Russian Journal of Genetics

, Volume 54, Issue 5, pp 536–547 | Cite as

Identification and Expression Analysis of the YABBY1 Gene in Wild Tomato Species

  • M. A. Filyushin
  • M. A. Slugina
  • A. V. Shchennikova
  • E. Z. Kochieva
Plant Genetics


The YABBY1 genes were identified in one cultivated and ten wild tomato species of the Lycopersicon section of the Solanum genus. The structural analysis of genes and encoded proteins was carried out, and the YABBY1 interspecies functional conservation in tomato was proposed. It was shown that the YABBY1 gene sequence can be used for phylogenetic dividing of tomatoes into self- and cross-pollinated species, as well as green- and red-fruited species. The significant YABBY1 expression level was detected in S. peruvianum fruits, indicating the possibility of abaxial properties preservation in the fruit skin. The obtained data confirmed the conservation of the YABBY1-mediated organ polarity control during the process of the evolutionary diversification and domestication of tomato species.


YABBY1 genome analysis Solanum Lycopersicon wild tomato species 


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  1. 1.
    Cronk, Q.C.B., Plant evolution and development in a post-genomic context, Nat. Rev. Genet., 2001, vol. 2, no. 8, pp. 607–619. doi 10.1038/35084556CrossRefPubMedGoogle Scholar
  2. 2.
    Stewart, W.N. and Rothwell, G.W., Paleobotany and the Evolution of Plants, New York: Cambridge University Press, 1993, vol. 12, 2nd ed.Google Scholar
  3. 3.
    Bowman, J.L., Eshed, Y., and Baum, S.F., Establishment of polarity in angiosperm lateral organs, Trends Genet., 2002, vol. 18, no. 3, pp. 134–141. doi 10.1016/S0168-9525(01)02601-4CrossRefPubMedGoogle Scholar
  4. 4.
    Becker, A., Winter, K.U., Meyer, B., et al., MADSBox gene diversity in seed plants 300 million years ago, Mol. Biol. Evol., 2000, vol. 17, no. 10, pp. 1425–1434.CrossRefPubMedGoogle Scholar
  5. 5.
    Husbands, A.Y., Chitwood, D.H., Plavskin, Y., and Timmermans, M.C., Signals and prepatterns: new insights into organ polarity in plants, Genes Dev., 2009, vol. 23, no. 17, pp. 1986–1997. doi 10.1101/gad. 1819909CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Yamaguchi, T., Nukazuka, A., and Tsukaya, H., Leaf adaxial-abaxial polarity specification and lamina outgrowth: evolution and development, Plant Cell Physiol., 2012, vol. 53, no. 7, pp. 1180–1194. doi 10.1093/pcp/pcs074CrossRefPubMedGoogle Scholar
  7. 7.
    Meyerowitz, E.M., Genetic control of cell division patterns in developing plants, Cell, 1997, vol. 88, no. 3, pp. 299–308. doi 10.1016/S0092-8674(00)81868-1CrossRefPubMedGoogle Scholar
  8. 8.
    Floyd, S.K. and Bowman, J.L., The ancestral developmental tool kit of land plants, Int. J. Plant Sci., 2007, vol. 168, no. 1, pp. 1–35. doi 10.1086/509079CrossRefGoogle Scholar
  9. 9.
    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. doi 10.1111/j.1365-313X.2011.04570.xCrossRefPubMedGoogle Scholar
  10. 10.
    Yang, C., Ma, Y., and Li, J., The rice YABBY4 gene regulates plant growth and development through modulating the gibberellin pathway, J. Exp. Bot., 2016, vol. 67, no. 18, pp. 5545–5556. doi 10.1093/jxb/erw319CrossRefPubMedGoogle Scholar
  11. 11.
    Bowman, J.L., The YABBY gene family and abaxial cell fate, Curr. Opin. Plant Biol., 2000, vol. 3, no. 1, pp. 17–22.CrossRefPubMedGoogle Scholar
  12. 12.
    Bartholmes, C., Hidalgo, O., and Gleissberg, S., Evolution of the YABBY gene family with emphasis on the basal eudicot Eschscholzia californica (Papaveraceae), Plant Biol. (Stuttgart), 2012, vol. 14, no. 1, pp. 11–23. doi 10.1111/j.1438-8677.2011.00486.xGoogle Scholar
  13. 13.
    Chen, Q., Atkinson, A., Otsuga, D., et al., The Arabidopsis FILAMENTOUS FLOWER gene is required for flower formation, Development, 1999, vol. 126, no. 12, pp. 2715–2726.PubMedGoogle Scholar
  14. 14.
    Sawa, S., Ito, T., Shimura, Y., and Okada, K., FILAMENTOUS FLOWER controls the formation and development of Arabidopsis inflorescences and floral meristems, Plant Cell, 1999, vol. 11, no. 1, pp. 69–86.PubMedPubMedCentralGoogle Scholar
  15. 15.
    Siegfried, K.R., Eshed, Y., Baum, S.F., et al., Members of the YABBY gene family specify abaxial cell fate in Arabidopsis, Development, 1999, vol. 126, pp. 4117–4128.PubMedGoogle Scholar
  16. 16.
    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. doi 10.1111/ede.12173CrossRefPubMedGoogle Scholar
  17. 17.
    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.PubMedGoogle Scholar
  18. 18.
