, Bachellerie JP, Rozhdestvensky T, Bortolin ML, Huber H, Drungowski M et al., Identification of 86 candidates for small non-messenger RNAs from the archaeon Archaeoglobus fulgidus. Proc Natl Acad Sci U S A 99:7536-7541 (2002).
Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA and Charpentier E, A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science (New York, NY) 337:816-821 (2012).
Horodecka K and Düchler M, CRISPR/Cas9: principle, applications, and delivery through extracellular vesicles. Int J Mol Sci 22:6072 (2021).
Lim JM and Kim HH, Basic principles and clinical applications of CRISPR-based genome editing. Yonsei Med J 63:105-113 (2022).
Wang SW, Gao C, Zheng YM, Yi L, Lu JC, Huang XY et al., Current applications and future perspective of CRISPR/Cas9 gene editing in cancer. Mol Cancer 21:57 (2022).
Makarova KS, Wolf YI, Alkhnbashi OS, Costa F, Shah SA, Saunders SJ et al., An updated evolutionary classification of CRISPR-Cas systems. Nat Rev Microbiol 13:722-736 (2015).
Mohanraju P, Makarova KS, Zetsche B, Zhang F, Koonin EV and van der Oost J, Diverse evolutionary roots and mechanistic variations of the CRISPR-Cas systems. Science (New York, NY) 353:aad5147 (2016).
Dong Z, Qin Q, Hu Z, Zhang X, Miao J, Huang L et al., CRISPR/Cas12a mediated genome editing enhances Bombyx mori resistance to BmNPV. Front Bioeng Biotechnol 8:841 (2020).
Safari F, Zare K, Negahdaripour M, Barekati-Mowahed M and Ghasemi Y, CRISPR Cpf1 proteins: structure, function and implications for genome editing. Cell Biosci 9:36 (2019).
Abudayyeh OO, Gootenberg JS, Konermann S, Joung J, Slaymaker IM, Cox DB et al., C2c2 is a single-component programmable RNA-guided RNA-targeting CRISPR effector. Science (New York, NY) 353:aaf5573 (2016).
Gootenberg JS, Abudayyeh OO, Lee JW, Essletzbichler P, Dy AJ, Joung J et al., Nucleic acid detection with CRISPR-Cas13a/C2c2. Science (New York, NY). 356:438-442 (2017).
Liu L, Li X, Wang J, Wang M, Chen P, Yin M et al., Two distant catalytic sites are responsible for C2c2 RNase activities. Cell 168:121-134 e12 (2017).
Mao F, Zhu Y, Gao X, Chen X, Ngowo J, Miao M et al., HSP/HSC70 activity is required for Bombyx mori nucleopolyhedrovirus replication at the early infectious phase. Microb Pathog 153:104647 (2021).
Hashimoto Y, Kawase S, Characteristics of structural proteins of infectious flacherie virus from the silkworm, Bombyx mori. Journal of Invertebrate Pathology 41:68-76 (1983).
Chen S, Hou C, Bi H, Wang Y, Xu J, Li M et al., Transgenic clustered regularly interspaced short palindromic repeat/Cas9-mediated viral gene targeting for antiviral therapy of Bombyx mori Nucleopolyhedrovirus. J Virol 91:e02465-16 (2017).
Isobe R, Kojima K, Matsuyama T, Quan GX, Kanda T, Tamura T et al., Use of RNAi technology to confer enhanced resistance to BmNPV on transgenic silkworms. Arch Virol 149:1931-1940 (2004).
Kanginakudru S, Royer C, Edupalli SV, Jalabert A, Mauchamp B, Prasad SV et al., Targeting ie-1 gene by RNAi induces baculoviral resistance in lepidopteran cell lines and in transgenic silkworms. Insect Mol Biol 16:635-644 (2007).
Jiang L, Zhao P, Wang G, Cheng T, Yang Q, Jin S et al., Comparison of factors that may affect the inhibitory efficacy of transgenic RNAi targeting of baculoviral genes in silkworm Bombyx mori. Antiviral Res 97:255-263 (2013).
Jiang L, Wang G, Cheng T, Yang Q, Jin S, Lu G et al., Resistance to Bombyx mori nucleopolyhedrovirus via overexpression of an endogenous antiviral gene in transgenic silkworms. Arch Virol 157:1323-1328 (2012).
Yashwant RS, Thomas DS, Manoharan C, Roy G, Kunjupillai V, Mishra RK et al., Transgenic silkworms overexpressing relish and expressing Drosomycin confer enhanced immunity to multiple pathogens. Mol Biotechnol 64:711-724 (2022).
