Разнообразие и эволюция репертуара повторяющихся элементов у двух подвидов медоносной пчелы Apis mellifera

Обложка

Цитировать

Полный текст

Открытый доступ Открытый доступ
Доступ закрыт Доступ предоставлен
Доступ закрыт Доступ платный или только для подписчиков

Аннотация

В настоящем исследовании предпринята попытка установить вклад повторяющихся последовательностей ДНК в формирование социальных структур у медоносных пчел Apis mellifera. Несмотря на прогресс в понимании молекулярных основ кастообразования, в частности связанных с сигнальным путем Notch, идентификация специфических геномных цис-регуляторных элементов остается неполной. Настоящая работа посвящена характеристике ландшафта повторяющихся элементов в геномах двух подвидов медоносной пчелы: A. m. mellifera и A. m. ligustica. Установлено, что увеличение копийности мобильных элементов у A. m. ligustica является существенным различием между исследованными подвидами. Выявлены дифференциально экспрессируемые повторяющиеся элементы, обладающие потенциалом цис-регуляторных функций. Вместе с тем анализ транскриптомов показал минимальные различия в экспрессии мобильных элементов в ходе кастовой дифференциации – ключевого процесса в эусоциальной организации пчел. Анализ расхождения транспозонов между подвидами указывает на последовательные изменения в их повторяющемся статусе, коррелирующие с временем происхождения. В совокупности полученные данные указывают на потенциальную роль повторяющихся элементов в приобретении новых регуляторных функций, что открывает новые перспективы для понимания молекулярных механизмов социального поведения медоносных пчел.

Об авторах

Е. Е. Лебедев

Центр стратегического планирования и управления медико-биологическими рисками здоровью Федерального медико-биологического агентства

Email: mainsalta@gmail.com
Москва, 119121 Россия

Н. В. Панюшев

Институт биоинформатики

Email: mainsalta@gmail.com
Санкт-Петербург, 197342 Россия

Л. С. Адонин

Санкт-Петербургский государственный университет телекоммуникаций им. проф. М.А. Бонч-Бруевича

Автор, ответственный за переписку.
Email: leo.adonin@gmail.com
Санкт-Петербург, 193232 Россия

