Skip to main content
SpringerLink
Log in

A neural m6A pathway regulates behavioral aggregation in migratory locusts

  • Research Paper
  • Published:
Science China Life Sciences Aims and scope Submit manuscript

Abstract

RNA N6-methyladenosine (m6A), as the most abundant modification of messenger RNA, can modulate insect behaviors, but its specific roles in aggregation behaviors remain unexplored. Here, we conducted a comprehensive molecular and physiological characterization of the individual components of the methyltransferase and demethylase in the migratory locust Locusta migratoria. Our results demonstrated that METTL3, METTL14 and ALKBH5 were dominantly expressed in the brain and exhibited remarkable responses to crowding or isolation. The individual knockdown of methyltransferases (i.e., METTL3 and METTL14) promoted locust movement and conspecific attraction, whereas ALKBH5 knockdown induced a behavioral shift toward the solitary phase. Furthermore, global transcriptome profiles revealed that m6A modification could regulate the orchestration of gene expression to fine tune the behavioral aggregation of locusts. In summary, our in vivo characterization of the m6A functions in migratory locusts clearly demonstrated the crucial roles of the m6A pathway in effectively modulating aggregation behaviors.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Anreiter, I., Kramer, J.M., and Sokolowski, M.B. (2017). Epigenetic mechanisms modulate differences in Drosophila foraging behavior. Proc Natl Acad Sci USA 114, 12518–12523.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  • Bewick, A.J., Vogel, K.J., Moore, A.J., and Schmitz, R.J. (2017). Evolution of DNA methylation across insects. Mol Biol Evol 34, 654–665.

    CAS  PubMed  Google Scholar 

  • Biergans, S.D., Jones, J.C., Treiber, N., Galizia, C.G., and Szyszka, P. (2012). DNA methylation mediates the discriminatory power of associative long-term memory in honeybees. PLoS ONE 7, e39349.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  • Bolger, A.M., Lohse, M., and Usadel, B. (2014). Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Certel, S.J., and Thor, S. (2004). Specification of Drosophila motoneuron identity by the combinatorial action of POU and LIM-HD factors. Development 131, 5429–5439.

    Article  CAS  PubMed  Google Scholar 

  • Chen, D., Hou, L., Wei, J., Guo, S., Cui, W., Yang, P., Kang, L., and Wang, X. (2022). Aggregation pheromone 4-vinylanisole promotes the synchrony of sexual maturation in female locusts. eLife 11, e74581.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen, S., Yang, P., Jiang, F., Wei, Y., Ma, Z., and Kang, L. (2010). De novo analysis of transcriptome dynamics in the migratory locust during the development of phase traits. PLoS ONE 5, e15633.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  • Cully, S.M., and Seeley, T.D. (2004). Self-assemblage formation in a social insect: the protective curtain of a honey bee swarm. Insect Soc 51, 317–324.

    Article  Google Scholar 

  • Dominissini, D., Moshitch-Moshkovitz, S., Schwartz, S., Salmon-Divon, M., Ungar, L., Osenberg, S., Cesarkas, K., Jacob-Hirsch, J., Amariglio, N., Kupiec, M., et al. (2012). Topology of the human and mouse m6A RNA methylomes revealed by m6A-seq. Nature 485, 201–206.

    Article  CAS  PubMed  ADS  Google Scholar 

  • du Preez, P.H., Breeds, K., Burger, N.F.V., Swiegers, H.W., Truter, J.C., and Botha, A. M. (2020). DNA methylation and demethylation are regulated by functional DNA methyltransferases and DnTET enzymes in Diuraphis noxia. Front Genet 11, 452.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Frye, M., Harada, B.T., Behm, M., and He, C. (2018). RNA modifications modulate gene expression during development. Science 361, 1346–1349.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  • Fu, Y., Dominissini, D., Rechavi, G., and He, C. (2014). Gene expression regulation mediated through reversible m6A RNA methylation. Nat Rev Genet 15, 293–306.

