Russian Journal of Plant Physiology

, Volume 64, Issue 2, pp 251–259 | Cite as

MiR164 is involved in delaying senescence of strawberry (Fragaria ananassa) fruit by negatively regulating NAC transcription factor genes under low temperature

  • J. Li
  • T. Lai
  • H. Song
  • X. Xu
Research Papers


The miRNAs and their targets involved in senescence of strawberry fruit (Fragaria ananassa L. cv. Zhangji) were analyzed in the present study. In the previous work, three members of miR164 family, mdmmiR164d_ 1ss21AC, mdm-miR164e and mdm-miR164f_1ss21TA, and three of their targets, NAC domain transcriptional regulator superfamily protein, NAC domain containing protein 38 and NAC domain containing protein 87 had been identified by high-throughput sequencing and degradome analysis. In the process of fruit senescence from 0 to 48 h at 4°C storage, the relative levels of mdm-miR164e and mdmmiR164d_1ss21AC expression were significantly increased resulting in decreased expression of NAC genes, and delayed senescence of strawberry fruits. These results suggested that miR164 was involved in strawberry fruit senescence by negatively mediating the expression of NAC transcription factors.


Fragaria ananassa fruit senescence miR164 target gene NAC transcription factors 



Arabidopsis transcription activation factor


cannabinoid receptor


cup-shaped cotyledon


minimum free energy


no apical meristem/ Arabidopsis transcription activation factor/Cup-shaped cotyledon


