CoChat
Sign Up
Cited by 2Neurobiology and Insect Physiology ResearchDevelopmental Biology and Gene RegulationAnimal Behavior and Reproduction

The DOI matches its Crossref record; 3 of the 3 references it cites were found in a registry or an index.

The maternal vGluT2 and embryonic mGluR3 signaling relay system controls offspring wing dimorphism in pea aphid

Open access
Yuan, Yiyang, Wang, Yanyan, Ye, Wanwan, Xie, Liqiang, Yuan, Erliang, Guo, Huijuan, Wang, Shifan, Dong, Fang, Zhu-Salzman, Keyan, Ge, Feng, Sun, Yucheng·2025·iScience
DOI 10.1016/j.isci.2025.112591PMC PMC12145829

Published version of a preprint

Open this paper in CoChat — free account

Abstract

Abstract Transgenerational phenotypic plasticity (TPP) refers to the phenomenon that environmental conditions experienced by one generation can influence the phenotype of subsequent generations to adapt to the environment without modification of their DNA sequences. Aphid wing dimorphism is a textbook example of TPP by which a maternal aphid perceives the environmental cues to decide the wing morph of her offspring. However, the signaling mechanism from mother to daughter remains unclear. In this study, we showed that the population density and physical contact caused high proportion of winged offspring in the pea aphid Acyrthosiphon pisum . Its vesicular glutamate transporter 2 ( ApvGluT2 ) and metabotropic glutamate receptor 3 ( ApmGluR3 ) were identified by tissue-specific RNA-seq as differentially expressed genes in the head and embryo respectively between solitary and more densely housed maternal aphids. Elevated expression of brain ApvGluT2 and embryonic ApmGluR3 led to increases in the winged proportion. Knockdown of either gene inhibited phosphorylation of ApFoxO in embryos. Furthermore, EMSA showed that dephosphorylated ApFoxO directly bound to the promotor of hedgehog ( ApHh ), a morphogen gene for wing development, to repress its transcription in stage 20 embryos, causing a lower winged proportion. Our results demonstrated that brain vGluT2 and embryonic mGluR3 coordinately relayed the maternal physical contact signals and control wing development in offspring, showcasing a novel regulatory mechanism underlying physical contact-dependent, transgenerational wing dimorphism in aphids.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1016/j.isci.2025.112591

