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Russian Journal of Genetics

, Volume 55, Issue 2, pp 253–258 | Cite as

Characteristics of INNER NO OUTER Homologous Genes in Wild Tomato Species

  • M. A. FilyushinEmail author
  • M. A. Slugina
  • E. Z. Kochieva
  • A. V. Shchennikova
SHORT COMMUNICATIONS

Abstract

INNER NO OUTER belongs to the YABBY transcription factor family and determines the abaxial identity of the outer ovule integument. In this study, complete genomic INO sequences were identified and characterized in 12 accessions of 11 tomato species (Solanum section Lycopersicon). It was shown that the identified INO genes encode proteins with the conserved zinc finger and YABBY domains. The INO sequences of all analyzed tomato species contain 243 (12.9% of the aligned length) variable sites, 43 of which are exon-specific and include 22 nonsynonymous SNPs leading to amino acid residue substitutions in zinc finger domain (10), YABBY domain (2), and interdomain regions (10). A deletion of 10 aa at the C-terminal interdomain sequence is characteristic of the S. arcanum INO.

Keywords:

INNER NO OUTER (INOSolanum YABBY wild tomato species 

Notes

ACKNOWLEDGMENTS

This study was supported by a grant from the Russian Science Foundation, project no. 16-16-10022, and was performed using the experimental climate control facility located in the Institute of Bioengineering, Research Center of Biotechnology of the Russian Academy of Sciences.

COMPLIANCE WITH ETHICAL STANDARDS

The authors declare that they have no conflict of interest. This article does not contain any studies involving animals or human participants performed by any of the authors.

