Skip to main content
Log in

Genome-Wide Identification and Comparative Analysis of Elongation of Very Long-Chain Fatty Acid (Elovl) Genes in Echinoderms

  • GENERAL GENETICS
  • Published:
Russian Journal of Genetics Aims and scope Submit manuscript

Abstract

Elongation of very long-chain fatty acid (Elovl) proteins is the critical rate-limiting enzyme that catalyzes the biosynthesis of long-chain polyunsaturated fatty acids (LC-PUFAs). Echinoderms are extremely important research objects in various fields, such as regeneration studies and developmental biology. However, to date, the genome-wide characterization and analysis of Elovl genes in echinoderms have not been investigated. In this study, the identification and analysis of Elovl genes in 10 representative echinoderms were performed using bioinformatics methods. A total of 117 Elovl genes have been found in the studied echinoderms. The phylogenetic tree showed that all Elovl genes from echinoderms can be subdivided into 6 classes, Elovl3-like class, Elovl4-like class, Elovl5-like class, Elovl6-like class, Elovl7-like class, and Elovl8-like class. Furthermore, the selection pressure analysis suggested that Elovl genes in echinoderms were mainly constrained by strong purifying selection events. In general, this study provides a molecular basis for echinoderm Elovl genes and may serve as a reference for in-depth phylogenomics.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.

DATA AVAILABILITY

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

REFERENCES

  1. Leonard, A.E., Pereira, S.L., Sprecher, H., et al., Elongation of long-chain fatty acids, Prog. Lipid Res., 2004, vol. 43, no. 1, pp. 36—54. https://doi.org/10.1016/s0163-7827(03)00040-7

    Article  CAS  PubMed  Google Scholar 

  2. Jakobsson, A., Westerberg, R., and Jacobsson, A., Fatty acid elongases in mammals: their regulation and roles in metabolism, Prog. Lipid Res., 2006, vol. 45, no. 3, pp. 237—249. https://doi.org/10.1016/j.plipres.2006.01.004

    Article  CAS  PubMed  Google Scholar 

  3. Castro, L.F., Tocher, D.R., and Monroig, O., Long-chain polyunsaturated fatty acid biosynthesis in chordates: insights into the evolution of Fads and Elovl gene repertoire, Prog. Lipid Res., 2016, vol. 62, pp. 25—40. https://doi.org/10.1016/j.plipres.2016.01.001

    Article  CAS  PubMed  Google Scholar 

  4. Jump, D.B., Mammalian fatty acid elongases, Methods Mol. Biol., 2009, vol. 579, pp. 375—389. https://doi.org/10.1007/978-1-60761-322-0_19

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Guillou, H., Zadravec, D., Martin, P.G., et al., The key roles of elongases and desaturases in mammalian fatty acid metabolism: insights from transgenic mice, Prog. Lipid Res., 2010, vol. 49, no. 2, pp. 186—199. https://doi.org/10.1016/j.plipres.2009.12.002

    Article  CAS  PubMed  Google Scholar 

  6. Ferraz, R.B., Paixão, R.V., Lopes-Marques, M., et al., The repertoire of the elongation of very long-chain fatty acids (Elovl) protein family is conserved in tambaqui (Colossoma macropomum): gene expression profiles offer insights into the sexual differentiation process, Comp. Biochem. Physiol., Part B: Biochem. Mol. Biol., 2022, vol. 261, p. 110749. https://doi.org/10.1016/j.cbpb.2022.110749

    Article  CAS  Google Scholar 

  7. Pasquier, J., Cabau, C., Nguyen, T., et al., Gene evolution and gene expression after whole genome duplication in fish: the PhyloFish database, BMC Genomics, 2016, vol. 17, p. 368. https://doi.org/10.1186/s12864-016-2709-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Liu, S., Li, X., Qi, D., et al., Genome-wide characterization of the Elovl gene family in Gymnocypris przewalskii and their potential roles in adaptation to cold temperature, Comp. Biochem. Physiol., Part B: Biochem. Mol. Biol., 2022, vol. 262, p. 110759. https://doi.org/10.1016/j.cbpb.2022.110759