    Article  CAS  PubMed  Google Scholar 

  • Gao, G., Duan, Y., Chang, F., Zhang, T., Huang, X., and Yu, C. (2022). METTL14 promotes apoptosis of spinal cord neurons by inducing EEF1A2 m6A methylation in spinal cord injury. Cell Death Discov 8, 15.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Geula, S., Moshitch-Moshkovitz, S., Dominissini, D., Mansour, A.A.F., Kol, N., Salmon-Divon, M., Hershkovitz, V., Peer, E., Mor, N., Manor, Y.S., et al. (2015). m6 A mRNA methylation facilitates resolution of naïve pluripotency toward differentiation. Science 347, 1002–1006.

    Article  CAS  PubMed  ADS  Google Scholar 

  • Guo, S., Jiang, F., Yang, P., Liu, Q., Wang, X., and Kang, L. (2016). Characteristics and expression patterns of histone-modifying enzyme systems in the migratory locust. Insect Biochem Mol Biol 76, 18–28.

    Article  CAS  PubMed  Google Scholar 

  • Guo, W., Song, J., Yang, P., Chen, X., Chen, D., Ren, D., Kang, L., and Wang, X.H. (2020). Juvenile hormone suppresses aggregation behavior through influencing antennal gene expression in locusts. PLoS Genet 16, e1008762.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo, W., Wang, X., Ma, Z., Xue, L., Han, J., Yu, D., and Kang, L. (2011). CSP and Takeout genes modulate the switch between attraction and repulsion during behavioral phase change in the migratory locust. PLoS Genet 7, e1001291.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hassan, J., Busto, M., Iyengar, B., and Campos, A.R. (2000). Behavioral characterization and genetic analysis of the Drosophila melanogaster larval response to light as revealed by a novel individual assay. Behav Genet 30, 59–69.

    Article  CAS  PubMed  Google Scholar 

  • Heinz, S., Benner, C., Spann, N., Bertolino, E., Lin, Y.C., Laslo, P., Cheng, J.X., Murre, C., Singh, H., and Glass, C.K. (2010). Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol Cell 38, 576–589.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Henry, J.R., and Harrison, J.F. (2014). Effects of body size on the oxygen sensitivity of dragonfly flight. J Exp Biol 217, 3447–3456.

    PubMed  Google Scholar 

  • Hou, L., Li, B., Ding, D., Kang, L., and Wang, X.H. (2019). CREB-B acts as a key mediator of NPF/NO pathway involved in phase-related locomotor plasticity in locusts. PLoS Genet 15, e1008176.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hou, L., Wang, X., Yang, P., Li, B., Lin, Z., Kang, L., and Wang, X. (2020). DNA methyltransferase 3 participates in behavioral phase change in the migratory locust. Insect Biochem Mol Biol 121, 103374.

    Article  CAS  PubMed  Google Scholar 

  • Hou, L., Yang, P., Jiang, F., Liu, Q., Wang, X., and Kang, L. (2017). The neuropeptide F/nitric oxide pathway is essential for shaping locomotor plasticity underlying locust phase transition. eLife 6, e22526.

    Article  PubMed  PubMed Central  Google Scholar 

  • Hu, Y., Wang, X., Xu, Y., Yang, H., Tong, Z., Tian, R., Xu, S., Yu, L., Guo, Y., Shi, P., et al. (2023). Molecular mechanisms of adaptive evolution in wild animals and plants. Sci China Life Sci 66, 453–495.

    Article  PubMed  PubMed Central  Google Scholar 

  • Huang, X., Liu, D., Cui, X., and Shi, X. (2018). Probing behaviors and their plasticity for the aphid Sitobion avenae on three alternative host plants. PLoS ONE 13, e0203219.

    Article  PubMed  PubMed Central  Google Scholar 

  • Jaenisch, R., and Bird, A. (2003). Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet 33, 245–254.