Cites

3 of 3 references verified0 citation errors · 0 not checkable

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

Flagged first, then by citations

Research works printed but not linked: 70

  1. Bell, 2019, An integrative framework for understanding the mechanisms and multigenerational consequences of transgenerational plasticity, Annu. Rev. Ecol. Evol. Syst., 50, 97, 10.1146/annurev-ecolsys-110218-024613 · DOI
  2. Guillaume, 2016, Transgenerational plasticity and environmental stress: do paternal effects act as a conduit or a buffer?, Funct. Ecol., 30, 1175, 10.1111/1365-2435.12604 · DOI
  3. Donelan, 2020, Transgenerational Plasticity in Human-Altered Environments, Trends Ecol. Evol., 35, 115, 10.1016/j.tree.2019.09.003 · DOI
  4. Brisson, 2010, Aphid wing dimorphisms: linking environmental and genetic control of trait variation, Philos. Trans. R. Soc. Lond. B Biol. Sci., 365, 605, 10.1098/rstb.2009.0255 · DOI
  5. Zera, 1997, Physiology and ecology of dispersal polymorphism in insects, Annu. Rev. Entomol., 42, 207, 10.1146/annurev.ento.42.1.207 · DOI
  6. Zhang, 2019, Molecular Mechanisms of Wing Polymorphism in Insects, Annu. Rev. Entomol., 64, 297, 10.1146/annurev-ento-011118-112448 · DOI
  7. Roff, 1990, The evolution of flightlessness in insects, Ecol. Monogr., 60, 389, 10.2307/1943013 · DOI
  8. Roff, 1994, The evolution of flightlessness: Is history important?, Evol. Ecol., 8, 639, 10.1007/BF01237847 · DOI
  9. Wagner, 1992, Flightlessness in insects, Trends Ecol. Evol., 7, 216, 10.1016/0169-5347(92)90047-F · DOI
  10. Braendle, 2005, Genetic variation for an aphid wing polyphenism is genetically linked to a naturally occurring wing polymorphism, Proc. Biol. Sci., 272, 657
  11. Ishikawa, 2013, Transduction of high-density signals across generations in aphid wing polyphenism, Physiol. Entomol., 38, 150, 10.1111/phen.12022 · DOI
  12. Deem, 2024, Evolution and molecular mechanisms of wing plasticity in aphids, Curr. Opin. Insect Sci., 61
  13. Sng, 2020, Too many people, women, men? The psychological effects of population density and sex ratio, Curr. Opin. Psychol., 32, 38, 10.1016/j.copsyc.2019.06.015 · DOI
  14. Sutherland, 1969, The role of crowding in the production of winged forms by two strains of the pea aphid, Acyrthosiphon pisum, J. Insect Physiol., 15, 1385, 10.1016/0022-1910(69)90199-1 · DOI
  15. Yuan, 2023, Functional evaluation of the insulin/insulin-like growth factor signaling pathway in determination of wing polyphenism in pea aphid, Insect Sci., 30, 816, 10.1111/1744-7917.13121 · DOI
  16. Yuan, 2023, A novel gene REPTOR2 activates the autophagic degradation of wing disc in pea aphid, Elife, 12, 10.7554/eLife.83023 · DOI
  17. Kunert, 2005, Alarm pheromone mediates production of winged dispersal morphs in aphids, Ecol. Lett., 8, 596, 10.1111/j.1461-0248.2005.00754.x · DOI
  18. Xu, 2015, Two insulin receptors determine alternative wing morphs in planthoppers, Nature, 519, 464, 10.1038/nature14286 · DOI
  19. Zhang, 2022, The transcription factor Zfh1 acts as a wing-morph switch in planthoppers, Nat. Commun., 13, 5670, 10.1038/s41467-022-33422-6 · DOI
  20. Chen, 2023, FoxO and rotund form a binding complex governing wing polyphenism in planthoppers, iScience, 26
  21. Lin, 2020, Cell cycle progression determines wing morph in the polyphenic insect Nilaparvata lugens, iScience, 23, 10.1016/j.isci.2020.101040 · DOI
  22. Xu, 2021, Transcriptome Analysis of the Regulatory Mechanism of FoxO on Wing Dimorphism in the Brown Planthopper, Nilaparvata lugens (Hemiptera: Delphacidae), Insects, 12, 413, 10.3390/insects12050413 · DOI
  23. Zhang, 2021, Vestigial mediates the effect of insulin signaling pathway on wing-morph switching in planthoppers, PLoS Genet., 17, 10.1371/journal.pgen.1009312 · DOI
  24. Liu, 2023, Dopamine mediates the pea aphid wing plasticity, Biol. Lett., 19, 10.1098/rsbl.2023.0024 · DOI
  25. Shang, 2020, The miR-9b microRNA mediates dimorphism and development of wing in aphids, Proc. Natl. Acad. Sci. USA, 117, 8404, 10.1073/pnas.1919204117 · DOI
  26. Vellichirammal, 2017, Ecdysone signaling underlies the pea aphid transgenerational wing polyphenism, Proc. Natl. Acad. Sci. USA, 114, 1419, 10.1073/pnas.1617640114 · DOI · Paper page
  27. Zhou, 2023, The Wnt pathway regulates wing morph determination in Acyrthosiphon pisum, Insect Biochem. Mol. Biol., 161, 10.1016/j.ibmb.2023.104003 · DOI
  28. Yang, 2023, Glutamate-GABA imbalance mediated by miR-8-5p and its STTM regulates phase-related behavior of locusts, Proc. Natl. Acad. Sci. USA, 120
  29. Jones, 2022, Transgenerational transmission of aspartame-induced anxiety and changes in glutamate-GABA signaling and gene expression in the amygdala, Proc. Natl. Acad. Sci. USA, 119, 10.1073/pnas.2213120119 · DOI
  30. Liu, 2017, Activity strengths of cortical glutamatergic and GABAergic neurons are correlated with transgenerational inheritance of learning ability, Oncotarget, 8, 112401, 10.18632/oncotarget.19918 · DOI
  31. Tao, 2020, MeCP2 mediates transgenerational transmission of chronic pain, Prog. Neurobiol., 189, 10.1016/j.pneurobio.2020.101790 · DOI
  32. Van Winkle, 2022, Perspective: Might Maternal Dietary Monosodium Glutamate (MSG) Consumption Impact Pre- and Peri-Implantation Embryos and Their Subsequent Development?, Int. J. Environ. Res. Public Health, 19, 10.3390/ijerph192013611 · DOI
  33. Featherstone, 2010, Intercellular glutamate signaling in the nervous system and beyond, ACS Chem. Neurosci., 1, 4, 10.1021/cn900006n · DOI
  34. Willard, 2013, Glutamate, glutamate receptors, and downstream signaling pathways, Int. J. Biol. Sci., 9, 948, 10.7150/ijbs.6426 · DOI
  35. Howlett, 2008, A PI3-kinase-mediated negative feedback regulates neuronal excitability, PLoS Genet., 4, 10.1371/journal.pgen.1000277 · DOI
