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RAS BiologyОнтогенез Russian Journal of Developmental Biology

  • ISSN (Print) 0475-1450
  • ISSN (Online) 3034-6266

Origin and Evolution of ANTP-Class Homeobox Genes

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PII
S0475145025030013-1
DOI
10.31857/S0475145025030013
Publication type
Article
Status
Published
Authors
M. A. Kulakova
  • Affiliation: St. Petersburg State University
Volume/ Edition
Volume 56 / Issue number 3
Pages
95-105
Abstract
Genes of the ANTP class are known as evolutionary conserved and hierarchically high-level regulators of development. They are the most studied and the most numerous homeobox genes in animals. These genes encode homeodomain transcription factors and possess a set of unique features, such as clustering, colinearity, evolutionary conservation, and consistent involvement in various differentiation processes throughout the ontogeny of multicellular animals. The first ANTP genes (from the NK subclass) appear in ctenophores and sponges, which is why the evolution of Metazoa from a common unicellular ancestor is often associated with the emergence of the ANTP class (Larroux et al., 2007; Moroz et al., 2014). Phylogenetic analysis of homeobox genes, conducted across a broad range of basal Metazoa taxa, has shown that ANTP genes from the Hox and ParaHox subclasses arose in the last common ancestor of Cnidaria and Bilateria. These new findings raise further questions. How does the evolution of these clusters correlate with the evolution of animals? What functions were acquired by the new genes, and which were inherited from ancestral NK genes? What changes in their regulation could have influenced the evolution of body plans in Metazoa? Is it even possible to answer these questions by studying modern multicellular organisms? This review aims to address these and other questions regarding the evolution of ANTP gene clusters. Special attention is given to the concept of the “megacluster” — a hypothetical synteny that united all ANTP subclasses at the dawn of Metazoa evolution. The decreasing cost of sequencing technologies offers some hope for answers, as it expands the range of model species available for study. The broader this range, the easier it becomes to identify universal and lineage-specific patterns of molecular and morphological evolution.
Keywords
гомеобоксные гены класс ANTP Hox-кластер ParaHox-кластер NK-кластер метакластер эволюция Bilateria Nephrozoa Cnidaria
Date of publication
18.09.2025
Year of publication
2025
Number of purchasers
0
Views
13