    Article  CAS  PubMed  Google Scholar 

  • Jia, G., Fu, Y., Zhao, X., Dai, Q., Zheng, G., Yang, Y., Yi, C., Lindahl, T., Pan, T., Yang, Y.G., et al. (2011). N6-methyladenosine in nuclear RNA is a major substrate of the obesity-associated FTO. Nat Chem Biol 7, 885–887.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jia, G., Yang, C.G., Yang, S., Jian, X., Yi, C., Zhou, Z., and He, C. (2008). Oxidative demethylation of 3-methylthymine and 3-methyluracil in single-stranded DNA and RNA by mouse and human FTO. FEBS Lett 582, 3313–3319.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang, T., Li, J., Qian, P., Xue, P., Xu, J., Chen, Y., Zhu, J., Tang, S., Zhao, Q., Qian, H., et al. (2019). The role of N6-methyladenosine modification on diapause in silkworm (Bombyx mori) strains that exhibit different voltinism. Mol Reprod Dev 86, 1981–1992.

    Article  CAS  PubMed  Google Scholar 

  • Kan, L., Ott, S., Joseph, B., Park, E.S., Dai, W., Kleiner, R.E., Claridge-Chang, A., and Lai, E.C. (2021). A neural m6A/Ythdf pathway is required for learning and memory in Drosophila. Nat Commun 12, 1458.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  • Kim, D., Langmead, B., and Salzberg, S.L. (2015). HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12, 357–360.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kocher, S.D., Mallarino, R., Rubin, B.E.R., Yu, D.W., Hoekstra, H.E., and Pierce, N.E. (2018). The genetic basis of a social polymorphism in halictid bees. Nat Commun 9, 1–7.

    Article  CAS  Google Scholar 

  • Koon, A.C., Ashley, J., Barria, R., DasGupta, S., Brain, R., Waddell, S., Alkema, M.J., and Budnik, V. (2011). Autoregulatory and paracrine control of synaptic and behavioral plasticity by octopaminergic signaling. Nat Neurosci 14, 190–199.

    Article  CAS  PubMed  Google Scholar 

  • Kumar, S., Stecher, G., and Tamura, K. (2016). MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33, 1870–1874.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lence, T., Akhtar, J., Bayer, M., Schmid, K., Spindler, L., Ho, C.H., Kreim, N., Andrade-Navarro, M.A., Poeck, B., Helm, M., et al. (2016). m6A modulates neuronal functions and sex determination in Drosophila. Nature 540, 242–247.

    Article  CAS  PubMed  ADS  Google Scholar 

  • Lence, T., Soller, M., and Roignant, J.Y. (2017). A fly view on the roles and mechanisms of the m6A mRNA modification and its players. RNA Biol 14, 1232–1240.

    Article  PubMed  PubMed Central  Google Scholar 

  • Li, B., Wang, X., Li, Z., Lu, C., Zhang, Q., Chang, L., Li, W., Cheng, T., Xia, Q., and Zhao, P. (2019). Transcriptome-wide analysis of N6-methyladenosine uncovers its regulatory role in gene expression in the lepidopteran Bombyx mori. Insect Mol Biol 28, 703–715.

    Article  CAS  PubMed  Google Scholar 

  • Li, J., Zhu, W.Y., Yang, W.Q., Li, C.T., and Liu, R.J. (2021). The occurrence order and cross-talk of different tRNA modifications. Sci China Life Sci 64, 1423–1436.

    Article  CAS  PubMed  Google Scholar 

  • Libbrecht, R., Nadrau, D., and Foitzik, S. (2020). A role of histone acetylation in the regulation of circadian rhythm in ants. iScience 23, 100846.

    Article  PubMed  PubMed Central  ADS  Google Scholar 

  • Lihoreau, M., Buhl, J., Charleston, M.A., Sword, G.A., Raubenheimer, D., and Simpson, S.J. (2015). Nutritional ecology beyond the individual: a conceptual framework for integrating nutrition and social interactions. Ecol Lett 18, 273–286.

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu, J., Yue, Y., Han, D., Wang, X., Fu, Y., Zhang, L., Jia, G., Yu, M., Lu, Z., Deng, X., et al. (2014). A METTL3-METTL14 complex mediates mammalian nuclear RNA N6-adenosine methylation. Nat Chem Biol 10, 93–95.