Список литературы

  1. Aizen M.A., Garibaldi L.A., Cunningham S.A., Klein A.M. How much does agriculture depend on pollinators? Lessons from long-term trends in crop production // Ann. Bot. 2009. V. 103. № 9. P. 1579–1588. https://doi.org/10.1093/aob/mcp076
  2. Christmann S. Do we realize the full impact of pollinator loss on other ecosystem services and the challenges for any restoration in terrestrial areas? // Restoration Ecology. 2019. V. 27. № 4. P. 720–725. https://doi.org/10.1111/rec.12950
  3. Patel V., Pauli N., Biggs E. et al. Why bees are critical for achieving sustainable development // Ambio. 2021. V. 50. № 1. P. 49–59. https://doi.org/10.1007/s13280-020-01333-9
  4. Dangles O., Casas J. Ecosystem services provided by insects for achieving sustainable development goals // Ecosystem Services. 2019. V. 35. P. 109–115. https://doi.org/10.1016/j.ecoser.2018.12.002
  5. Kohno H., Kubo T. Genetics in the honey bee: Achievements and prospects toward the functional analysis of molecular and neural mechanisms underlying social behaviors: 10 // Insects. 2019. V. 10. № 10. https://doi.org/10.3390/insects10100348
  6. Wilson E.O., Hölldobler B. Eusociality: Origin and consequences // Proc. Natl Acad. Sci. USA. 2005. V. 102. № 38. P. 13367–13371. https://doi.org/10.1073/pnas.0505858102
  7. Da Silva J. Life history and the transitions to eusociality in the hymenoptera // Front. Ecol. and Evol. 2021. V. 9.
  8. Ashby R., Forêt S., Searle I., Maleszka R. MicroRNAs in honey bee caste determination // Sci. Rep. 2016. V. 6. https://doi.org/10.1038/srep18794
  9. Alaux C., Sinha S., Hasadsri L. et al. Honey bee aggression supports a link between gene regulation and behavioral evolution // Proc. Natl Acad. Sci. USA. 2009. V. 106. № 36. P. 15400–15405. https://doi.org/10.1073/pnas.0907043106
  10. Greenberg J.K., Xia J., Zhou X. et al. Behavioral plasticity in honey bees is associated with differences in brain microRNA transcriptome: 6 // Genes Brain Behav. 2012. V. 11. № 6. P. 660–670. https://doi.org/10.1111/j.1601-183X.2012.00782.x
  11. Eyer M., Dainat B., Neumann P., Dietemann V. Social regulation of ageing by young workers in the honey bee, Apis mellifera // Exp. Gerontol. 2017. V. 87. Pt. A. P. 84–91. https://doi.org/10.1016/j.exger.2016.11.006
  12. De Paula Junior D.E., de Oliveira M.T., Brusca- din J.J. Caste-specific gene expression underlying the differential adult brain development in the honeybee Apis mellifera // Insect Mol. Biol. 2021. V. 30. № 1. P. 42–56. https://doi.org/10.1111/imb.12671
  13. Wang M., Xiao Y., Li Y., Wang X. RNA m6A Modification functions in larval development and caste differentiation in honeybee (Apis mellifera): 1 // Cell Rep. 2021. V. 34. № 1. https://doi.org/10.1016/j.celrep.2020.108580
  14. Yokoi K., Wakamiya T., Bono H. Meta-analysis of the public RNA-Seq data of the western honeybee Apis mellifera to construct reference transcriptome data // Insects. 2022. V. 13. № 10. https://doi.org/10.3390/insects13100931
  15. Brenman-Suttner D., Zayed A. An integrative genomic toolkit for studying the genetic, evolutionary, and molecular underpinnings of eusociality in insects // Curr. Opin. Insect Sci. 2024. V. 65. https://doi.org/10.1016/j.cois.2024.101231
  16. Smutin D., Taldaev A., Lebedev E., Adonin L. Shotgun metagenomics reveals minor micro“bee”omes diversity defining differences between larvae and pupae brood combs: 2 // Int. J. Mol. Sci. 2024. V. 25. № 2. https://doi.org/10.3390/ijms25020741
  17. Robinson S.D., Schendel V., Schroeder C.I. Intra-colony venom diversity contributes to maintaining eusociality in a cooperatively breeding ant // BMC Biol. 2023. V. 21. № 1. P. 5. https://doi.org/10.1186/s12915-022-01507-9
  18. Kreider J.J., Pen I. The evolution of eusociality: Kin selection theory, division of labour models, and evo-devo explanations // EcoEvoRxiv. 2022.