    Article  CAS  Google Scholar 

  9. Zuo, W., Li, C., Luan, Y., et al., Genome-wide identification and analysis of elongase of very long chain fatty acid genes in the silkworm, Bombyx mori, Genome, 2018, vol. 61, no. 3, pp. 167—176. https://doi.org/10.1139/gen-2017-0224

    Article  CAS  PubMed  Google Scholar 

  10. Jung, A., Hollmann, M., and Schäfer, M.A., The fatty acid elongase NOA is necessary for viability and has a somatic role in Drosophila sperm development, J. Cell Sci., 2007, vol. 120, no. 16, pp. 2924—2934. https://doi.org/10.1242/jcs.006551

    Article  CAS  PubMed  Google Scholar 

  11. Sun, S., Wang, Y., Goh, P.T., et al., Evolution and functional characteristics of the novel elovl8 that play pivotal roles in fatty acid biosynthesis, Genes (Basel), 2021, vol. 12, no. 8. https://doi.org/10.3390/genes12081287

  12. Ofman, R., Dijkstra, I.M., van Roermund, C.W., et al., The role of ELOVL1 in very long-chain fatty acid homeostasis and X-linked adrenoleukodystrophy, EMBO Mol. Med., 2010, vol. 2, no. 3, pp. 90—97. https://doi.org/10.1002/emmm.201000061

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Bhandari, S., Lee, J.N., Kim, Y.I., et al., The fatty acid chain elongase, Elovl1, is required for kidney and swim bladder development during zebrafish embryogenesis, Organogenesis, 2016, vol. 12, no. 2, pp. 78—93. https://doi.org/10.1080/15476278.2016.1172164

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Tanaka, K., Kandori, S., Sakka, S., et al., ELOVL2 promotes cancer progression by inhibiting cell apoptosis in renal cell carcinoma, Oncol. Rep., 2022, vol. 47, no. 2. https://doi.org/10.3892/or.2021.8234

  15. Zadravec, D., Tvrdik, P., Guillou, H., et al., ELOVL2 controls the level of n-6 28:5 and 30:5 fatty acids in testis, a prerequisite for male fertility and sperm maturation in mice, J. Lipid Res., 2011, vol. 52, no. 2, pp. 245—255. https://doi.org/10.1194/jlr.M011346

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Liu, C., Ye, D., Wang, H., et al., Elovl2 but not Elovl5 is essential for the biosynthesis of docosahexaenoic acid (DHA) in zebrafish: insight from a comparative gene knockout study, Mar. Biotechnol. (New York), 2020, vol. 22, no. 5, pp. 613—619. https://doi.org/10.1007/s10126-020-09992-1

    Article  CAS  Google Scholar 

  17. Zadravec, D., Brolinson, A., Fisher, R.M., et al., Ablation of the very-long-chain fatty acid elongase ELOVL3 in mice leads to constrained lipid storage and resistance to diet-induced obesity, FASEB J., 2010, vol. 24, no. 11, pp. 4366—4377. https://doi.org/10.1096/fj.09-152298

    Article  CAS  PubMed  Google Scholar 

  18. Monroig, Ó., Wang, S., Zhang, L., et al., Elongation of long-chain fatty acids in rabbitfish Siganus canaliculatus: cloning, functional characterisation and tissue distribution of Elovl5- and Elovl4-like elongases, Aquaculture, 2012, vols. 350—353, pp. 63—70. https://doi.org/10.1016/j.aquaculture.2012.04.017

    Article  CAS  Google Scholar 

  19. Carmona-Antoñanzas, G., Tocher, D.R., Taggart, J.B., et al., An evolutionary perspective on Elovl5 fatty acid elongase: comparison of Northern pike and duplicated paralogs from Atlantic salmon, BMC Evol. Biol., 2013, vol. 13, p. 85. https://doi.org/10.1186/1471-2148-13-85