Liu Y, Ma S, Chang J, Zhang T, Chen X, Liang Y et al., Programmable targeted epigenetic editing using CRISPR system in Bombyx mori. Insect Biochem Mol Biol 110:105-111 (2019).
Brady D, Saviane A, Cappellozza S and Sandrelli F, An efficient workflow for screening and stabilizing CRISPR/Cas9-mediated mutant lines in Bombyx mori. Methods Protocols 4:4 (2020).
Dong ZQ, Chen TT, Zhang J, Hu N, Cao MY, Dong FF et al., Establishment of a highly efficient virus-inducible CRISPR/Cas9 system in insect cells. Antiviral Res 130:50-57 (2016).
Dong Z, Huang L, Dong F, Hu Z, Qin Q, Long J et al., Establishment of a baculovirus-inducible CRISPR/Cas9 system for antiviral research in transgenic silkworms. Appl Microbiol Biotechnol 102:9255-9265 (2018).
Dong Z, Qin Q, Hu Z, Chen P, Huang L, Zhang X et al., Construction of a one-vector multiplex CRISPR/Cas9 editing system to inhibit Nucleopolyhedrovirus replication in silkworms. Virol Sin 34:444-453 (2019).
Dong Z, Dong F, Yu X, Huang L, Jiang Y, Hu Z et al., Excision of Nucleopolyhedrovirus form transgenic silkworm using the CRISPR/Cas9 system. Front Microbiol 9:209 (2018).
Pan X, Luo Y, Liao N, Zhang Y, Xiao M, Chen P et al., CRISPR/Cpf1 multiplex genome editing system increases silkworm tolerance to BmNPV. Int J Biol Macromol 200:566-573 (2022).
Dong ZQ, Hu N, Dong FF, Chen TT, Jiang YM, Chen P et al., Baculovirus LEF-11 hijack host ATPase ATAD3A to promote virus multiplication in Bombyx mori cells. Sci Rep 7:46187 (2017).
Dong Z, Qin Q, Zhang X, Li K, Chen P and Pan M, Development of a CRISPR/Cpf1 gene editing system in silkworm Bombyx mori. Sheng wu gong cheng xue bao Chin J Biotechnol 37:4342-4350 (2021).
Lü P, Pan Y, Yang Y, Zhu F, Li C, Guo Z et al., Discovery of anti-viral molecules and their vital functions in Bombyx mori. J Invertebr Pathol 154:12-18 (2018).
Bao YY, Chen LB, Wu WJ, Zhao D, Wang Y, Qin X et al., Direct interactions between bidensovirus BmDNV-Z proteins and midgut proteins from the virus target Bombyx mori. 280:939-949 (2013).
Zhu F, Li D, Song D, Huo S, Ma S, Lü P et al., Glycoproteome in silkworm Bombyx mori and alteration by BmCPV infection. J Proteomics 222:103802 (2020).
Sun Z, Lu Y, Zhang H, Kumar D, Liu B, Gong Y et al., Effects of BmCPV infection on silkworm Bombyx mori intestinal bacteria. PloS one 11:e0146313 (2016).
Pan ZH, Gao K, Hou CX, Wu P, Qin GX, Geng T et al., dsRNA interference on expression of a RNA-dependent RNA polymerase gene of Bombyx mori cytoplasmic polyhedrosis virus. Gene 565:56-61 (2015).
Kay S, Hahn S, Marois E, Hause G and Bonas UJS, A bacterial effector acts as a plant transcription factor and induces a cell size regulator. 318:648-651 (2007).
Dong Z, Wu Q, Long J, Lu B, Zheng N, Hu C et al., Silver nanoparticles are effective in controlling microsporidia. Mater Sci Eng C Mater Biol Appl 125:112106 (2021).
Franzen C, How do microsporidia invade cells? Folia Parasitol (Praha) 52:36-40 (2005).
Didier ES, Didier PJ, Snowden KF and Shadduck JA, Microsporidiosis in mammals. Microbes Infect 2:709-720 (2000).
Li Z, Wang Y, Wang L and Zhou Z, Molecular and biochemical responses in the midgut of the silkworm, Bombyx mori, infected with Nosema bombycis. Parasit Vectors 11:147 (2018).
Dong Z, Zheng N, Hu C, Deng B, Fang W, Wu Q et al., Nosema bombycis microRNA-like RNA 8 (Nb-milR8) increases fungal pathogenicity by modulating BmPEX16 gene expression in its host, Bombyx mori. Microbiol Spectrum 9:e0104821 (2021).
Dong Z, Long J, Huang L, Hu Z, Chen P, Hu N et al., Construction and application of an HSP70 promoter-inducible genome editing system in transgenic silkworm to induce resistance to Nosema bombycis. Appl Microbiol Biotechnol 103:9583-9592 (2019).
Barber GN, STING: infection, inflammation and cancer. Nat Rev Immunol 15:760-770 (2015).