  19. Mikhailova A.A., Rinke S., Harrison M.C. Genomic signatures of eusocial evolution in insects // Curr. Opin. Insect Sci. 2024. V. 61. https://doi.org/10.1016/j.cois.2023.101136
  20. Gregory T.R., Nicol J.A., Tamm H. Eukaryotic genome size databases // Nucl. Acids Res. 2007. V. 35. P. D332–D338. https://doi.org/10.1093/nar/gkl828
  21. Petersen M., Armisen D., Gibbs R.A. Diversity and evolution of the transposable element repertoire in arthropods with particular reference to insects: 1 // BMC Evol. Biol. 2019. V. 19. № 1. P. 11. https://doi.org/10.1186/s12862-018-1324-9
  22. Jiang F., Yang M., Guo W. et al. Large-scale transcriptome analysis of retroelements in the migratory locust, Locusta migratoria // PLoS One. 2012. V. 7. № 7. https://doi.org/10.1371/journal.pone.0040532
  23. Gilbert C., Peccoud J., Cordaux R. Transposable elements and the evolution of insects // Annu. Rev. Entomol. 2021. V. 66. P. 355–372. https://doi.org/10.1146/annurev-ento-070720-074650
  24. Feschotte C. Transposable elements and the evolution of regulatory networks: 5 // Nat. Rev. Genet. 2008. V. 9. № 5. P. 397–405. https://doi.org/10.1038/nrg2337
  25. Bourque G., Burns K.H., Gehring M. et al. Ten things you should know about transposable elements // Genome Biology. 2018. V. 19. № 1. P. 199. https://doi.org/10.1186/s13059-018-1577-z
  26. Carareto C.M.A., Hernandez E.H., Vieira C. Genomic regions harboring insecticide resistance-associated Cyp genes are enriched by transposable element fragments carrying putative transcription factor binding sites in two sibling Drosophila species // Gene. 2014. V. 537. № 1. P. 93–99. https://doi.org/10.1016/j.gene.2013.11.080
  27. Wu C., Lu J. Diversification of transposable elements in Arthropods and its impact on genome evolution // Genes. 2019. V. 10. № 5. https://doi.org/10.3390/genes10050338
  28. Ellison C.E., Bachtrog D. Dosage compensation via transposable element mediated rewiring of a regulatory network // Science. 2013. V. 342. № 6160. P. 846–850. https://doi.org/10.1126/science.1239552
  29. Pardue M.L., Rashkova S., Casacuberta E. et al. Two retrotransposons maintain telomeres in Drosophila // Chromosome Res. 2005. V. 13. № 5. P. 443–453. https://doi.org/10.1007/s10577-005-0993-6
  30. Jangam D., Feschotte C., Betrán E. Transposable element domestication as an adaptation to evolutionary conflicts: 11 // Trends Genet. 2017. V. 33. № 11. P. 817–831. https://doi.org/10.1016/j.tig.2017.07.011
  31. Sieber K.R., Dorman T., Newell N., Yan H. (Epi)Genetic mechanisms underlying the evolutionary success of eusocial insects // Insects. 2021. V. 12. № 6. https://doi.org/10.3390/insects12060498
  32. Rubin B.E.R., Jones B.M., Hunt B.G., Kocher S.D. Rate variation in the evolution of non-coding DNA associated with social evolution in bees // Philosophical Transactions of the Royal Society. B. Biol. Sci. 2019. V. 374. № 1777. https://doi.org/10.1098/rstb.2018.0247
  33. Lebedev E., Smutin D., Timkin P. et al. The eusocial non-code: Unveiling the impact of noncoding RNAs on Hymenoptera eusocial evolution // Non-coding RNA Res. 2025. V. 11. P. 48–59. https://doi.org/10.1016/j.ncrna.2024.10.007
  34. Berger J., Legendre F., Zelosko K.M. et al. Eusocial transition in Blattodea: transposable elements and shifts of gene expression: 11 // Genes. 2022. V. 13. № 11. https://doi.org/10.3390/genes13111948
  35. Matsuura K., Mizumoto N., Kobayashi K. et al. A Genomic imprinting model of termite caste determination: Not genetic but epigenetic inheritance influences offspring caste fate // Am. Nat. 2018. V. 191. № 6. P. 677–690. https://doi.org/10.1086/697238