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Zhang, K., Kniazeva, M., Han, M., et al., A 5-bp deletion in ELOVL4 is associated with two related forms of autosomal dominant macular dystrophy, Nat. Genet., 2001, vol. 27, no. 1, pp. 89—93. https://doi.org/10.1038/83817

    Article  CAS  PubMed  Google Scholar 

  21. Di Gregorio, E., Borroni, B., Giorgio, E., et al., ELOVL5 mutations cause spinocerebellar ataxia 38, Am. J. Hum. Genet., 2014, vol. 95, no. 2, pp. 209—217. https://doi.org/10.1016/j.ajhg.2014.07.001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Mir, H., Raza, S.I., Touseef, M., et al., A novel recessive mutation in the gene ELOVL4 causes a neuro-ichthyotic disorder with variable expressivity, BMC Med. Genet., 2014, vol. 15, p. 25. https://doi.org/10.1186/1471-2350-15-25

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Matsuzaka, T., Kuba, M., Koyasu, S., et al., Hepatocyte ELOVL fatty acid elongase 6 determines ceramide acyl-chain length and hepatic insulin sensitivity in mice, Hepatology, 2020, vol. 71, no. 5, pp. 1609—1625. https://doi.org/10.1002/hep.30953

    Article  CAS  PubMed  Google Scholar 

  24. Li, Y., Wen, Z., You, C., et al., Genome wide identification and functional characterization of two LC-PUFA biosynthesis elongase (elovl8) genes in rabbitfish (Siganus canaliculatus), Aquaculture, 2020, vol. 522, p. 735127. https://doi.org/10.1016/j.aquaculture.2020.735127

    Article  CAS  Google Scholar 

  25. Kalinin, V.I., Echinoderms metabolites: structure, functions, and biomedical perspectives, Mar. Drugs, 2021, vol. 19, no. 3. https://doi.org/10.3390/md19030125

  26. Medina-Feliciano, J.G. and García-Arrarás, J.E., Regeneration in echinoderms: molecular advancements, Front. Cell. Dev. Biol., 2021, vol. 9, p. 768641. https://doi.org/10.3389/fcell.2021.768641

    Article  PubMed  PubMed Central  Google Scholar 

  27. Wei, Z., Liu, X., Zhou, Z., et al., De novo transcriptomic analysis of gonad of Strongylocentrotus nudus and gene discovery for biosynthesis of polyunsaturated fatty acids, Genes Genomics, 2019, vol. 41, no. 5, pp. 583—597. https://doi.org/10.1007/s13258-019-00799-6

    Article  CAS  PubMed  Google Scholar 

  28. Finn, R.D., Mistry, J., Tate, J., et al., The Pfam protein families database, Nucleic Acids Res,, 2010, vol. 38, database issue, pp. D211—D222. https://doi.org/10.1093/nar/gkp985

  29. Finn, R.D., Clements, J., and Eddy, S.R., HMMER web server: interactive sequence similarity searching, Nucleic Acids Res., 2011, vol. 39, web server issue, pp. W29—W37. https://doi.org/10.1093/nar/gkr367

  30. Letunic, I., Doerks, T., and Bork, P., SMART 7: recent updates to the protein domain annotation resource, Nucleic Acids Res., 2012, vol. 40, database issue, pp. D302—D305. https://doi.org/10.1093/nar/gkr931

  31. Gasteiger, E., Hoogland, C., Gattiker, A., et al., Protein Identification and Analysis Tool on the ExPASy Server, 2007. pp. 571—607.

    Google Scholar 

  32. Katoh, K. and Standley, D.M., MAFFT multiple sequence alignment software version 7: improvements in performance and usability, Mol. Biol. Evol., 2013, vol. 30, no. 4, pp. 772—780.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Nguyen, L.-T., Schmidt, H.A., von Haeseler, A., et al., IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies, Mol. Biol. Evol., 2015, vol. 32, no. 1, pp. 268—274.