    Article  CAS  PubMed  ADS  Google Scholar 

  • Livneh, I., Moshitch-Moshkovitz, S., Amariglio, N., Rechavi, G., and Dominissini, D. (2020). The m6A epitranscriptome: transcriptome plasticity in brain development and function. Nat Rev Neurosci 21, 36–51.

    Article  CAS  PubMed  Google Scholar 

  • Lorbeck, M.T., Singh, N., Zervos, A., Dhatta, M., Lapchenko, M., Yang, C., and Elefant, F. (2010). The histone demethylase DmelKdm4A controls genes required for life span and male-specific sex determination in Drosophila. Gene 450, 8–17.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma, C., Chang, M., Lv, H., Zhang, Z.W., Zhang, W., He, X., Wu, G., Zhao, S., Zhang, Y., Wang, D., et al. (2018). RNA m6A methylation participates in regulation of postnatal development of the mouse cerebellum. Genome Biol 19, 68.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ma, Z., Guo, W., Guo, X., Wang, X., and Kang, L. (2011). Modulation of behavioral phase changes of the migratory locust by the catecholamine metabolic pathway. Proc Natl Acad Sci USA 108, 3882–3887.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  • Mendel, M., Chen, K.M., Homolka, D., Gos, P., Pandey, R.R., McCarthy, A.A., and Pillai, R.S. (2018). Methylation of structured RNA by the m6A writer METTL16 is essential for mouse embryonic development. Mol Cell 71, 986–1000.e11.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martin, M. (2011). Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J 17, 10–12.

    Article  Google Scholar 

  • Meyer, K.D., Saletore, Y., Zumbo, P., Elemento, O., Mason, C.E., and Jaffrey, S.R. (2012). Comprehensive analysis of mRNA methylation reveals enrichment in 3′ UTRs and near stop codons. Cell 149, 1635–1646.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Özbey, N.P., Thompson, M.A., and Taylor, R.C. (2021). The regulation of animal behavior by cellular stress responses. Exp Cell Res 405, 112720.

    Article  PubMed  PubMed Central  Google Scholar 

  • Parr, C.L., and Bishop, T.R. (2022). The response of ants to climate change. Glob Change Biol 28, 3188–3205.

    Article  CAS  Google Scholar 

  • Pener, M.P., and Simpson, S.J. (2009). Locust phase polyphenism: an update. Adv Insect Phys 36, 1–272.

    Article  Google Scholar 

  • Perlegos, A.E., Shields, E.J., Shen, H., Liu, K.F., and Bonini, N.M. (2022). Mettl3-dependent m6A modification attenuates the brain stress response in Drosophila. Nat Commun 13, 5387.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  • Pirooznia, S.K., Chiu, K., Chan, M.T., Zimmerman, J.E., and Elefant, F. (2012). Epigenetic regulation of axonal growth of Drosophila pacemaker cells by histone acetyltransferase Tip60 controls sleep. Genetics 192, 1327–1345.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Portela, A., and Esteller, M. (2010). Epigenetic modifications and human disease. Nat Biotechnol 28, 1057–1068.

    Article  CAS  PubMed  Google Scholar 

  • Pradhan, S., Quilez, S., Homer, K., and Hendricks, M. (2019). Environmental programming of adult foraging behavior in C. elegans. Curr Biol 29, 2867–2879.e4.

    Google Scholar 

  • Privalova, V., Szlachcic, E., Sobczyk, L., Szabla, N., and Czarnoleski, M. (2021). Oxygen dependence of flight performance in ageing Drosophila melanogaster. Biology 10, 327.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Quinlan, A.R., and Hall, I.M. (2010). BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841–842.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reynolds, A.M., Sword, G.A., Simpson, S.J., and Reynolds, D.R. (2009). Predator percolation, insect outbreaks, and phase polyphenism. Curr Biol 19, 20–24.

    Article  CAS  PubMed  Google Scholar 

  • Robinson, M.D., McCarthy, D.J., and Smyth, G.K. (2010). edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139–140.