  36. Zhang H., Liu Q., Lu J. et al. Genomic and transcriptomic analyses of a social hemipteran provide new insights into insect sociality // Mol. Ecol. Resour. 2024. V. 24. № 8. https://doi.org/10.1111/1755-0998.14019
  37. Dayal S., Chaubey D., Joshi D.C. et al. Noncoding RNAs: Emerging regulators of behavioral complexity // Wiley Interdiscip. Rev. RNA. 2024. V. 15. № 3. https://doi.org/10.1002/wrna.1847
  38. Wojciechowski M., Lowe R., Maleszka J. et al. Phenotypically distinct female castes in honey bees are defined by alternative chromatin states during larval develop- ment // Genome Res. 2018. V. 28. № 10. P. 1532–1542. https://doi.org/10.1101/gr.236497.118
  39. Bray N.L., Pimentel H., Melsted P., Pachter L. Near-optimal probabilistic RNA-Seq quantification // Nat. Biotechnol. 2016. V. 34. P. 525–527. https://doi.org/10.1038/nbt.3519
  40. Love M.I., Huber W., Anders S. Moderated Estimation of frold change and dispersion for RNA-Seq data with DESeq2 // Genome Biol. 2014. V. 15. https://doi.org/10.1186/s13059-014-0550-8
  41. Zhang W., Wang L., Zhao Y. et al. Single-cell transcriptomic analysis of honeybee brains identifies vitellogenin as caste differentiation-related factor // Science. 2022. V. 25. № 7. https://doi.org/10.1016/j.isci.2022.104643
  42. Satija R., Farrell J.A., Gennert D. et al. Spatial reconstruction of single-cell gene expression data: 5 // Nat. Biotechnol. 2015. V. 33. № 5. P. 495–502. https://doi.org/10.1038/nbt.319
  43. Edwards T.N., Meinertzhagen I.A. The functional organisation of glia in the adult brain of Drosophila and other insects // Prog. Neurobiol. 2010. V. 90. № 4. P. 471–497. https://doi.org/10.1016/j.pneurobio.2010.01.001
  44. Allen A.M., Neville M.C., Birtles S. et al. A single-cell transcriptomic atlas of the adult Drosophila ventral nerve cord // Elife. 2020. V. 9. https://doi.org/10.7554/eLife.54074
  45. Davie K., Janssens J., Koldere D. et al. A single-cell transcriptome atlas of the aging Drosophila brain // Cell. 2018. V. 174. № 4. P. 982–998. https://doi.org/10.1016/j.cell.2018.05.057
  46. Robinow S., White K. Characterization and spatial distribution of the ELAV protein during Drosophila melanogaster development // J. Neurobiol. 1991. V. 22. № 5. P. 443–461. https://doi.org/10.1002/neu.480220503
  47. Galizia C.G., Menzel R. Odour perception in honeybees: Coding information in glomerular patterns // Curr. Opin. Neurobiol. 2000. V. 10. № 4. P. 504–510. https://doi.org/10.1016/s0959-4388(00)00109-4
  48. Groh C., Rössler W. Analysis of synaptic microcircuits in the mushroom bodies of the honeybee // Insects. 2020. V. 11. № 1. https://doi.org/10.3390/insects11010043
  49. Roat T.C., Landim C. da C. Mitosis and cell death in the optic lobes of workers, queens and drones of the honey bee (Apis mellifera) during metamorphosis // J. Biosci. 2010. V. 35. № 3. P. 415–425. https://doi.org/10.1007/s12038-010-0047-x
  50. Caron S., Abbott L.F. Neuroscience: Intelligence in the honeybee mushroom body // Curr. Biol. 2017. V. 27. № 6. P. R220–R223. https://doi.org/10.1016/j.cub.2017.02.011
  51. Suenami S., Oya S., Kohno H. Kenyon cell subtypes/populations in the honeybee mushroom bodies: Possible function based on their gene expression profiles, differentiation, possible evolution, and application of genome editing // Front. in Psychology. 2018. V. 9.
  52. Kaneko K., Suenami S., Kubo T. Gene expression profiles and neural activities of Kenyon cell subtypes in the honeybee brain: Identification of novel “middle-type” Kenyon cells // Zoological Lett. 2016. V. 2. P. 14. https://doi.org/10.1186/s40851-016-0051-6
  53. Eleftherianos I., Xu M., Yadi H. et al. Plasmatocyte-spreading peptide (PSP) plays a central role in insect cellular immune defenses against bacterial infection // J. Exp. Biol. 2009. V. 212. № Pt. 12. P. 1840–1848. https://doi.org/10.1242/jeb.026278