    Article  CAS  PubMed  Google Scholar 

  34. Nguyen, L.-T., Schmidt, H.A., von Haeseler, A., et al., IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies, Mol. Biol. Evol., 2015, vol. 32, no. 1, pp. 268—274. https://doi.org/10.1093/molbev/msu300

    Article  CAS  PubMed  Google Scholar 

  35. Chen, C., Chen, H., Zhang, Y., et al., TBtools: an integrative toolkit developed for interactive analyses of big biological data, Mol. Plant, 2020, vol. 13, no. 8, pp. 1194—1202. https://doi.org/10.1016/j.molp.2020.06.009

    Article  CAS  PubMed  Google Scholar 

  36. Bailey, T.L., Johnson, J., Grant, C.E., et al., The MEME suite, Nucleic Acids Res., 2015, vol. 43, no. W1, pp. W39—W49. https://doi.org/10.1093/nar/gkv416

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Yang, Z., PAML: a program package for phylogenetic analysis by maximum likelihood, Comput. Appl. Biosci., 1997, vol. 13, no. 5, pp. 555—556. https://doi.org/10.1093/bioinformatics/13.5.555

    Article  CAS  PubMed  Google Scholar 

  38. Monroig, O., Rotllant, J., Cerdá-Reverter, J.M., et al., Expression and role of Elovl4 elongases in biosynthesis of very long-chain fatty acids during zebrafish Danio rerio early embryonic development, Biochim. Biophys. Acta, 2010, vol. 1801, no. 10, pp. 1145—1154. https://doi.org/10.1016/j.bbalip.2010.06.005

    Article  CAS  PubMed  Google Scholar 

  39. Xue, X., Feng, C.Y., Hixson, S.M., et al., Characterization of the fatty acyl elongase (elovl) gene family, and hepatic elovl and delta-6 fatty acyl desaturase transcript expression and fatty acid responses to diets containing camelina oil in Atlantic cod (Gadus morhua), Comp. Biochem. Physiol., Part B: Biochem. Mol. Biol., 2014, vol. 175, pp. 9—22. https://doi.org/10.1016/j.cbpb.2014.06.005

    Article  CAS  Google Scholar 

  40. Xu, J., Liu, D., Yin, H., et al., Fatty acids promote bovine skeletal muscle satellite cell differentiation by regulating ELOVL3 expression, Cell Tissue Res., 2018, vol. 373, no. 2, pp. 499—508. https://doi.org/10.1007/s00441-018-2812-3

    Article  CAS  PubMed  Google Scholar 

  41. Wilkerson, A., Bhat, N., Quoc Hai Pham, H., et al., Physiological effects of inactivation and the roles of Elovl3/ELOVL3 in maintaining ocular homeostasis, FASEB J., 2021, vol. 35, no. 2, p. e21327. https://doi.org/10.1096/fj.202002323R

    Article  CAS  PubMed  Google Scholar 

  42. Su, Y.C., Feng, Y.H., Wu, H.T., et al., Elovl6 is a negative clinical predictor for liver cancer and knockdown of Elovl6 reduces murine liver cancer progression, Sci. Rep., 2018, vol. 8, no. 1, p. 6586. https://doi.org/10.1038/s41598-018-24633-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Fan, X., Zhu, W., Qiu, L., et al., Elongase of very long chain fatty acids 6 (ELOVL6) promotes lipid synthesis in buffalo mammary epithelial cells, J. Anim. Physiol. Anim. Nutr. (Berlin), 2022, vol. 106, no. 1, pp. 1—11. https://doi.org/10.1111/jpn.13536

    Article  CAS  Google Scholar 

  44. Li, Y., Pang, Y., Zhao, Z., et al., Molecular characterization, nutritional and insulin regulation of Elovl6 in rainbow trout (Oncorhynchus mykiss), Biomolecules, 2020, vol. 10, no. 2. https://doi.org/10.3390/biom10020264

  45. Wang, X., Sun, S., Cao, X., et al., Quantitative phosphoproteomic analysis reveals the regulatory networks of Elovl6 on lipid and glucose metabolism in zebrafish, Int. J. Mol. Sci., 2020, vol. 21, no. 8. https://doi.org/10.3390/ijms21082860

