Characterization and expression analysis of circadian clock genes in the diploid woodland strawberry Fragaria vesca

Article
  • 19 Downloads

Abstract

Strawberry is an economically important fruit crop worldwide. Circadian clock genes are endogenous timers that regulate a wide range of metabolic processes and consequently plant development. However, little is known about the circadian clock genes in strawberry. In the present work, we identified 12 primary circadian clock genes from the diploid woodland strawberry (Fragaria vesca L.) genome. Phylogenetic, conserved motif, and gene structure analyses revealed the evolutionary relationships of strawberry circadian clock genes with homologous genes from other species. Promoter analysis revealed different regulatory elements responding to abiotic and biotic stresses and phytohormones. We characterized the transcript patterns of strawberry circadian clock genes over a 48-h period. The expression patterns of seven circadian clock genes displayed circadian rhythms. We also examined the expression patterns of these genes in response to low-temperature stress and six of them showed an upregulated expression. Interestingly, most of these upregulated genes were highly expressed during the day. Our study reveals the characteristics of primary circadian clock components in diploid woodland strawberry and their responses to low-temperature stress and lays a foundation for future functional studies of these circadian clock genes during the growth and development of diploid woodland strawberry.

Additional key words

Arabidopsis thaliana cold stress gene expression phylogenetic analysis 

Abbreviations

BOA

brother of lux arrhythmo

CCA1

circadian clock-associated 1

CHE

CCA1 hiking expedition

ELF

early flowering

LHY

late elongated hypocotyl

LUX

lux arrhythmo

PRR

pseudo-response regulator

qPCR

quantitative polymerase chain reaction

RVE

REVEILLE

TOC 1

timing of CAB 1

ZTL

ZEITLUPE.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Supplementary material

10535_2018_793_MOESM1_ESM.pdf (1.2 mb)
Supplementary material, approximately 1264 KB.

References

  1. Alabadi, D., Yanovsky, M.J., Mas, P., Harmer, S.L., Kay, S.A.: Critical role for CCA1 and LHY in maintaining circadian rhythmicity in Arabidopsis. - Curr. Biol. 12: 757᾿61, 2002.CrossRefPubMedGoogle Scholar
  2. Bailey, T.L., Boden, M., Buske, F.A., Frith, M., Grant, C.E., Clementi, L., Ren, J., Li, W.W., Noble, W.S.: MEME SUITE: tools for motif discovery and searching. - Nucl. Acids Res. 37: W202–W208, 2009.CrossRefPubMedPubMedCentralGoogle Scholar
  3. Bendix, C., Marshall, C.M., Harmon, F.G.: Circadian clock genes universally control key agricultural traits. - Mol. Plant 8: 1135᾿152, 2015.CrossRefPubMedGoogle Scholar
  4. Calixto, C.P., Waugh, R., Brown, J.W.: Evolutionary relationships among barley and Arabidopsis core circadian clock and clock-associated genes. - J. mol. Evol. 80: 108᾿19, 2015.CrossRefPubMedPubMedCentralGoogle Scholar
  5. Campoli, C., Shtaya, M., Davis, S.J., Von Korff, M.: Expression conservation within the circadian clock of a monocot: natural variation at barley Ppd-H1 affects circadian expression of flowering time genes, but not clock orthologs. - BMC Plant Biol. 12: 97, 2012.CrossRefPubMedPubMedCentralGoogle Scholar
  6. Chinnusamy, V., Zhu, J., Zhu, J. K.: Cold stress regulation of gene expression in plants. - Trends Plant Sci. 12: 444᾿51, 2007.CrossRefPubMedGoogle Scholar
  7. Dong, G.G., Golden, S.S.: How a cyanobacterium tells time. - Curr. Opin. Microbiol. 11: 541᾿46, 2008.CrossRefPubMedPubMedCentralGoogle Scholar
  8. Dong, M.A., Farre, E.M., Thomashow, M.F.: Circadian clockassociated 1 and late elongated hypocotyl regulate expression of the C-repeat binding factor (CBF) pathway in Arabidopsis. - Proc. nat. Acad. Sci. USA 108: 7241᾿246, 2011.CrossRefPubMedPubMedCentralGoogle Scholar
  9. Eriksson, M.E., Webb, A.A.: Plant cell responses to cold are all about timing. - Curr. Opin. Plant Biol. 14: 731᾿37, 2011.CrossRefPubMedGoogle Scholar
  10. Fowler, S., Thomashow, M. F.: Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway. - Plant Cell 14: 1675᾿690, 2002.CrossRefPubMedPubMedCentralGoogle Scholar
  11. Fukushima, A., Kusano, M., Nakamichi, N., Kobayashi, M., Hayashi, N., Sakakibara, H., Mizuno, T., Saito, K.: Impact of clock-associated Arabidopsis pseudo-response regulators in metabolic coordination. - Proc. nat. Acad. Sci. USA 106: 7251᾿256, 2009.CrossRefPubMedPubMedCentralGoogle Scholar
  12. Greenham, K., McClung, C.R.: Integrating circadian dynamics with physiological processes in plants. - Nat. Rev. Genet. 16: 598᾿10, 2015.CrossRefPubMedGoogle Scholar
  13. Gu, T., Ren, S., Wang, Y., Han, Y., Li, Y.: Characterization of DNA methyltransferase and demethylase genes in Fragaria vesca. - Mol. Genet. Genomics 291: 1333᾿345, 2016.CrossRefPubMedGoogle Scholar
  14. Herrero, E., Kolmos, E., Bujdoso, N., Yuan, Y., Wang, M., Berns, M. C., Uhlworm, H., Coupland, G., Saini, R., Jaskolski, M., Webb, A., Goncalves, J., Davis, S. J.: EARLY FLOWERING4 recruitment of EARLY FLOWERING3 in the nucleus sustains the Arabidopsis circadian clock. - Plant Cell 24: 428᾿43, 2012.CrossRefPubMedPubMedCentralGoogle Scholar
  15. Hsu, P.Y., Harmer, S.L.: Wheels within wheels: the plant circadian system. - Trends Plant Sci. 19: 240᾿49, 2014.CrossRefPubMedGoogle Scholar
  16. Hu, B., Jin, J., Guo, A. Y., Zhang, H., Luo, J., Gao, G.: GSDS 2.0: an upgraded gene feature visualization server. - Bioinformatics 31: 1296᾿297, 2015.CrossRefPubMedGoogle Scholar
  17. Ibanez, C., Ramos, A., Acebo, P., Contreras, A., Casado, R., Allona, I., Aragoncillo, C.: Overall alteration of circadian clock gene expression in the chestnut cold response. - PLoS ONE 3: e3567, 2008.CrossRefPubMedPubMedCentralGoogle Scholar