Hua X, Xu W, Ma S and Xia Q, STING-dependent autophagy suppresses Nosema bombycis infection in silkworms Bombyx mori. Dev Compar Immunol 115:103862 (2021).
Varada B, Pradeep ANR, Awasthi AK and Ponnuvel KM, Modulation of NPV gene expression pattern and retention of RNAi- based antiviral activity in inbred transgenic silkworm. International journal of tropical insect. Science 2020:483-491 (2020).
Hu C, Dong Z, Deng B, Wu Q, Chen P, Lu C et al., MicroRNA-6498-5p inhibits Nosema bombycis proliferation by downregulating BmPLPP2 in Bombyx mori. J Fungi (Basel, Switzerland) 7(12):1051 (2021).
Chen S, Dong Z, Ren X, Zhao D, Zhang Y, Tang M et al., Proteomic identification of immune-related silkworm proteins involved in the response to bacterial infection. J Insect Sci 19(4):13 (2019).
Lin P, Cheng T, Jin S, Wu Y, Fu B, Long R et al., PC, a novel Oral insecticidal toxin from bacillus bombysepticus involved in host lethality via APN and BtR-175. Sci Rep 5:11101 (2015).
Jiang L, Insights into the antiviral pathways of the silkworm Bombyx mori. Front Immunol 12:639092 (2021).
Jiang L and Xia Q, The progress and future of enhancing antiviral capacity by transgenic technology in the silkworm Bombyx mori. Insect Biochem Mol Biol 48:1-7 (2014).
Ito K, Ponnuvel KM and Kadono-Okuda K, Host response against virus infection in an insect: Bidensovirus infection effect on silkworm (Bombyx mori). Antioxidants (Basel) 10(4):522 (2021).
Behan FM, Iorio F, Picco G, Gonçalves E, Beaver CM, Migliardi G et al., Prioritization of cancer therapeutic targets using CRISPR-Cas9 screens. Nature 568:511-516 (2019).
Chang J, Wang R, Yu K, Zhang T, Chen X, Liu Y et al., Genome-wide CRISPR screening reveals genes essential for cell viability and resistance to abiotic and biotic stresses in Bombyx mori. Genome Res 30:757-767 (2020).
Yuan Y, Zhu F, Xiao R, Ge Q, Tang H, Kong M et al., Increased expression of suppressor of cytokine signaling 2 (BmSOCS2) is correlated with suppression of Bombyx mori nucleopolyhedrovirus replication in silkworm larval tissues and cells. J Invertebr Pathol 174:107419 (2020).
Awan MJA, Pervaiz K, Rasheed A, Amin I, Saeed NA, Dhugga KS et al., Genome edited wheat- current advances for the second green revolution. Biotechnol Adv 60:108006 (2022).
Liang F, Zhang Y, Li L, Yang Y, Fei JF, Liu Y et al., SpG and SpRY variants expand the CRISPR toolbox for genome editing in zebrafish. Nat Commun 13:3421 (2022).
Chen Y, Hu Y, Wang X, Luo S, Yang N, Chen Y et al., Synergistic engineering of CRISPR-Cas nucleases enables robust mammalian genome editing. Innovation (Cambridge (Mass)) 3:100264 (2022).
Singh CP, Viral-encoded microRNAs in host-pathogen interactions in silkworm. MicroRNA (Shariqah, United Arab Emirates) 10:3-13 (2021).
Singh CP, Singh J and Nagaraju J, A baculovirus-encoded MicroRNA (miRNA) suppresses its host miRNA biogenesis by regulating the exportin-5 cofactor ran. J Virol 86:7867-7879 (2012).
Dong ZQ, Hu ZG, Li HQ, Jiang YM, Cao MY, Chen P et al., Construction and characterization of a synthetic Baculovirus-inducible 39K promoter. J Biol Eng 12:30 (2018).

Auteurs

Kejie Li (K)

State Key Laboratory of Resource Insects, Southwest University, Chongqing, China.
The First Affiliated Hospital of Chongqing Medical and pharmaceutical College, Chongqing, China.

Zhanqi Dong (Z)

State Key Laboratory of Resource Insects, Southwest University, Chongqing, China.
Key Laboratory of Sericultural Biology and Genetic Breeding, Ministry of Agriculture and Rural Affairs, Southwest University, Chongqing, China.

Minhui Pan (M)

State Key Laboratory of Resource Insects, Southwest University, Chongqing, China.
Key Laboratory of Sericultural Biology and Genetic Breeding, Ministry of Agriculture and Rural Affairs, Southwest University, Chongqing, China.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH