Volume 42 Issue 5
Sep.  2021
Turn off MathJax
Article Contents
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. Role of juvenile hormone receptor Methoprene-tolerant 1 in silkworm larval brain development and domestication. Zoological Research, 2021, 42(5): 637-649. doi: 10.24272/j.issn.2095-8137.2021.126
Citation: 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. Role of juvenile hormone receptor Methoprene-tolerant 1 in silkworm larval brain development and domestication. Zoological Research, 2021, 42(5): 637-649. doi: 10.24272/j.issn.2095-8137.2021.126

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

doi: 10.24272/j.issn.2095-8137.2021.126
#Authors contributed equally to this work
Funds:  This work was supported by the National Natural Science Foundation of China (32070411, 31720103916, 31330071, 31672494), Natural Science Foundation of Guangdong Province (2019A1515011012), and Strategic Priority Research Program of the Chinese Academy of Sciences (XDB11010600)
More Information
  • 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 transcriptome level, the ecdysteroid (20-hydroxyecdysone, 20E) 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 domestication.
  • #Authors contributed equally to this work
  • loading
  • [1]
    Abdou MA, He QY, Wen D, Zyaan O, Wang J, Xu JJ, et al. 2011. Drosophila Met and Gce are partially redundant in transducing juvenile hormone action. Insect Biochemistry and Molecular Biology, 41(12): 938−945. doi: 10.1016/j.ibmb.2011.09.003
    [2]
    Agnvall B, Bélteky J, Jensen P. 2017. Brain size is reduced by selection for tameness in Red Junglefowl-correlated effects in vital organs. Scientific Reports, 7(1): 3306. doi: 10.1038/s41598-017-03236-4
    [3]
    Anders S, Pyl PT, Huber W. 2015. HTSeq—a Python framework to work with high-throughput sequencing data. Bioinformatics, 31(2): 166−169. doi: 10.1093/bioinformatics/btu638
    [4]
    Axelsson E, Ratnakumar A, Arendt ML, Maqbool K, Webster MT, Perloski M, et al. 2013. The genomic signature of dog domestication reveals adaptation to a starch-rich diet. Nature, 495(7441): 360−364. doi: 10.1038/nature11837
    [5]
    Bai PP, Xie YF, Shen GM, Wei DD, Wang JJ. 2014. Phenoloxidase and its zymogen are required for the larval-pupal transition in Bactrocera dorsalis (Diptera: Tephritidae). Journal of Insect Physiology, 71: 137−146. doi: 10.1016/j.jinsphys.2014.10.013
    [6]
    Broadie K, Baumgartner S, Prokop A. 2011. Extracellular matrix and its receptors in drosophila neural development. Developmental Neurobiology, 71(11): 1102−1130. doi: 10.1002/dneu.20935
    [7]
    Cayre M, Malaterre J, Scotto-Lomassese S, Aouane A, Strambi C, Strambi A. 2005. Hormonal and sensory inputs regulate distinct neuroblast cell cycle properties in adult cricket brain. Journal of Neuroscience Research, 82(5): 659−664. doi: 10.1002/jnr.20672
    [8]
    Cayre M, Strambi C, Strambi A. 1994. Neurogenesis in an adult insect brain and its hormonal control. Nature, 368(6466): 57−59. doi: 10.1038/368057a0
    [9]
    Champlin DT, Truman JW. 1998. Ecdysteroid control of cell proliferation during optic lobe neurogenesis in the moth Manduca sexta. Development, 125(2): 269−277. doi: 10.1242/dev.125.2.269
    [10]
    Charles JP, Iwema T, Epa VC, Takaki K, Rynes J, Jindra M. 2011. Ligand-binding properties of a juvenile hormone receptor, Methoprene-tolerant. Proceedings of the National Academy of Sciences of the United States of America, 108(52): 21128−21133. doi: 10.1073/pnas.1116123109
    [11]
    Cui Y, Zhu YA, Lin YJ, Chen L, Feng QL, Wang W, et al. 2018. New insight into the mechanism underlying the silk gland biological process by knocking out fibroin heavy chain in the silkworm. BMC Genomics, 19(1): 215. doi: 10.1186/s12864-018-4602-4
    [12]
    Daimon T, Kozaki T, Niwa R, Kobayashi I, Furuta K, Namiki T, et al. 2012. Precocious metamorphosis in the juvenile hormone-deficient mutant of the silkworm, Bombyx mori. PLoS Genetics, 8(3): e1002486. doi: 10.1371/journal.pgen.1002486
    [13]
    Daimon T, Uchibori M, Nakao H, Sezutsu H, Shinoda T. 2015. Knockout silkworms reveal a dispensable role for juvenile hormones in holometabolous life cycle. Proceedings of the National Academy of Sciences of the United States of America, 112(31): E4226−E4235. doi: 10.1073/pnas.1506645112
    [14]
    Ezure T, Suzuki T, Shikata M, Ito M, Ando E. 2010. A cell-free protein synthesis system from insect cells. Methods in Molecular Biology, 607: 31−42.
    [15]
    Fessler LI, Nelson RE, Fessler JH. 1994. Drosophila extracellular matrix. Methods in Enzymology, 245: 271−294.
    [16]
    Fu YF, Sander JD, Reyon D, Cascio VM, Joung JK. 2014. Improving CRISPR-Cas nuclease specificity using truncated guide RNAs. Nature Biotechnology, 32(3): 279−284. doi: 10.1038/nbt.2808
    [17]
    Ghosh S, Chan CK. 2016. Analysis of RNA-seq data using TopHat and cufflinks. Methods in Molecular Biology, 1374: 339−361.
    [18]
    Golan-Mashiach M, Grunspan M, Emmanuel R, Gibbs-Bar L, Dikstein R, Shapiro E. 2012. Identification of CTCF as a master regulator of the clustered protocadherin genes. Nucleic Acids Research, 40(8): 3378−3391. doi: 10.1093/nar/gkr1260
    [19]
    Gross BL, Olsen KM. 2010. Genetic perspectives on crop domestication. Trends in Plant Science, 15(9): 529−537. doi: 10.1016/j.tplants.2010.05.008
    [20]
    Guex N, Peitsch MC. 1997. SWISS-MODEL and the Swiss-Pdb Viewer: an environment for comparative protein modeling. Electrophoresis, 18(15): 2714−2723. doi: 10.1002/elps.1150181505
    [21]
    Huang TT, Hwang JK, Chen CH, Chu CS, Lee CW, Chen CC. 2015. (PS)2: protein structure prediction server version 3.0. Nucleic Acids Research, 43(W1): W338−W342. doi: 10.1093/nar/gkv454
    [22]
    Hwang WY, Fu YF, Reyon D, Maeder ML, Tsai SQ, Sander JD, et al. 2013. Efficient genome editing in zebrafish using a CRISPR-Cas system. Nature Biotechnology, 31(3): 227−229. doi: 10.1038/nbt.2501
    [23]
    Kanost MR, Arrese EL, Cao XL, Chen YR, Chellapilla S, Goldsmith MR, et al. 2016. Multifaceted biological insights from a draft genome sequence of the tobacco hornworm moth, Manduca sexta. Insect Biochemistry and Molecular Biology, 76: 118−147. doi: 10.1016/j.ibmb.2016.07.005
    [24]
    Kayukawa T, Minakuchi C, Namiki T, Togawa T, Yoshiyama M, Kamimura M, et al. 2012. Transcriptional regulation of juvenile hormone-mediated induction of Krüppel homolog 1, a repressor of insect metamorphosis. Proceedings of the National Academy of Sciences of the United States of America, 109(29): 11729−11734. doi: 10.1073/pnas.1204951109
    [25]
    Kayukawa T, Nagamine K, Ito Y, Nishita Y, Ishikawa Y, Shinoda T. 2016. Krüppel homolog 1 inhibits insect metamorphosis via direct transcriptional repression of Broad-Complex, a pupal specifier gene. Journal of Biololgical Chemisty, 291(4): 1751−1762.
    [26]
    Kayukawa T, Jouraku A, Ito Y, Shinoda T. 2017. Molecular mechanism underlying juvenile hormone-mediated repression of precocious larval-adult metamorphosis. Proceedings of the National Academy of Sciences of the United States of America, 114(5): 1057−1062. doi: 10.1073/pnas.1615423114
    [27]
    Kim SR, Kwak W, Kim H, Caetano-Anolles K, Kim KY, Kim SB, et al. 2018. Genome sequence of the Japanese oak silk moth, Antheraea yamamai: the first draft genome in the family Saturniidae. Gigascience, 7(1): gix113.
    [28]
    Kim Y, Davari ED, Sevala V, Davey KG. 1999. Functional binding of a vertebrate hormone, L-3,5,3'-triiodothyronine (T3), on insect follicle cell membranes. Insect Biochemistry and Molecular Biology, 29(10): 943−950. doi: 10.1016/S0965-1748(99)00070-3
    [29]
    Langfelder P, Horvath S. 2008. WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics, 9(1): 559. doi: 10.1186/1471-2105-9-559