    Article  CAS  PubMed  Google Scholar 

  • Roignant, J.Y., and Soller, M. (2017). m6A in mRNA: an ancient mechanism for fine-tuning gene expression. Trends Genet 33, 380–390.

    Article  CAS  PubMed  Google Scholar 

  • Ruud, J., Alber, J., Tokarska, A., Engström Ruud, L., Nolte, H., Biglari, N., Lippert, R., Lautenschlager, Ä., Cieślak, P.E., Szumiec, L., et al. (2019). The fat mass and obesity-associated protein (FTO) regulates locomotor responses to novelty via D2R medium spiny neurons. Cell Rep 27, 3182–3198.e9.

    Google Scholar 

  • Rybina, O.Y., Sarantseva, S.V., Veselkina, E.R., Bolschakova, O.I., Symonenko, A.V., Krementsova, A.V., Ryabova, E.V., Roshina, N.V., and Pasyukova, E.G. (2017). Tissue-specific transcription of the neuronal gene Lim3 affects Drosophila melanogaster lifespan and locomotion. Biogerontology 18, 739–757.

    Article  CAS  PubMed  Google Scholar 

  • Shi, C., Lou, Q., Fu, B., Jin, J., Huang, J., Lu, Y., Jin, X., He, J., Zhai, G., Xie, S., et al. (2022). Genomic polymorphisms at the crhr2 locus improve feed conversion efficiency through alleviation of hypothalamus-pituitary-interrenal axis activity in gibel carp (Carassius gibelio). Sci China Life Sci 65, 206–214.

    Article  CAS  PubMed  Google Scholar 

  • Simola, D.F., Ye, C., Mutti, N.S., Dolezal, K., Bonasio, R., Liebig, J., Reinberg, D., and Berger, S.L. (2013). A chromatin link to caste identity in the carpenter ant Camponotus floridanus. Genome Res 23, 486–496.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stige, L.C., Chan, K.S., Zhang, Z., Frank, D., and Stenseth, N.C. (2007). Thousand-year-long Chinese time series reveals climatic forcing of decadal locust dynamics. Proc Natl Acad Sci USA 104, 16188–16193.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  • Strauss, U., Dietemann, V., Human, H., Crewe, R.M., and Pirk, C.W.W. (2016). Resistance rather than tolerance explains survival of savannah honeybees (Apis mellifera scutellata) to infestation by the parasitic mite Varroa destructor. Parasitology 143, 374–387.

    Article  PubMed  Google Scholar 

  • Villalta, I., Oms, C.S., Angulo, E., Molinas-González, C.R., Devers, S., Cerdá, X., and Boulay, R. (2020). Does social thermal regulation constrain individual thermal tolerance in an ant species? J Anim Ecol 89, 2063–2076.

    Article  PubMed  Google Scholar 

  • Wada-Katsumata, A., Zurek, L., Nalyanya, G., Roelofs, W.L., Zhang, A., and Schal, C. (2015). Gut bacteria mediate aggregation in the German cockroach. Proc Natl Acad Sci USA 112, 15678–15683.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  • Wallace, D.L., Han, M.H., Graham, D.L., Green, T.A., Vialou, V., Iñiguez, S.D., Cao, J. L., Kirk, A., Chakravarty, S., Kumar, A., et al. (2009). CREB regulation of nucleus accumbens excitability mediates social isolation-induced behavioral deficits. Nat Neurosci 12, 200–209.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, B.B., Lai, Y.F., Li, F.F., Jiao, L., Qiao, Q.X., Li, S.Y., Xiang, X.J., Liao, H., You, M. S., and He, W.Y. (2022a). Functional characterization of two RNA methyltransfer-ase genes METTL3 and METTL14 uncovers the roles of m6A in mediating adaptation of Plutella xylostella to host plants. Int J Mol Sci 23, 10013.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, M., Xiao, Y., Li, Y., Wang, X., Qi, S., Wang, Y., Zhao, L., Wang, K., Peng, W., Luo, G.Z., et al. (2021a). RNA m6A modification functions in larval development and caste differentiation in honeybee (Apis mellifera). Cell Rep 34, 108580.