  36. Roccaro-Waldmeyer, 2018, Eliminating the VGlut2-dependent glutamatergic transmission of parvalbumin-expressing neurons leads to deficits in locomotion and vocalization, decreased pain sensitivity, and increased dominance, Front. Behav. Neurosci., 12, 146, 10.3389/fnbeh.2018.00146 · DOI
  37. Lin, 2016, Ecological trade-offs between migration and reproduction are mediated by the nutrition-sensitive insulin-signaling pathway, Int. J. Biol. Sci., 12, 607, 10.7150/ijbs.14802 · DOI
  38. Ogawa, 2013, Two developmental switch points for the wing polymorphisms in the pea aphid Acyrthosiphon pisum, EvoDevo, 4, 30, 10.1186/2041-9139-4-30 · DOI
  39. Furuyama, 2000, Identification of the differential distribution patterns of mRNAs and consensus binding sequences for mouse DAF-16 homologues, Biochem. J., 349, 629, 10.1042/bj3490629 · DOI
  40. Xuan, 2005, From worm to human: bioinformatics approaches to identify FOXO target genes, Mech. Ageing Dev., 126, 209, 10.1016/j.mad.2004.09.021 · DOI
  41. Brass, 2021, Phenotypic plasticity as a cause and consequence of population dynamics, Ecol. Lett., 24, 2406, 10.1111/ele.13862 · DOI
  42. Topaz, 2012, Locust dynamics: behavioral phase change and swarming, PLoS Comput. Biol., 8, 10.1371/journal.pcbi.1002642 · DOI
  43. Vellichirammal, 2016, The genomewide transcriptional response underlying the pea aphid wing polyphenism, Mol. Ecol., 25, 4146, 10.1111/mec.13749 · DOI
  44. Seal, 2016, Do the distinct synaptic properties of VGLUTs shape pain?, Neurochem. Int., 98, 82, 10.1016/j.neuint.2016.04.016 · DOI
  45. Seal, 2009, Injury-induced mechanical hypersensitivity requires C-low threshold mechanoreceptors, Nature, 462, 651, 10.1038/nature08505 · DOI
  46. Tong, 2001, Vesicular glutamate transporter 2 in the brain–gut axis, Neuroreport, 12, 3929, 10.1097/00001756-200112210-00015 · DOI
  47. Uehara, 2006, Vesicular storage and secretion of L-glutamate from glucagon-like peptide 1-secreting clonal intestinal L cells, J. Neurochem., 96, 550, 10.1111/j.1471-4159.2005.03575.x · DOI
  48. Baj, 2019, Glutamatergic signaling along the microbiota-gut-brain axis, Int. J. Mol. Sci., 20, 1482, 10.3390/ijms20061482 · DOI
  49. Hnasko, 2012, Ventral tegmental area glutamate neurons: electrophysiological properties and projections, J. Neurosci., 32, 15076, 10.1523/JNEUROSCI.3128-12.2012 · DOI
  50. Trudeau, 2018, Glutamate cotransmission in cholinergic, GABAergic and monoamine systems: contrasts and commonalities, Front. Neural Circuits, 12, 113, 10.3389/fncir.2018.00113 · DOI
  51. Aguilar, 2017, Neuronal depolarization drives increased dopamine synaptic vesicle loading via VGLUT, Neuron, 95, 1074, 10.1016/j.neuron.2017.07.038 · DOI
  52. Ibrahim, 2020, Targeting Vesicular Glutamate Transporter Machinery: Implications on Metabotropic Glutamate Receptor 5 Signaling and Behavior, Mol. Pharmacol., 98, 314, 10.1124/molpharm.120.000089 · DOI
  53. Huang, 1991, The emergence of sense organs in the wing disc of Drosophila, Development, 111, 1087, 10.1242/dev.111.4.1087 · DOI
  54. Castellanos, 2013, Female-biased dimorphism underlies a female-specific role for post-embryonic Ilp7 neurons in Drosophila fertility, Development, 140, 3915, 10.1242/dev.094714 · DOI · Paper page
  55. Deshpande, 2022, Regulation of Drosophila oviduct muscle contractility by octopamine, iScience, 25, 10.1016/j.isci.2022.104697 · DOI
  56. Rodríguez-Valentín, 2006, Oviduct contraction in Drosophila is modulated by a neural network that is both, octopaminergic and glutamatergic, J. Cell. Physiol., 209, 183, 10.1002/jcp.20722 · DOI
  57. Ferraguti, 2006, Metabotropic glutamate receptors, Cell Tissue Res., 326, 483, 10.1007/s00441-006-0266-5 · DOI
  58. Liu, 2020, Ultrabithorax is a key regulator for the dimorphism of wings, a main cause for the outbreak of planthoppers in rice, Natl. Sci. Rev., 7, 1181, 10.1093/nsr/nwaa061 · DOI
  59. Hartl, 2014, Wing tips: The wing disc as a platform for studying Hedgehog signaling, Methods, 68, 199, 10.1016/j.ymeth.2014.02.002 · DOI
  60. Neto-Silva, 2009, Mechanisms of growth and homeostasis in the Drosophila wing, Annu. Rev. Cell Dev. Biol., 25, 197, 10.1146/annurev.cellbio.24.110707.175242 · DOI
  61. Bejarano, 2007, Hedgehog restricts its expression domain in the Drosophila wing, EMBO Rep., 8, 778, 10.1038/sj.embor.7401003 · DOI
  62. Briscoe, 2013, The mechanisms of Hedgehog signalling and its roles in development and disease, Nat. Rev. Mol. Cell Biol., 14, 416, 10.1038/nrm3598 · DOI · Paper page
  63. Ishikawa, 2008, Morphological and histological examination of polyphenic wing formation in the pea aphid Acyrthosiphon pisum (Hemiptera, Hexapoda), Zoomorphology, 127, 121, 10.1007/s00435-008-0057-5 · DOI
  64. Livak, 2001, Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT Method, Methods, 25, 402, 10.1006/meth.2001.1262 · DOI · Paper page
  65. Kliot, 2014, Fluorescence in situ hybridizations (FISH) for the localization of viruses and endosymbiotic bacteria in plant and insect tissues, J. Vis. Exp., 84
  66. Hellman, 2007, Electrophoretic mobility shift assay (EMSA) for detecting protein-nucleic acid interactions, Nat. Protoc., 2, 1849, 10.1038/nprot.2007.249 · DOI
  67. Katoh, 2002, MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform, Nucleic Acids Res., 30, 3059, 10.1093/nar/gkf436 · DOI · Paper page
  68. Capella-Gutiérrez, 2009, trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses, Bioinformatics, 25, 1972, 10.1093/bioinformatics/btp348 · DOI
  69. Minh, 2020, IQ-TREE 2: New Models and Efficient Methods for Phylogenetic Inference in the Genomic Era, Mol. Biol. Evol., 37, 1530, 10.1093/molbev/msaa015 · DOI · Paper page
  70. Letunic, 2021, Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation, Nucleic Acids Res., 49, W293, 10.1093/nar/gkab301 · DOI