    [30]
    Leinwand SG, Scott K. 2021. Juvenile hormone drives the maturation of spontaneous mushroom body neural activity and learned behavior. Neuron, 109(11): 1836−1847.e5. doi: 10.1016/j.neuron.2021.04.006
    [31]
    Li K, Jia QQ, Li S. 2019. Juvenile hormone signaling - a mini review. Insect Science, 26(4): 600−606. doi: 10.1111/1744-7917.12614
    [32]
    Li M, Li DY, Tang Y, Wu FX, Wang JX. 2017. CytoCluster: a cytoscape plugin for cluster analysis and visualization of biological networks. International Journal of Molecular Sciences, 18(9): 1880. doi: 10.3390/ijms18091880
    [33]
    Lin CP, Huang SW, Lai YL, Yen SC, Shih CH, Lu CH, et al. 2008. Deriving protein dynamical properties from weighted protein contact number. Proteins, 72(3): 929−935. doi: 10.1002/prot.21983
    [34]
    Liu SN, Li K, Gao Y, Liu X, Chen WT, Ge W, et al. 2018. Antagonistic actions of juvenile hormone and 20-hydroxyecdysone within the ring gland determine developmental transitions in Drosophila. Proceedings of the National Academy of Sciences of the United States of America, 115(1): 139−144. doi: 10.1073/pnas.1716897115
    [35]
    Love MI, Huber W, Anders S. 2014. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology, 15(12): 550. doi: 10.1186/s13059-014-0550-8
    [36]
    Mignon-Grasteau S, Boissy A, Bouix J, Faure JM, Fisher AD, Hinch GN, et al. 2005. Genetics of adaptation and domestication in livestock. Livestock Production Science, 93(1): 3−14. doi: 10.1016/j.livprodsci.2004.11.001
    [37]
    Nusinovich Y, Ucko S, Ucko H. 2017. How to tame a fox (and Build a Dog): visionary scientists and a siberian tale of jump-started evolution. Science, 358(6368): 1250−1250.
    [38]
    Pennisi E. 2011. The biology of genomes. On the trail of brain domestication genes. Science, 332(6033): 1030−1031.
    [39]
    Riddiford LM. 2020. Rhodnius, golden oil, and Met: a history of juvenile hormone research. Frontiers in Cell and Developmental Biology, 8: 679. doi: 10.3389/fcell.2020.00679
    [40]
    Riddiford LM, Truman JW, Mirth CK, Shen YC. 2010. A role for juvenile hormone in the prepupal development of Drosophila melanogaster. Development, 137(7): 1117−1126. doi: 10.1242/dev.037218
    [41]
    Riemensperger T, Isabel G, Coulom H, Neuser K, Seugnet L, Kume K, et al. 2011. Behavioral consequences of dopamine deficiency in the Drosophila central nervous system. Proceedings of the National Academy of Sciences of the United States of America, 108(2): 834−839. doi: 10.1073/pnas.1010930108
    [42]
    Roger LJ, Fellows RE. 1979. Evidence for thyroxine-growth hormone interaction during brain development. Nature, 282(5737): 414−415. doi: 10.1038/282414a0
    [43]
    Sasaki K, Akasaka S, Mezawa R, Shimada K, Maekawa K. 2012. Regulation of the brain dopaminergic system by juvenile hormone in honey bee males (Apis mellifera L.). Insect Molecular Biology, 21(5): 502−509. doi: 10.1111/j.1365-2583.2012.01153.x
    [44]
    Schützler N, Girwert C, Hügli I, Mohana G, Roignant JY, Ryglewski S, et al. 2019. Tyramine action on motoneuron excitability and adaptable tyramine/octopamine ratios adjust Drosophila locomotion to nutritional state. Proceedings of the National Academy of Sciences of the United States of America, 116(9): 3805−3810. doi: 10.1073/pnas.1813554116
    [45]
    Shpigler HY, Herb B, Drnevich J, Band M, Robinson GE, Bloch G. 2020. Juvenile hormone regulates brain-reproduction tradeoff in bumble bees but not in honey bees. Hormones and Behavior, 126: 104844. doi: 10.1016/j.yhbeh.2020.104844
    [46]
    Stuermer IW, Wetzel W. 2006. Early experience and domestication affect auditory discrimination learning, open field behaviour and brain size in wild Mongolian gerbils and domesticated laboratory gerbils (Meriones unguiculatus forma domestica). Behavioural Brain Research, 173(1): 11−21. doi: 10.1016/j.bbr.2006.05.025