  46. Chen, J., Cui, Y., Yan, J., et al., Molecular characterization of elongase of very long-chain fatty acids 6 (elovl6) genes in Misgurnus anguillicaudatus and their potential roles in adaptation to cold temperature, Gene, 2018, vol. 666, pp. 134—144. https://doi.org/10.1016/j.gene.2018.05.019

    Article  CAS  PubMed  Google Scholar 

  47. Zhukova, N.V., Fatty acids of echinoderms: diversity, current applications and future opportunities, Mar. Drugs, 2022, vol. 21, no. 1. https://doi.org/10.3390/md21010021

  48. Chen, S., Hu, Z., He, H., et al., Fatty acid elongase7 is regulated via SP1 and is involved in lipid accumulation in bovine mammary epithelial cells, J. Cell Physiol., 2018, vol. 233, no. 6, pp. 4715—4725. https://doi.org/10.1002/jcp.26255

    Article  CAS  PubMed  Google Scholar 

  49. Takagi, T., Eaton, C.A., Ackman, R.G.J.C.J.o.F., et al., Distribution of fatty acids in lipids of the common atlantic sea urchin Strongylocentrotus droebachiensis, 1980, vol. 37, pp. 195—202.

  50. Cook, E.J., Bell, M.V., Black, K.D., et al., Fatty acid compositions of gonadal material and diets of the sea urchin, Psammechinus miliaris: trophic and nutritional implications, J. Exp. Mar. Biol. Ecol., 2000, vol. 255, no. 2, pp. 261—274. https://doi.org/10.1016/s0022-0981(00)00301-4

    Article  CAS  PubMed  Google Scholar 

  51. Takagi, T., Kaneniwa, M., Itabashi, Y., et al., Fatty acids in echinoidea: unusualcis-5-olefinic acids as distinctive lipid components in sea urchins, Lipids, 1986, vol. 21, no. 9, pp. 558—565. https://doi.org/10.1007/BF02534052

    Article  CAS  Google Scholar 

  52. Siliani, S., Melis, R., Loi, B., et al., Influence of seasonal and environmental patterns on the lipid content and fatty acid profiles in gonads of the edible sea urchin Paracentrotus lividus from Sardinia, Mar. Environ. Res., 2016, vol. 113, pp. 124—133. https://doi.org/10.1016/j.marenvres.2015.12.001

    Article  CAS  PubMed  Google Scholar 

  53. Hayashi, K. and Takagi, T., Occurrence of Branched- and Odd-Chain Fatty Acids in a Mud-Feeding Sea Urchin, Strongylocentrotus franciscanus, 1977.

Download references

Funding

This work was supported by the Open Project Program of Key Laboratory of Ecological Warning, Protection and Restoration for Bohai Sea, Ministry of Natural Resources (2022204), Natural Science Foundation of Shandong Province (ZR2021MC151, ZR2021QD158, ZR2022QC234), and Internal fund project of Yantai Institute of China Agricultural University (Z202303).

Author information

Authors and Affiliations

Authors

Contributions

M.Y.L. conducted the experiment and data processing. X.H.S. conceived and supervised the project. Q.C.W., J.Q.L., D.Z., and J.H.M. contributed to the data collection. All authors reviewed the manuscript.

Corresponding author

Correspondence to X.-H. Shen.

Ethics declarations

ETHICS APPROVAL AND CONSENT TO PARTICIPATE

This work does not contain any studies involving human and animal subjects.

CONFLICT OF INTEREST

The authors of this work declare that they have no conflicts of interest.

Additional information

Publisher’s Note.

Pleiades Publishing remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, MY., Wang, QC., Li, JQ. et al. Genome-Wide Identification and Comparative Analysis of Elongation of Very Long-Chain Fatty Acid (Elovl) Genes in Echinoderms. Russ J Genet 60, 450–459 (2024). https://doi.org/10.1134/S1022795424040070

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1022795424040070

Keywords:

Navigation