References

  1. 1. Albertin C.B., Medina-Ruiz S., Mitros T. et al. Genome and transcriptome mechanisms driving cephalopod evolution // Nat. Commun. 2022. V. 13(1). Art. no. 2427. https://doi.org/10.1038/s41467-022-29748-w
  2. 2. Azpiazu N., Frasch M. Tinman and bagpipe: Two homeobox genes that determine cell fates in the dorsal mesoderm of Drosophila // Genes Dev. 1993. V. 7(8). P. 1325–1340. https://doi.org/10.1101/gad.7.7b.1325
  3. 3. Avgulewitsch A. Hox in hair growth and development // Naturwissenschaften. 2003 V. 90(5). P. 193–211. https://doi.org/10.1007/s00114-003-0417-4
  4. 4. Battulin N., Fishman V.S., Mazur A.M. et al. Comparison of the three-dimensional organization of sperm and fibroblast genomes using the Hi-C approach // Genome biology. 2015. V. 16. P. 1–15.
  5. 5. Brooke N.M., Garcia-Fernández J., Holland P.W. The ParaHox gene cluster is an evolutionary sister of the Hox gene cluster // Nature. 1998. V. 392(6679). P. 920–922. https://doi.org/10.1038/31933
  6. 6. Bürglin T.R., Affolter M. Homeodomain proteins: An update // Chromosoma. 2016. V. 125(3). P. 497–521. https://doi.org/10.1007/s00412-015-0543-8
  7. 7. Butts T., Holland P.W., Ferrier D.E. The urbilaterian Super-Hox cluster // Trends Genet. 2008. V. 24(6). P. 259–262. https://doi.org/10.1016/j.tig.2007.09.006
  8. 8. Cannon J.T., Vellutini B.C., Smith J. 3rd, Ronquist F., Jondelius U., Hejnol A. Xenacoelomorpha is the sister group to Nephrozoa // Nature. 2016. V. 530(7588). P. 89–93. https://doi.org/10.1038/nature16520
  9. 9. Chan C., Jayasekera S., Kao B., Páramo M., von Grothuss M., Ranz J.M. Remodelling of a homeobox gene cluster by multiple independent gene reunions in Drosophila // Nat. Commun. 2015. V. 6. Art. no. 6509. https://doi.org/10.1038/ncomms7509
  10. 10. Chiori R., Jager M., Denker E., Wincker P., Da Silva C., Le Guyader H., Manuel M., Quéinnec E. Are Hox genes ancestrally involved in axial patterning? Evidence from the hydrozoan Clytia hemisphaerica (Cnidaria). PLoS One. 2009. V. 4(1). Art. no. e4231. https://doi.org/10.1371/journal.pone.0004231
  11. 11. Ferrier D.E.K. Evolution of homeobox gene clusters in animals: the giga-cluster and primary vs. secondary clustering // Frontiers in Ecology and Evolution. 2016. V. 4. P. 36.
  12. 12. Fröbius A.C., Funch P. Rotiferan Hox genes give new insights into the evolution of metazoan bodyplans // Nat. Commun. 2017. V. 8(1). P. 9. https://doi.org/10.1038/s41467-017-00020-w
  13. 13. Garcia-Fernández J. The genesis and evolution of homeobox gene clusters // Nat. Rev. Genet. 2005. V. 6(12). P. 881–892. https://doi.org/10.1038/nrg1723
  14. 14. Guiglielmoni N., Rivera-Vicéns R., Koszul R., Flot J.F. A deep dive into genome assemblies of non-vertebrate animals // Peer Community Journal. 2022. V. 2. Art. no. e29
  15. 15. He S., Del Viso F., Chen C.Y., Ikmi A., Kroesen A.E., Gibson M.C. An axial Hox code controls tissue segmentation and body patterning in Nematostella vectensis // Science. 2018. V. 361(6409). P. 1377–1380. https://doi.org/10.1126/science.aar8384
  16. 16. Hecox-Lea B.J., Mark Welch D.B. Evolutionary diversity and novelty of DNA repair genes in asexual Bdelloid rotifers // BMC Evol. Biol. 2018. V. 18(1). P. 177 https://doi.org/10.1186/s12862-018-1288-9
  17. 17. Holland P.W., Booth H.A., Bruford E.A. Classification and nomenclature of all human homeobox genes // BMC Biol. 2007. V. 5. P. 47. https://doi.org/10.1186/1741-7007-5-47
  18. 18. Holland P.W. Evolution of homeobox genes // Wiley Interdiscip Rev. Dev. Biol. 2013. V. 2(1). P. 31–45 https://doi.org/10.1002/wdev.78
  19. 19. Hombría J.C., García-Ferrés M., Sánchez-Higueras C. Anterior Hox genes and the process of cephalization // Front. Cell Dev. Biol. 2021. V. 9. P. 718175. https://doi.org/10.3389/fcell.2021.718175
  20. 20. Hui J.H., McDougall C., Monteiro A.S., Holland P.W., Arendt D., Balavoine G., Ferrier D.E. Extensive chordate and annelid macrosyntery reveals ancestral homeobox gene organization // Mol. Biol. Evol. 2012. V. 29(1). P. 157–165. https://doi.org/10.1093/molbev/msr175
  21. 21. Ikuta T., Yoshida N., Satoh N., Saiga H. Ciona intestinalis Hox gene cluster: Its dispersed structure and residual colinear expression in development // Proc. Natl. Acad. Sci USA. 2004. V. 101(42). P. 15118–15123. https://doi.org/10.1073/pnas.0401389101
  22. 22. Jagla K., Bellard M., Frasch M. A cluster of Drosophila homeobox genes involved in mesoderm differentiation programs // Bioessays. 2001. V. 23(2). P. 125–133. https://doi.org/10.1002/1521-1878 (200102)23:23.0.CO;2-C
  23. 23. Kaul-Sirehlow S., Urata M., Praher D., Wanninger A. Neuronal patterning of the tubular collar cord is highly conserved among enteropneusts but dissimilar to the chordate neural tube // Sci. Rep. 2017. V. 7(1). P. 7003. https://doi.org/10.1038/s41598-017-07052-8