no apical meristem




Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Bartel, D.P., MicroRNAs: genomics, biogenesis, mechanism, and function, Cell, 2004, vol. 116, pp. 281–297.CrossRefPubMedGoogle Scholar
  2. 2.
    Cherian, S., Figueroa, C.R., and Nair, H., ‘Movers and shakers’ in the regulation of fruit ripening–a cross dissection of climacteric versus non-climacteric fruit, J. Exp. Bot., 2014, vol. 65, pp. 4705–4722.CrossRefPubMedGoogle Scholar
  3. 3.
    Schommer, C., Palatnik, J.F., Aggarwal, P., Chetelat, A., Cubas, P., Farmer, E.E., Nath, U., and Weigel, D., Control of jasmonate biosynthesis and senescence by miR319 targets, PLoS Biol., 2008, vol. 6: e230.CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Kim, J.H., Woo, H.R., Kim, J., Lim, P.O., Lee, I.C., Choi, S.H., Hwang, D., and Nam, H.G., Trifurcate feed-forward regulation of age-dependent cell death involving miR164 in Arabidopsis, Science, 2009, vol. 323, pp. 1053–1057.CrossRefPubMedGoogle Scholar
  5. 5.
    Dalmay, T., Short RNAs in tomato, J. Integr. Plant Biol., 2010, vol. 52, pp. 388–392.CrossRefPubMedGoogle Scholar
  6. 6.
    Addo-Quaye, C., Eshoo, T.W., Bartel, D.P., and Axtell, M.J., Endogenous siRNA and miRNA targets identified by sequencing of the Arabidopsis degradome, Curr. Biol., 2008, vol. 18, pp. 758–762.CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Xu, X.B., Yin, L.L., Ying, Q.C., Song, H.M., Xue, D.W., Lai, T.F., Xu, M.J., Shen, B., Wang, H.Z., and Shi, X.Q., High-throughput sequencing and degradome analysis identify miRNAs and their targets involved in fruit senescence of Fragaria ananassa, PLoS One, 2013, vol. 8, pp. e70959.CrossRefGoogle Scholar
  8. 8.
    Xu, X.B., Ma, X.Y., Lei, H.H., Yin, L.L., Shi, X.Q., and Song, H.M., MicroRNAs play an important role in the regulation of strawberry fruit senescence in low temperature, Postharvest Biol. Technol., 2015, vol. 108, pp. 39–47.CrossRefGoogle Scholar
  9. 9.
    Livak, K.J. and Schmittgen, T.D., Analysis of relative gene expression data using real-time quantitative PCR and the 2–?CT method, Methods, 2001, vol. 25, pp. 402–408.CrossRefPubMedGoogle Scholar
  10. 10.
    Olsen, A.N., Ernst, H.A., Leggio, L.L., and Skriver, K., NAC transcription factors: structurally distinct, functionally diverse, Trends Plant Sci., 2005, vol. 1, pp. 79–87.CrossRefGoogle Scholar
  11. 11.
    Zhong, R., Lee, C., and Ye, Z.H., Global analysis of direct targets of secondary wall NAC master switches in Arabidopsis, Mol. Plant, 2010, vol. 3, pp. 1087–1103.CrossRefPubMedGoogle Scholar
  12. 12.
    Rhoades, M.W., Reinhart, B.J., Lim, L.P., Burge, C.B., Bartel, B., and Bartel, D.P., Prediction of plant microRNA targets, Cell, 2002, vol. 110, pp. 513–520.CrossRefPubMedGoogle Scholar
  13. 13.
    Guo, Y., Cai, Z., and Gan, S., Transcriptome of Arabidopsis leaf senescence, Plant Cell Environ., 2004, vol. 27, pp. 521–549.CrossRefGoogle Scholar
  14. 14.
    Yoon, H.K., Kim, S.G., Kim, S.Y., and Park, C.M., Regulation of leaf senescence by NTL9-mediated osmotic stress signaling in Arabidopsis, Mol. Cells, 2008, vol. 25, pp. 438–445.PubMedGoogle Scholar
  15. 15.
    Balazadeh, S., Siddiqui, H., Allu, A.D., Matallana-Ramirez, L.P., Caldana, C., Mehrnia, M., Zanor, M.I., Köhler, B., and Mueller-Roeber, B., A gene regulatory network controlled by the NAC transcription factor ANAC092/AtNAC2/ORE1 during salt-promoted senescence, Plant J., 2010, vol. 62, pp. 250–264.CrossRefPubMedGoogle Scholar
  16. 16.
    Guo, Y. and Gan, S., AtNAP, a NAC family transcription factor, has an important role in leaf senescence, Plant J., 2006, vol. 46, pp. 601–612.PubMedGoogle Scholar
  17. 17.
    He, X.J., Mu, R.L., Cao, W.H., Zhang, Z.G., Zhang, J.S., and Chen, S.Y., AtNAC2, a transcription factor downstream of ethylene and auxin signaling pathways, is involved in salt stress response and lateral root development, Plant J., 2005, vol. 44, pp. 903–916.CrossRefPubMedGoogle Scholar
  18. 18.
    Takada, S., Hibara, K., Ishida, T., and Tasaka, M., The CUP-SHAPED COTYLEDON1 gene of Arabidopsis regulates shoot apical meristem formation, Development, 2001, vol. 128, pp. 1127–1135.PubMedGoogle Scholar
  19. 19.
    Mallory, A.C., Dugas, D.V., Bartel, D.P., and Bartel, B., MicroRNA regulation of NAC-domain targets is required for proper formation and separation of adjacent embryonic, vegetative, and floral organs, Curr. Biol., 2004, vol. 14, pp. 1035–1046.CrossRefPubMedGoogle Scholar
  20. 20.
    Laufs, P., Peaucelle, A., Morin, H., and Traas, J., MicroRNA regulation of the CUC genes is required for boundary size control in Arabidopsis meristems, Development, 2004, vol. 131, pp. 4311–4322.CrossRefPubMedGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2017

Authors and Affiliations

  1. 1.College of Life and Environmental SciencesHangzhou Normal UniversityHangzhouChina
  2. 2.Tianjin Key Laboratory of Postharvest Physiology and Storage of Agricultural ProductsNational Engineering and Technology Research Center for Preservation of Agricultural ProductsTianjinChina

Personalised recommendations