  54. Negri P., Maggi M., Ramirez L. et al. Cellular immunity in Apis mellifera: Studying hemocytes brings light about bees skills to confront threats: 3 // Apidologie. 2016. V. 47. № 3. P. 379–388. https://doi.org/10.1007/s13592-015-0418-2
  55. Chak S.T.C., Harris S.E., Hultgren K.M. et al. Eusociality in snapping shrimps is associated with larger genomes and an accumulation of transposable elements // Proc. Natl Acad. Sci. USA. 2021. V. 118. № 24. https://doi.org/ 10.1073/pnas.2025051118
  56. Lawson S.P., Legan A.W., Graham C., Abbot P. Comparative phenotyping across a social transition in aphids // Animal Behaviour. 2014. V. 96. P. 117–125. https://doi.org/10.1016/j.anbehav.2014.08.003
  57. Chapman T.W., Crespi B.J., Kranz B.D., Schwarz M.P. High relatedness and inbreeding at the origin of eusociality in gall-inducing thrips // Proc. Natl Acad. Sci. USA. 2000. V. 97. № 4. P. 1648–1650. https://doi.org/10.1073/pnas.020510097
  58. Biedermann P.H.W., Taborsky M. Larval helpers and age polyethism in ambrosia beetles // Proc. Natl Acad. Sci. USA. 2011. V. 108. № 41. P. 17064–17069. https://doi.org/10.1073/pnas.1107758108
  59. Oeyen J.P., Baa-Puyoulet P., Benoit J.B. Sawfly genomes reveal evolutionary acquisitions that fostered the mega-radiation of parasitoid and eusocial Hymenoptera // Genome Biol. and Evol. 2020. V. 12. № 7. P. 1099–1188. https://doi.org/10.1093/gbe/evaa106
  60. Torres V.O., Montagna T.S., Raizer J., Antonialli-Juni- or W.F. Division of labor in colonies of the eusocial wasp, Mischocyttarus consimilis // J. Insect Sci. 2012. V. 12. P. 21. https://doi.org/10.1673/031.012.2101
  61. Cardinal S., Danforth B.N. The antiquity and evolutionary history of social behavior in bees // PLoS One. 2011. V. 6. № 6. https://doi.org/10.1371/journal.pone.0021086
  62. Favreau E., Martínez-Ruiz C., Rodrigues Santiago L. et al. Genes and genomic processes underpinning the social lives of ants // Curr. Opin. Insect Sci. 2018. V. 25. P. 83–90. https://doi.org/10.1016/j.cois.2017.12.001
  63. Rees-Baylis E., Pen I., Kreider J.J. Maternal manipulation of offspring size can trigger the evolution of eusociality in promiscuous species // Proc. Natl Acad. Sci. USA. 2024. V. 121. № 33. https://doi.org/10.1073/pnas.2402179121
  64. Lagos-Oviedo J.J., Pen I., Kreider J.J. Coevolution of larval signalling and worker response can trigger developmental caste determination in social insects // Proc. Biol. Sci. 2024. V. 291. № 2027. https://doi.org/10.1098/rspb.2024.0538
  65. Ashrafi H., Hultgren K.M. Eusociality unveiled: Discovery and documentation of two new eusocial shrimp species (Caridea: Alpheidae) from the Western Indian Ocean // Arthropod Syst. & Phylogeny. 2023. V. 81. P. 1103–1120. https://doi.org/10.3897/asp.81.e111799
  66. Opachaloemphan C., Yan H., Leibholz A. et al. Recent advances in behavioral (epi)genetics in eusocial insects // Annu. Rev. Genet. 2018. V. 52. P. 489–510. https://doi.org/10.1146/annurev-genet-120116-024456
  67. Berger J., Legendre F., Zelosko K.M. et al. Eusocial transition in Blattodea: Transposable elements and shifts of gene expression // Genes (Basel). 2022. V. 13. № 11. https://doi.org/10.3390/genes13111948
  68. Korb J., Poulsen M., Hu H. et al. A genomic comparison of two termites with different social complexity // Front. Genet. 2015. V. 6. P. 9. https://doi.org/10.3389/fgene.2015.00009
  69. Kapheim K.M., Pan H., Li C. et al. Genomic signatures of evolutionary transitions from solitary to group living // Science. 2015. V. 348. № 6239. P. 1139–1143. https://doi.org/10.1126/science.aaa4788
  70. Fouks B., Brand P., Nguyen H.N. et al. The geno- mic basis of evolutionary differentiation among honey bees // Genome Res. 2021. V. 31. № 7. P. 1203–1215. https://doi.org/10.1101/gr.272310.12