  24. 24. Khaliurin K., Shinzato C., Khaliurina M. et al. Medusozoan genomes inform the evolution of the jellyfish body plan // Nat. Ecol. Evol. 2019. V. 3(5). V. 811–822. https://doi.org/10.1038/s41559-019-0853-y
  25. 25. Kim Y., Nirenberg M. Drosophila NK-homeobox genes // Proc. Natl. Acad. Sci. U S A. 1989. V. 86(20). P. 7716–7720. https://doi.org/10.1073/pnas.86.20.7716
  26. 26. Kulakova M.A., Cook C.E., Andreeva T.F. ParaHox gene expression in larval and postlarval development of the polychaete Nereis virens (Annelida, Lophotrochozoa) // BMC Dev. Biol. 2008. V. 8. P. 61.
  27. 27. Maconochie M., Nonchev S., Morrison A., Krumlauf R. Paralogous Hox genes: Function and regulation // Annu. Rev. Genet. 1996. V. 30. P. 529–556. https://doi.org/10.1146/annurev.genet.30.1.529
  28. 28. Matus D.Q., Halanych K.M., Martindale M.Q. The Hox gene complement of a pelagic chaetognath, Flaccisagitta enflata // Integr. Comp. Biol. 2007. V. 47(6). P. 854–864. https://doi.org/10.1093/icb/jcm077
  29. 29. Mio C., Baldan F., Damante G. NK2 homeobox gene cluster: Functions and roles in human diseases // Genes Dis. 2022. V. 10(5). P. 2038–2048. https://doi.org/10.1016/j.gendis.2022.10.001
  30. 30. Moroz L.L., Kocot K.M., Citarella M.R. et al. The ctenophore genome and the evolutionary origins of neural systems // Nature. 2014. V. 510(7503). V. 109–114. https://doi.org/10.1038/nature13400
  31. 31. Nong W., Cao J., Li Y., Qu Z. et al. Jellyfish genomes reveal distinct homeobox gene clusters and conservation of small RNA processing // Nat. Commun. 2020. V. 11(1). P. 3051. https://doi.org/10.1038/s41467-020-16801-9
  32. 32. Paps J., Rossi M.E., Bowles A.M.C., Álvarez-Presas M. Assembling animals: Trees, genomes, cells, and contrast to plants // Front. Ecol. Evol. 2023. V. 11. Art. no. 1185566. https://doi.org/10.3389/fevo.2023.1185566
  33. 33. Powers T.P., Amemiya C.T. Evidence for a Hox14 paralog group in vertebrates // Curr. Biol. 2004. V. 14(5). P. R183–184. https://doi.org/10.1016/j.cub.2004.02.015
  34. 34. Ryan J.F., Mazza M.E., Pang K., Matus D.Q., Baxevanis A.D., Martindale M.Q., Finnerty J.R. Pre-bilaterian origins of the Hox cluster and the Hox code: Evidence from the sea anemone, Nematostella vectensis // PLoS One. 2007. V. 2(1). Art. no. e153. https://doi.org/10.1371/journal.pone.0000153
  35. 35. Ryan J.F., Pang K. Mullikin J.C., Martindale M.Q., Baxevanis A.D. The homeodomain complement of the ctenophore Mnemiopsis leidyi suggests that Ctenophora and Porifera diverged prior to the ParaHoxozoa // Evodevo. 2010. V. 1(1). Art. no. 9. https://doi.org/10.1186/2041-9139-1-9
  36. 36. Saudemont A., Dray N., Hudry B., Le Gouar M., Vervoort M., Balavoine G. Complementary striped expression patterns of NK homeobox genes during segment formation in the annelid Platynereis // Dev. Biol. 2008. V. 317(2). P. 430–443. https://doi.org/10.1016/j.ydbio.2008.02.013
  37. 37. Schnitzler C.E., Chang E.S., Waletich J. et al. The genome of the colonial hydroid Hydractinia reveals that their stem cells use a toolkit of evolutionarily shared genes with all animals // Genome Res. 2024. V. 34(3). P. 498–513. https://doi.org/10.1101/gr.278382.123
  38. 38. Seo H.C., Edvardsen R.B., Maeland A.D. et al. Hox cluster disintegration with persistent anteroposterior order of expression in Oikopleura dioica // Nature. 2004. V. 431(7004). P. 67–71. https://doi.org/10.1038/nature02709
  39. 39. Sharkey M., Graba Y., Scott M.P. Hox genes in evolution: Protein surfaces and paralog groups // Trends Genet. 1997. V. 13(4). P. 145–151. https://doi.org/10.1016/s0168-9525 (97)01096-2
  40. 40. Smith J.J., Kraisios P. Hox gene functions in the C. elegans nervous system: From early patterning to maintenance of neuronal identity // Semin. Cell Dev. Biol. 2024. V. 152–153. P. 58–69. https://doi.org/10.1016/j.semcdb.2022.11.012
  41. 41. Suga H., Chen Z., de Mendoza A. et al. The Capaspora genome reveals a complex unicellular prehistory of animals // Nat. Commun. 2013. V. 4. Art. no. 2325 https://doi.org/10.1038/ncomms3325
  42. 42. Technau U., Genikhovich G. Evolution: Directives from sea anemone Hox genes // Curr. Biol. 2018. V. 28(22). P. R1303-R1305. https://doi.org/10.1016/j.cub.2018.09.040
  43. 43. Tomikawa J. Potential roles of inter-chromosomal interactions in cell fate determination // Front. Cell Dev. Biol. 2024. V. 12. Art. no. 1397807. https://doi.org/10.3389/fcell.2024.1397807
  44. 44. Zimmermann B., Montenegro J.D., Robb S.M.C. et al. Topological structures and syntenic conservation in sea anemone genomes // Nat. Commun. 2023. V. 14(1). Art. no. 8270. https://doi.org/10.1038/s41467-023-44080-7
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