    Kanaya, E., Nakajima, N., and Okada, K., Nonsequence-specific DNA binding by the FILAMENTOUS FLOWER protein from Arabidopsis thaliana is reduced by EDTA, J. Biol. Chem., 2002, vol. 277, no. 14, pp. 11957–11964. doi 10.1074/jbc.M108889200CrossRefPubMedGoogle Scholar
  19. 19.
    Peralta, I.E., Spooner, D.M., and Knapp, S., Taxonomy of wild tomatoes and their relatives (Solanum sect. Lycopersicoides, sect. Juglandifolia, sect. Lycopersicon; Solanaceae), in Systematic Botany Monographs American Society of Plant Taxonomists, USA, 2008, vol. 84.Google Scholar
  20. 20.
    Sarojam, R., Sapp, P.J., Goldshmidt, A., et al., Differentiating Arabidopsis shoots from leaves by combined YABBY activities, Plant Cell, 2010, vol. 22, no. 7, pp. 2113–2130. doi 10.1105/tpc.110.075853CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    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. doi 10.1007/s00438-013-0733-0CrossRefPubMedGoogle Scholar
  22. 22.
    Filyushin, M.A., Reshetnikova, N.M., Kochieva, E.Z., and Skryabin, K.G., Intraspecific variability of ITS sequences in the parasitic plant Monotropa hypopitys L. from the European Russian populations, Russ. J. Genet., 2015, vol. 51, no. 11, pp. 1149–1152. doi 10.1134/S102279541511006XCrossRefGoogle Scholar
  23. 23.
    Kumar, S., Stecher, G., and Tamura, K., MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets, Mol. Biol. Evol., 2016, vol. 33, no. 7, pp. 1870–1874. doi 10.1093/molbev/msw054CrossRefPubMedGoogle Scholar
  24. 24.
    Grantham, R., Amino acid difference formula to help explain protein evolution, Science, 1974, vol. 185, pp. 862–864.CrossRefPubMedGoogle Scholar
  25. 25.
    Choi, Y., Sims, G.E., Murphy, S., et al., Predicting the functional effect of amino acid substitutions and indels, PLoS One, 2012, vol. 7, no. 10. e46688. doi 10.1371/journal.pone.0046688CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Kelley, L.A., Mezulis, S., Yates, C.M., et al., The Phyre2 web portal for protein modeling, prediction and analysis, Nat. Protoc., 2015, vol. 10, no. 6, pp. 845–858. doi 10.1038/nprot. 2015.053CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Kozlowski, L.P., IPC—Isoelectric Point Calculator, Biol. Direct., 2016, vol. 11, no. 1, p. 55.CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Expósito-Rodríguez, M., Borges, A.A., Borges-Pérez, A., and Pérez, J.A., Selection of internal control genes for quantitative real-time RT-PCR studies during tomato development process, BMC Plant Biol., 2008, vol. 8, no. 131, pp. 1–12.Google Scholar
  29. 29.
    Gangelhoff, T.A., Mungalachetty, P.S., Nix, J.C., and Churchill, M.E., Structural analysis and DNA binding of the HMG domains of the human mitochondrial transcription factor A, Nucleic Acids Res., 2009, vol. 37, no. 10, pp. 3153–3164. doi 10.1093/nar/gkp157CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Hasegawa, M., Kishino, H., and Yano, T., Dating of human-ape splitting by a molecular clock of mitochondrial DNA, J. Mol. Evol., 1985, vol. 22, no. 2, pp. 160–174.CrossRefPubMedGoogle Scholar
  31. 31.
    Tamura, K., Estimation of the number of nucleotide substitutions when there are strong transition—transversion and G+C content biases, Mol. Biol. Evol., 1992, vol. 9, no. 4, pp. 678–687.PubMedGoogle Scholar
  32. 32.
    Knapp, S. and Peralta, I.E., The tomato (Solanum lycopersicum L., Solanaceae) and its botanical relatives, in The Tomato Genome, Compendium of Plant Genomes, Causse, M., Eds., Berlin: Springer-Verlag, 2016.Google Scholar
  33. 33.
    Pease, J.B., Haak, D.C., Hahn, M.W., and Moyle, L.C., Phylogenomics reveals three sources of adaptive variation during a rapid radiation, PLoS Biol., 2016, vol. 14, no. 2. e1002379. doi 10.1371/journal.pbio.1002379CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Igic, B., Lande, R., and Kohn, J.R., Loss of selfincompatibility and its evolutionary consequences, Int. J. Plant Sci., 2008, vol. 169, no. 1, pp. 93–104. doi 10.1086/523362CrossRefGoogle Scholar
  35. 35.
    Miller, J.S. and Kostyun, J.L., Functional gametophytic self-incompatibility in a peripheral population of Solanum peruvianum (Solanaceae), Heredity (Edinburgh), 2011, vol. 107, no. 1, pp. 30–39. doi 10.1038/hdy.2010.151CrossRefGoogle Scholar
  36. 36.
    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. doi 10.4238/2015.June.29.1CrossRefPubMedGoogle Scholar

Copyright information

© Pleiades Publishing, Inc. 2018

Authors and Affiliations

  • M. A. Filyushin
    • 1
  • M. A. Slugina
    • 1
    • 2
  • A. V. Shchennikova
    • 1
  • E. Z. Kochieva
    • 1
    • 2
  1. 1.Institute of Bioengineering, Research Center of BiotechnologyRussian Academy of SciencesMoscowRussia
  2. 2.Moscow State UniversityMoscowRussia

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