  71. Schartl M., Kneitz S., Volkoff H. et al. The piranha genome provides molecular insight associated to its unique feeding behavior // Genome Biol. Evol. 2019. V. 11. № 8. P. 2099–2106. https://doi.org/10.1093/gbe/evz139
  72. Elsik C.G., Worley K.C., Bennett A.K. et al. Finding the missing honey bee genes: lessons learned from a genome upgrade // BMC Genomics. 2014. V. 15. P. 86. https://doi.org/10.1186/1471-2164-15-86
  73. Song J.L., Stoeckius M., Maaskola J. et al. Select microRNAs are essential for early development in the sea urchin // Dev. Biol. 2012. V. 362. № 1. P. 104–113. https://doi.org/10.1016/j.ydbio.2011.11.015
  74. Santos D., Feng M., Kolliopoulou A. et al. What are the functional roles of piwi proteins and piRNAs in insects? // Insects. 2023. V. 14. № 2. https://doi.org/10.3390/insects14020187
  75. Lukic S., Nicolas J.-C., Levine A.J. The diversity of zinc-finger genes on human chromosome 19 provides an evolutionary mechanism for defense against inherited endogenous retroviruses // Cell Death Differ. 2014. V. 21. № 3. P. 381–387. https://doi.org/10.1038/cdd.2013.150
  76. Baumgartner L., Handler D., Platzer S.W. et al. The Drosophila ZAD zinc finger protein Kipferl guides rhino to piRNA clusters // eLife. 2022. V. 11. https://doi.org/10.7554/eLife.80067
  77. Catlin N.S., Josephs E.B. The important contribution of transposable elements to phenotypic variation and evolution // Curr. Opin. Plant Biol. 2022. V. 65. https://doi.org/10.1016/j.pbi.2021.102140
  78. Wells J.N., Chang N.C., McCormick J. et al. Transposable elements drive the evolution of metazoan zinc finger genes // Genome Res. 2023. V. 33. № 8. P. 1325–1339. https://doi.org/10.1101/gr.277966.123
  79. Harrison M.C., Jongepier E., Robertson H.M. et al. Hemimetabolous genomes reveal molecular basis of termite eusociality: 3 // Nat. Ecol. Evol. 2018. V. 2. № 3. P. 557–566. https://doi.org/10.1038/s41559-017-0459-1
  80. Gebrie A. Transposable elements as essential elements in the control of gene expression // Mob. DNA. 2023. V. 14. № 1. P. 9. https://doi.org/10.1186/s13100-023-00297-3
  81. Sundaram V., Wysocka J. Transposable elements as a potent source of diverse cis-regulatory sequences in mammalian genomes // Philosophical Transactions of the Royal Society. B. Biol. Sci. 2020. V. 375. № 1795. https://doi.org/10.1098/rstb.2019.0347
  82. He J., Babarinde I.A., Sun L. et al. Identifying transposable element expression dynamics and heterogeneity during development at the single-cell level with a processing pipeline scTE: 1 // Nat. Commun. 2021. V. 12. № 1. P. 1456. https://doi.org/10.1038/s41467-021-21808-x
  83. Sekine K., Onoguchi M., Hamada M. Transposons contribute to the acquisition of cell type-specific cis-elements in the brain // Commun. Biol. 2023. V. 6. № 1. P. 631. https://doi.org/10.1038/s42003-023-04989-7
  84. Wang R., Zheng Y., Zhang Z. et al. MATES: A deep learning-based model for locus-specific quantification of transposable elements in single cell // Nat. Commun. 2024. V. 15. № 1. P. 8798. https://doi.org/10.1038/s41467-024-53114-7
  85. Rodríguez-Quiroz R., Valdebenito-Maturana B. Solo TE for improved analysis of transposable elements in single-cell RNA-Seq data using locus-specific expression // Commun. Biol. 2022. V. 5. № 1. P. 1063. https://doi.org/10.1038/s42003-022-04020-5
  86. He J., Babarinde I.A., Sun L. et al. Unveiling transposable element expression heterogeneity in cell fate regulation at the single-cell level // bioRxiv. 2020. P. 2020.07.23.218800.
  87. Treiber C.D., Waddell S. Transposon expression in the Drosophila brain is driven by neighboring genes and diversifies the neural transcriptome // Genome Res. 2020. V. 30. № 11. P. 1559–1569. https://doi.org/10.1101/gr.259200.119

Дополнительные файлы

Доп. файлы
Действие
1. JATS XML
Скачать

© Российская академия наук, 2025