REFERENCES

  1. 1.
    Skinner, D.J., Brown, R.H., Kuzoff, R.K., and Gasser, C.S., Conservation of the role of INNER NO OUTER in development of unitegmic ovules of the Solanaceae despite a divergence in protein function, BMC Plant Biol., 2016, vol. 16, article 143.  https://doi.org/10.1186/s12870-016-0835-z CrossRefGoogle Scholar
  2. 2.
    Nakayama, H., Yamaguchi, T., and Tsukaya, H., Expression patterns of AaDL, a CRABS CLAW ortholog in Asparagus asparagoides (Asparagaceae), demonstrate a stepwise evolution of CRC/DL subfamily of YABBY genes, Am. J. Bot., 2010, vol. 97, no. 4, pp. 591—600.  https://doi.org/10.3732/ajb.0900378 CrossRefGoogle Scholar
  3. 3.
    Simon, M.K., Skinner, D.J., Gallagher, T.L., and Gasser, C.S., Integument development in Arabidopsis depends on interaction of YABBY protein INNER NO OUTER with coactivators and corepressors, Genetics. 2017, vol. 207, no. 4, pp. 1489—1500.  https://doi.org/10.1534/genetics.117.300140 Google Scholar
  4. 4.
    Bowman, J.L. and Smyth, D.R., CRABS CLAW, a gene that regulates carpel and nectary development in Arabidopsis, encodes a novel protein with zinc finger and helix—loop—helix domains, Development, 1999, vol. 126, pp. 2387—2396.Google Scholar
  5. 5.
    Meister, R.J., Oldenhof, H., Bowman, J.L., and Gasser, C.S., Multiple protein regions contribute to differential activities of YABBY proteins in reproductive development, Plant Physiol., 2005, vol. 137, no. 2, pp. 651—662.  https://doi.org/10.1104/pp.104.055368 CrossRefGoogle Scholar
  6. 6.
    Finet, C., Floyd, S.K., Conway, S.J., et al., Evolution of the YABBY gene family in seed plants, Evol. Dev., 2016, vol. 18, no. 2, pp. 116—126.  https://doi.org/10.1111/ede.12173 CrossRefGoogle Scholar
  7. 7.
    Yamada, T., Yokota, S., Hirayama, Y., et al., Ancestral expression patterns and evolutionary diversification of YABBY genes in angiosperms, Plant J., 2011, vol. 67, no. 1, pp. 26—36.  https://doi.org/10.1111/j.1365-313X.2011.04570.x CrossRefGoogle Scholar
  8. 8.
    Simon, M.K., Williams, L.A., Brady-Passerini, K., et al., Positive- and negative-acting regulatory elements contribute to the tissue-specific expression of INNER NO OUTER, a YABBY-type transcription factor gene in Arabidopsis, BMC Plant Biol., 2012, vol. 12, article 214.  https://doi.org/10.1186/1471-2229-12-214 CrossRefGoogle Scholar
  9. 9.
    Lee, J.Y., Baum, S.F., Oh, S.H., et al., Recruitment of CRABS CLAW to promote nectary development within the eudicot clade, Development, 2005, vol. 132, pp. 5021—5032.CrossRefGoogle Scholar
  10. 10.
    Sun, W., Huang, W., Li, Z., et al., Characterization of a Crabs Claw gene in basal eudicot species Epimedium sagittatum (Berberidaceae), Int. J. Mol. Sci., 2013, vol. 14, no. 1, pp. 1119—1131.  https://doi.org/10.3390/ijms14011119 CrossRefGoogle Scholar
  11. 11.
    Toriba, T., Harada, K., Takamura, A., et al., Molecular characterization the YABBY gene family in Oryza sativa and expression analysis of OsYABBY1, Mol. Genet. Genomics, 2007, vol. 277, no. 5, pp. 457—468.CrossRefGoogle Scholar
  12. 12.
    Shchennikova, A.V., Slugina, M.A., Beletsky, A.V., et al., The YABBY genes of leaf and leaf-like organ polarity in leafless plant Monotropa hypopitys, Int. J. Genomics, 2018, vol. 2018, article ID 7203469.  https://doi.org/10.1155/2018/7203469 CrossRefGoogle Scholar
  13. 13.
    Gallagher, T.L. and Gasser, C.S., Independence and interaction of regions of the INNER NO OUTER protein in growth control during ovule development, Plant Physiol., 2008, vol. 147, no. 1, pp. 306—315.  https://doi.org/10.1104/pp.107.114603 CrossRefGoogle Scholar
  14. 14.
    Peralta, I.E., Spooner, D.M., and Knapp, S., Taxonomy of wild tomatoes and their relatives (Solanum sect. Lycopersicoides, sect. Juglandifolia, sect. Lycopersicon; Solanaceae), Systematic Botany Monographs American Society of Plant Taxonomists, USA, 2008, vol. 84.Google Scholar
  15. 15.
    Spooner, D.M., Peralta, I.E., and Knapp, S., Comparison of AFLPs with other markers for phylogenetic inference in wild tomatoes [Solanum L. section Lycopersicon (Mill.) Wettst.], Taxon, 2005, vol. 54, pp. 43—61.CrossRefGoogle Scholar
  16. 16.
    Han, H.Q., Liu, Y., Jiang, M.M., et al., Identification and expression analysis of YABBY family genes associated with fruit shape in tomato (Solanum lycopersicum L.), Genet. Mol. Res., 2015, vol. 14, no. 2, pp. 7079—7091.CrossRefGoogle Scholar
  17. 17.
    Ezura, K., Ji-Seong, K., Mori, K., et al., Genome-wide identification of pistil-specific genes expressed during fruit set initiation in tomato (Solanum lycopersicum), PLoS One, 2017, vol. 12, no. 7, article e0180003.  https://doi.org/10.1371/journal.pone.0180003 CrossRefGoogle Scholar
  18. 18.
    Huang, Z., Van Houten, J., Gonzalez, G., et al., Genome-wide identification, phylogeny and expression analysis of SUN, OFP and YABBY gene family in tomato, Mol. Genet. Genomics, 2013, vol. 288, nos. 3—4, pp. 111—129.  https://doi.org/10.1007/s00438-013-0733-0 CrossRefGoogle Scholar
  19. 19.
    Filyushin, M.A., Slugina, M.A., Shchennikova, A.V., and Kochieva, E.Z., YABBY3-orthologous genes in wild tomato species: structure, variability, and expression, Acta Nat., 2017, vol. 9, no. 4 (35), pp. 106—115.Google Scholar
  20. 20.
    Filyushin, M.A., Slugina, M.A., Pyshnaya, O.N., et al., Structure analysis of INNER NO OUTER (INO) homologs in Capsicum species, Russ. J. Genet., 2018, vol. 54, no. 6, pp. 753—757.  https://doi.org/10.1134/S1022795418050034 CrossRefGoogle Scholar
  21. 21.
    Lora, J., Hormaza, J.I., and Herrero, M., Transition from two to one integument in Prunus species: expression pattern of INNER NO OUTER (INO), ABERRANT TESTA SHAPE (ATS) and ETTIN (ETT), New Phytol., 2015, vol. 208, no. 2, pp. 584—595.  https://doi.org/10.1111/nph.13460 CrossRefGoogle Scholar
  22. 22.
    Aflitos, S., Schijlen, E., de Jong, H., et al., Exploring genetic variation in the tomato (Solanum section Lycopersicon) clade by whole-genome sequencing, Plant J., 2014, vol. 80, no. 1, pp. 136—148.CrossRefGoogle Scholar
  23. 23.
    Filyushin, M.A., Slugina, M.A., Shchennikova, A.V., and Kochieva, E.Z., Identification and expression analysis of the YABBY1 gene in wild tomato species, Russ. J. Genet., 2018, vol. 54, no. 5, pp. 536—547.  https://doi.org/10.1134/S1022795418050022.CrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Inc. 2019

Authors and Affiliations

  • M. A. Filyushin
    • 1
    Email author
  • M. A. Slugina
    • 1
    • 2
  • E. Z. Kochieva
    • 1
    • 2
  • A. V. Shchennikova
    • 1
  1. 1.Federal Research Center “Fundamentals of Biotechnology,” Russian Academy of SciencesMoscowRussia
  2. 2.Department of Biotechnology, Moscow State UniversityMoscowRussia

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