  18. Jung, S., Ficklin, S.P., Lee, T., Cheng, C.H., Blenda, A., Zheng, P., Yu, J., Bombarely, A., Cho, I., Ru, S., Evans, K., Peace, C., Abbott, A.G., Mueller, L.A., Olmstead, M.A., Main, D.: The genome database for Rosaceae (GDR): year 10 update. - Nucl. Acids Res. 42: D1237–D1244, 2014.CrossRefPubMedGoogle Scholar
  19. Lamesch, P., Berardini, T.Z., Li, D., Swarbreck, D., Wilks, C., Sasidharan, R., Muller, R., Dreher, K., Alexander, D.L., Garcia-Hernandez, M., Karthikeyan, A.S., Lee, C.H., Nelson, W.D., Ploetz, L., Singh, S., Wensel, A., Huala, E.: The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools. - Nucl. Acids Res. 40: D1202–D1210, 2012.CrossRefPubMedGoogle Scholar
  20. Lescot, M., Dehais, P., Thijs, G., Marchal, K., Moreau, Y., Van de Peer, Y., Rouze, P., Rombauts, S.: PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. - Nucl. Acids Res. 30: 325᾿27, 2002.CrossRefPubMedPubMedCentralGoogle Scholar
  21. Linde, A.-M., Eklund, D.M., Kubota, A., Pederson, E.R.A., Holm, K., Gyllenstrand, N., Nishihama, R., Cronberg, N., Muranaka, T., Oyama, T., Kohchi, T., Lagercrantz, U.: Early evolution of the land plant circadian clock. - New Phytol. 216: 576᾿90, 2017.CrossRefPubMedPubMedCentralGoogle Scholar
  22. Lou, P., Wu, J., Cheng, F., Cressman, L. G., Wang, X., McClung, C. R.: Preferential retention of circadian clock genes during diploidization following whole genome triplication in Brassica rapa. - Plant Cell 24: 2415᾿426, 2012.CrossRefPubMedPubMedCentralGoogle Scholar
  23. Lu, S.X., Webb, C. J., Knowles, S.M., Kim, S.H., Wang, Z., Tobin, E.M.: CCA1 and ELF3 interact in the control of hypocotyl length and flowering time in Arabidopsis. - Plant Physiol. 158: 1079᾿088, 2012.CrossRefPubMedGoogle Scholar
  24. Maibam, P., Nawkar, G.M., Park, J.H., Sahi, V.P., Lee, S.Y., Kang, C.H.: The influence of light quality, circadian rhythm, and photoperiod on the CBF-mediated freezing tolerance. - Int. J. mol. Sci. 14: 11527᾿1543, 2013.CrossRefPubMedPubMedCentralGoogle Scholar
  25. Marcolino-Gomes, J., Rodrigues, F.A., Fuganti-Pagliarini, R., Bendix, C., Nakayama, T.J., Celaya, B., Molinari, H.B.C., De Oliveira, M.C.N., Harmon, F.G., Nepomuceno, A.: Diurnal oscillations of soybean circadian clock and drought responsive genes. - PLoS ONE 9: e86402, 2014.CrossRefPubMedPubMedCentralGoogle Scholar
  26. Mas, P., Kim, W.Y., Somers, D.E., Kay, S.A.: Targeted degradation of TOC1 by ZTL modulates circadian function in Arabidopsis thaliana. - Nature 426: 567᾿70, 2003.CrossRefPubMedGoogle Scholar
  27. Matsushika, A., Makino, S., Kojima, M., Mizuno, T.: Circadian waves of expression of the APRR1/TOC1 family of pseudoresponse regulators in Arabidopsis thaliana: insight into the plant circadian clock. - Plant Cell Physiol. 41: 1002᾿012, 2000.CrossRefPubMedGoogle Scholar
  28. Medina, J., Catala, R., Salinas, J.: The CBFs: three arabidopsis transcription factors to cold acclimate. - Plant Sci. 180: 3᾿1, 2011.CrossRefPubMedGoogle Scholar
  29. Mizoguchi, T., Wheatley, K., Hanzawa, Y., Wright, L., Mizoguchi, M., Song, H.R., Carre, I.A., Coupland, G.: LHY and CCA1 are partially redundant genes required to maintain circadian rhythms in Arabidopsis. - Develop. Cell 2: 629᾿41, 2002.CrossRefGoogle Scholar
  30. Mouhu, K., Hytonen, T., Folta, K., Rantanen, M., Paulin, L., Auvinen, P., Elomaa, P.: Identification of flowering genes in strawberry, a perennial SDplant. - BMC Plant Biol. 9: 122, 2009.CrossRefPubMedPubMedCentralGoogle Scholar
  31. Nakamichi, N., Kiba, T., Henriques, R., Mizuno, T., Chua, N. H., Sakakibara, H.: PSEUDO-RESPONSE REGULATORS 9, 7, and 5 are transcriptional repressors in the Arabidopsis circadian clock. - Plant Cell 22: 594᾿05, 2010.CrossRefPubMedPubMedCentralGoogle Scholar