    Article  CAS  PubMed  Google Scholar 

  • Wang, X., Fang, X., Yang, P., Jiang, X., Jiang, F., Zhao, D., Li, B., Cui, F., Wei, J., Ma, C., et al. (2014). The locust genome provides insight into swarm formation and long-distance flight. Nat Commun 5, 2957.

    Article  PubMed  ADS  Google Scholar 

  • Wang, X., and Kang, L. (2014). Molecular mechanisms of phase change in locusts. Annu Rev Entomol 59, 225–244.

    Article  CAS  PubMed  Google Scholar 

  • Wang, Y.J., Yang, B., Lai, Q., Shi, J.F., Peng, J.Y., Zhang, Y., Hu, K.S., Li, Y.Q., Peng, J. W., Yang, Z.Z., et al. (2021b). Reprogramming of m6A epitranscriptome is crucial for shaping of transcriptome and proteome in response to hypoxia. RNA Biol 18, 131–143.

    Article  CAS  PubMed  Google Scholar 

  • Wang, Y., Fang, G., Xu, P., Gao, B., Liu, X., Qi, X., Zhang, G., Cao, S., Li, Z., Ren, X., et al. (2022b). Behavioral and genomic divergence between a generalist and a specialist fly. Cell Rep 41, 111654.

    Article  CAS  PubMed  Google Scholar 

  • Wheeler, D.E., Buck, N., and Evans, J.D. (2006). Expression of insulin pathway genes during the period of caste determination in the honey bee, Apis mellifera. Insect Mol Biol 15, 597–602.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Williamson, S.M., Ingelson-Filpula, W.A., Hadj-Moussa, H., and Storey, K.B. (2021). Epigenetic underpinnings of freeze avoidance in the goldenrod gall moth, Epiblema scudderiana. J Insect Physiol 134, 104298.

    Article  CAS  PubMed  Google Scholar 

  • Wu, R., Li, A., Sun, B., Sun, J.G., Zhang, J., Zhang, T., Chen, Y., Xiao, Y., Gao, Y., Zhang, Q., et al. (2019). A novel m6A reader Prrc2a controls oligodendroglial specification and myelination. Cell Res 29, 23–41.

    Article  PubMed  Google Scholar 

  • Wu, R., Wu, Z., Wang, X., Yang, P., Yu, D., Zhao, C., Xu, G., and Kang, L. (2012). Metabolomic analysis reveals that carnitines are key regulatory metabolites in phase transition of the locusts. Proc Natl Acad Sci USA 109, 3259–3263.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  • Xiang, Y., Laurent, B., Hsu, C.H., Nachtergaele, S., Lu, Z., Sheng, W., Xu, C., Chen, H., Ouyang, J., Wang, S., et al. (2017). RNA m6A methylation regulates the ultraviolet-induced DNA damage response. Nature 543, 573–576.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  • Yang, P., Hou, L., Wang, X., and Kang, L. (2019). Core transcriptional signatures of phase change in the migratory locust. Protein Cell 10, 883–901.

    Article  PubMed  PubMed Central  Google Scholar 

  • Yang, X., Wei, X., Yang, J., Du, T., Yin, C., Fu, B., Huang, M., Liang, J., Gong, P., Liu, S., et al. (2021). Epitranscriptomic regulation of insecticide resistance. Sci Adv 7, eabe5903.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  • Zaccara, S., and Jaffrey, S.R. (2020). A unified model for the function of YTHDF proteins in regulating m6A-modified mRNA. Cell 181, 1582–1595.e18.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zamurrad, S., Hatch, H.A.M., Drelon, C., Belalcazar, H.M., and Secombe, J. (2018). A Drosophila model of intellectual disability caused by mutations in the histone demethylase KDM5. Cell Rep 22, 2359–2369.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, C., and Zhang, B. (2023). RNA therapeutics: updates and future potential. Sci China Life Sci 66, 12–30.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, C., Chen, Y., Sun, B., Wang, L., Yang, Y., Ma, D., Lv, J., Heng, J., Ding, Y., Xue, Y., et al. (2017). m6A modulates haematopoietic stem and progenitor cell specification. Nature 549, 273–276.