    [47]
    Swanson-Wagner R, Briskine R, Schaefer R, Hufford MB, Ross-Ibarra J, Myers CL, et al. 2012. Reshaping of the maize transcriptome by domestication. Proceedings of the National Academy of Sciences of the United States of America, 109(29): 11878−11883. doi: 10.1073/pnas.1201961109
    [48]
    Tan AJ, Fu GL, Jin L, Guo QH, Li ZQ, Niu BL, et al. 2013. Transgene-based, female-specific lethality system for genetic sexing of the silkworm, Bombyx mori. Proceedings of the National Academy of Sciences of the United States of America, 110(17): 6766−6770. doi: 10.1073/pnas.1221700110
    [49]
    Tanriverdi OE, Yelkovan S. 2020. Histological investigation of the effects of fenoxycarb on neurosecretory cells in the silkworm, Bombyx mori brain. Invertebrate Neuroscience, 20(4): 20. doi: 10.1007/s10158-020-00253-3
    [50]
    Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. 2013. MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Molecular Biology and Evolution, 30(12): 2725−2729. doi: 10.1093/molbev/mst197
    [51]
    Trapnell C, Pachter L, Salzberg SL. 2009. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics, 25(9): 1105−1111. doi: 10.1093/bioinformatics/btp120
    [52]
    Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, et al. 2010. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nature Biotechnology, 28(5): 511−515. doi: 10.1038/nbt.1621
    [53]
    Vierk R, Pflueger HJ, Duch C. 2009. Differential effects of octopamine and tyramine on the central pattern generator for Manduca flight. Journal of Comparative Physiology A, 195(3): 265−277. doi: 10.1007/s00359-008-0404-5
    [54]
    Wang MS, Zhang RW, Su LY, Li Y, Peng MS, Liu HQ, et al. 2016. Positive selection rather than relaxation of functional constraint drives the evolution of vision during chicken domestication. Cell Research, 26(5): 556−573. doi: 10.1038/cr.2016.44
    [55]
    Wang PY, Qiu ZY, Xia DG, Tang SM, Shen XJ, Zhao QL. 2017. Transcriptome analysis of the epidermis of the purple quail-like (q-l p) mutant of silkworm, Bombyx mori. PLoS One, 12(4): e0175994. doi: 10.1371/journal.pone.0175994
    [56]
    Wheeler MM, Ament SA, Rodriguez-Zas SL, Southey B, Robinson GE. 2015. Diet and endocrine effects on behavioral maturation-related gene expression in the pars intercerebralis of the honey bee brain. Journal of Experimental Biology, 218(Pt 24): 4005−4014.
    [57]
    Xiang H, Liu XJ, Li MW, Zhu YN, Wang LZ, Cui Y, et al. 2018. The evolutionary road from wild moth to domestic silkworm. Nature Ecology & Evolution, 2(8): 1268−1279.
    [58]
    Yang Z. 1997. PAML: a program package for phylogenetic analysis by maximum likelihood. Computer Applications in the Biosciences, 13(5): 555−556.
    [59]
    Yang ZH, Wong WSW, Nielsen R. 2005. Bayes empirical bayes inference of amino acid sites under positive selection. Molecular Biology and Evolution, 22(4): 1107−1118. doi: 10.1093/molbev/msi097
    [60]
    Zhu GH, Jiao YY, Chereddy SCRR, Noh MY, Palli SR. 2019. Knockout of juvenile hormone receptor, Methoprene-tolerant, induces black larval phenotype in the yellow fever mosquito, Aedes aegypti. Proceedings of the National Academy of Sciences of the United States of America, 116(43): 21501−21507. doi: 10.1073/pnas.1905729116
    [61]
    Zhu HS, Gegear RJ, Casselman A, Kanginakudru S, Reppert SM. 2009. Defining behavioral and molecular differences between summer and migratory monarch butterflies. BMC Biology, 7(1): 14. doi: 10.1186/1741-7007-7-14
  • ZR-2021-126 Supplementary Materials.zip
  • 加载中

Catalog

    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Figures(7)  / Tables(1)

    Article Metrics

    Article views (817) PDF downloads(145) Cited by()
    Proportional views
    Related

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return