  32. Nakamichi, N., Kusano, M., Fukushima, A., Kita, M., Ito, S., Yamashino, T., Saito, K., Sakakibara, H., Mizuno, T.: Transcript profiling of an Arabidopsis PSEUDO RESPONSE REGULATOR arrhythmic triple mutant reveals a role for the circadian clock in cold stress response. - Plant Cell Physiol. 50: 447᾿62, 2009.CrossRefPubMedGoogle Scholar
  33. Nusinow, D.A., Helfer, A., Hamilton, E.E., King, J.J., Imaizumi, T., Schultz, T.F., Farre, E.M., Kay, S.A.: The ELF4-ELF3- LUX complex links the circadian clock to diurnal control of hypocotyl growth. - Nature 475: 398᾿02, 2011.CrossRefPubMedPubMedCentralGoogle Scholar
  34. Pruneda-Paz, J.L., Breton, G., Para, A., Kay, S.A.: A functional genomics approach reveals CHE as a component of the Arabidopsis circadian clock. - Science 323: 1481᾿485, 2009.CrossRefPubMedPubMedCentralGoogle Scholar
  35. Rawat, R., Takahashi, N., Hsu, P.Y., Jones, M.A., Schwartz, J., Salemi, M.R., Phinney, B.S., Harmer, S.L.: REVEILLE8 and PSEUDO-REPONSE REGULATOR5 form a negative feedback loop within the Arabidopsis circadian clock. - PLoS Genet. 7: e1001350, 2011.CrossRefPubMedPubMedCentralGoogle Scholar
  36. Schmittgen, T.D., Livak, K.J.: Analyzing real-time PCR data by the comparative CTmethod. - Natur. Protocols 3: 1101᾿108, 2008.CrossRefGoogle Scholar
  37. Shi, Y., Ding, Y., Yang, S.: Cold signal transduction and its interplay with phytohormones during cold acclimation. - Plant Cell Physiol. 56: 7᾿5, 2015.CrossRefPubMedGoogle Scholar
  38. Shulaev, V., Sargent, D.J., Crowhurst, R.N., Mockler, T.C., Folkerts, O., Delcher, A.L., Jaiswal, P., Mockaitis, K., Liston, A., Mane, S.P., Burns, P., Davis, T.M., Slovin, J.P., Bassil, N., Hellens, R.P., Evans, C., Harkins, T., Kodira, C., Desany, B., Crasta, O.R., Jensen, R.V., Allan, A.C., Michael, T.P., Setubal, J.C., Celton, J.M., Rees, D.J., Williams, K.P., Holt, S.H., Ruiz Rojas, J.J., Chatterjee, M., Liu, B., Silva, H., Meisel, L., Adato, A., Filichkin, S.A., Troggio, M., Viola, R., Ashman, T.L., Wang, H., Dharmawardhana, P., Elser, J., Raja, R., Priest, H.D., Bryant, D.W., Jr., Fox, S.E., Givan, S.A., Wilhelm, L.J., Naithani, S., Christoffels, A., Salama, D.Y., Carter, J., Lopez Girona, E., Zdepski, A., Wang, W., Kerstetter, R.A., Schwab, W., Korban, S.S., Davik, J., Monfort, A., Denoyes- Rothan, B., Arus, P., Mittler, R., Flinn, B., Aharoni, A., Bennetzen, J.L., Salzberg, S.L., Dickerman, A.W., Velasco, R., Borodovsky, M., Veilleux, R.E., Folta, K.M.: The genome of woodland strawberry (Fragaria vesca). - Nat. Genet. 43: 109᾿16, 2011.CrossRefPubMedGoogle Scholar
  39. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., Kumar, S.: MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. - Mol. Biol. Evol. 28: 2731᾿739, 2011.CrossRefPubMedPubMedCentralGoogle Scholar
  40. Wang, Y.Q., Ni, X., Yan, J., Yang, L.: Modeling transcriptional co-regulation of mammalian circadian clock. - Math. Biosci. Eng. 14: 1447᾿462, 2017.CrossRefPubMedGoogle Scholar
  41. Wei, W., Hu, Y., Cui, M.Y., Han, Y.T., Gao, K., Feng, J.Y.: Identification and transcript analysis of the TCP transcription factors in the diploid woodland strawberry Fragaria vesca. - Front. Plant Sci. 7: 1937, 2016.PubMedPubMedCentralGoogle Scholar
  42. Yang, Y., Peng, Q., Chen, G.X., Li, X.H., Wu, C.Y.: OsELF3 is involved in circadian clock regulation for promoting flowering under long-day conditions in rice. - Mol. Plant 6: 202᾿15, 2013.CrossRefPubMedGoogle Scholar

Copyright information

© The Institute of Experimental Botany 2018

Authors and Affiliations

  1. 1.Institute of Pomology, Jiangsu Academy of Agricultural Sciences and Jiangsu Key Laboratory for HorticulturalCrop Genetic ImprovementNanjingP.R. China

Personalised recommendations