    Article  CAS  PubMed  ADS  Google Scholar 

  • Zhang, L., Lecoq, M., Latchininsky, A., and Hunter, D. (2019). Locust and grasshopper management. Annu Rev Entomol 64, 15–34.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, M., Chen, J.L., Liang, S.K., Li, G.H., Wang, F.H., and Ahmad, I. (2015). Differentially methylated genomic fragments related with sexual dimorphism of rice pests, Sogatella furcifera. Insect Sci 22, 731–738.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, X., Xu, Y.N., Chen, B., and Kang, L. (2020). Long noncoding RNA PAHAL modulates locust behavioural plasticity through the feedback regulation of dopamine biosynthesis. PLoS Genet 16, e1008771.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, X., Zhu, Y., Chen, B., and Kang, L. (2022). A Gypsy element contributes to the nuclear retention and transcriptional regulation of the resident lncRNA in locusts. RNA Biol 19, 206–220.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, Y., Liu, T., Meyer, C.A., Eeckhoute, J., Johnson, D.S., Bernstein, B.E., Nusbaum, C., Myers, R.M., Brown, M., Li, W., et al. (2008). Model-based Analysis of ChIP-Seq (MACS). Genome Biol 9, R137.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhao, B.S., Roundtree, I.A., and He, C. (2017). Post-transcriptional gene regulation by mRNA modifications. Nat Rev Mol Cell Biol 18, 31–42.

    Article  CAS  PubMed  Google Scholar 

  • Zheng, X., Xin, Y., Peng, Y., Shan, J., Zhang, N., Wu, D., Guo, J., Huang, J., Guan, W., Shi, S., et al. (2021). Lipidomic analyses reveal enhanced lipolysis in planthoppers feeding on resistant host plants. Sci China Life Sci 64, 1502–1521.

    Article  CAS  PubMed  Google Scholar 

  • Zhou, J., Wan, J., Gao, X., Zhang, X., Jaffrey, S.R., and Qian, S.B. (2015). Dynamic m6 A mRNA methylation directs translational control of heat shock response. Nature 526, 591–594.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

Download references

Acknowledgement

This work was supported by the National Key Research and Development Program of China (2022YFD1400503), the National Natural Science Foundation of China (32102208), Hebei Natural Science Foundation (C2022201042, C2023201075) and Hebei Educational Committee Foundation (BJK2023015). We would like to thank D.G. Liu (Northwest A&F University, China) for critical comments on previous versions of this manuscript.

Author information

Author notes

  1. Contributed equally to this work

Authors and Affiliations

  1. School of Life Science, Institutes of Life Science and Green Development, Hebei University, Baoding, 071002, China

    Xianliang Huang, Le Kang & Bing Chen

  2. College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, 430070, China

    Qing Li & Shaoqin Li

  3. State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, 100101, China

    Qing Li, Chunrui Zhang, Xia Zhang & Le Kang

  4. Institute of Health Sciences, Anhui University, Hefei, 230601, China

    Yanan Xu

  5. Beijing Institute of Genomics, Chinese Academy of Sciences, Beijing, 100101, China

    Ang Li, Shanzheng Wang, Yusheng Chen & Baofa Sun

  6. State Key Laboratory of Environmental Chemistry and Ecotoxicology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing, 100101, China

    Hailin Wang & Cong Lv

Authors
  1. Xianliang Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Qing Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yanan Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ang Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Shanzheng Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yusheng Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Chunrui Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Xia Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Hailin Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Cong Lv
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Baofa Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Shaoqin Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Le Kang
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Bing Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Le Kang or Bing Chen.

Ethics declarations

The author(s) declare that they have no conflict of Interest.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Huang, X., Li, Q., Xu, Y. et al. A neural m6A pathway regulates behavioral aggregation in migratory locusts. Sci. China Life Sci. (2024). https://doi.org/10.1007/s11427-023-2476-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11427-023-2476-1

Search

Navigation