Metadata

Authors
Yuan, Y., Wang, Y., Ye, W., Xie, L., Yuan, E., Guo, H., Wang, S., Dong, F., Zhu-Salzman, K., Ge, F., & Sun, Y.
Affiliations
  • Chinese Academy of Sciences (CN)
  • Harvard University (US)
  • Shihezi University (CN)
  • Shandong Academy of Agricultural Sciences (CN)
Corresponding author
  • Ge, Feng
  • Sun, Yucheng
ORCID
Venue
iScience
Publisher
Elsevier BV
Published
2025-06
Volume
28
Issue
6
Pages
112591
ISSN
2589-0042 (ISSN-L)
DOI
10.1016/j.isci.2025.112591
PMC
PMC12145829
OpenAlex
W4410109380
Cited by
2
References
3
Citations by year
2026: 2
FWCI
0.78
Type
journal article
Language
en
Open access
Licence
Locations
  • iScience (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
Funders
  • National Natural Science Foundation of China
  • Ministry of Science and Technology of the People's Republic of China
  • Department of Science and Technology of Shandong Province
  • Shandong Academy of Agricultural Sciences
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
  • Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
Keywords
Acyrthosiphon pisum, wing polymorphism, VGLUT2, mGluR3, glutamate signaling, physical contact, wing development

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review