biologia plantarum

International journal on Plant Life established by Bohumil Němec in 1959

Biologia plantarum 61:631-640, 2017 | DOI: 10.1007/s10535-017-0711-1

The identification of almond GIGANTEA gene and its expression under cold stress, variable photoperiod, and seasonal dormancy

P. M. Barros1, S. Cherian1, M. Costa1, H. Sapeta1, N. J. M. Saibo1, M. M. Oliveira1,*
1 Instituto de Tecnologia Química e Biológica António Xavier, Universidade Nova de Lisboa, Oeiras, Portugal

Seasonal growth is characteristic for many tree species including almond. Varying conditions during the season are responsible for growth cessation, bud set, dormancy entry, cold hardening, and bud burst. Here, we report the characterization of an almond homologue of the Arabidopsis GIGANTEA (AtGI) gene (designated as PdGI, GenBank accession No. KJ502316). We propose a role for this gene in the transition to dormancy and cold acclimation. The complementary DNA (cDNA) sequence of PdGI was 4 322 bp long and contained an open reading frame of 3 512 bp. The deduced amino acid sequence of PdGI shared 76 % identity with AtGI. The expression of PdGI at ambient day/night temperatures of 22/20 ºC was differentially regulated under a 16-h or 12-h photoperiod, increasing during the day and decreasing after dusk. However, this diurnal regulation was disrupted when plants were transferred to cold (12 ºC) conditions. In addition, we have assessed the expression of PdGI and putative almond homologues of the downstream target genes CONSTANS (PdCO-like) and FLOWERING LOCUS T (PdFT-like) in flower buds and shoots from adult trees during the bud break period in autumn and early winter. Our results show a clear increase in transcript abundance towards anthesis, suggesting a role of these genes in flower development.

Keywords: bud break; flowering; Prunus dulcis; seasonal development
Subjects: GIGANTEA gene; cold stress; photoperiod; dormancy; bud break; flowering; phylogenetic tree; almond

Received: August 11, 2016; Revised: November 1, 2016; Accepted: November 23, 2016; Published: December 1, 2017  Show citation

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Barros, P.M., Cherian, S., Costa, M., Sapeta, H., Saibo, N.J.M., & Oliveira, M.M. (2017). The identification of almond GIGANTEA gene and its expression under cold stress, variable photoperiod, and seasonal dormancy. Biologia plantarum61(4), 631-640. doi: 10.1007/s10535-017-0711-1
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References

  1. Alonso, J.M., Espiau, M.T., Socias i Company, R.: Increase in the chill and heat requirements for blooming of the new almond cultivars. - In: Zakynthinos, G. (ed.): XIV GREMPA Meeting on Pistachios and Almonds. Zaragoza: CIHEAM / FAO / AUA / TEI Kalamatas / NAGREF. Pp. 65-69 (Options Méditerranéennes: Série A. Séminaires Méditerranéens; n. 94), 2010.
  2. Araki, T., Komeda, Y.: Analysis of the role of the lateflowering locus, Gl, in the flowering of Arabidopsis thaliana. - Plant J. 3: 231-239, 1993. Go to original source...
  3. Arús, P., Gradziel, T., Oliveira, M.M., Tao, R.: Genomics of almond. - In: Folta, K.M., Gardiner, S.E. (ed.): Plant Genetics and Genomics: Crops and Models. Genetics and Genomics of Rosaceae. Vol. 6. Pp 187-219. Springer, New York 2009. Go to original source...
  4. Barros, P.M., Gonçalves, N., Saibo, N.J.M., Oliveira, M.M.: Functional characterization of two almond C-repeat-binding factors involved in cold response. - Tree Physiol. 32: 1113-1128, 2012. Go to original source...
  5. Böhlenius, H., Huang, T., Charbonnel-Campaa, L., Brunner, A.M., Jansson, S., Strauss, S.H., Nilsson, O.: CO/FT regulatory module controls timing of flowering and seasonal growth cessation in trees. - Science 312: 1040-1043, 2006. Go to original source...
  6. Cao, S., Ye, M., Jiang, S.: Involvement of GIGANTEA gene in the regulation of the cold stress response in Arabidopsis. - Plant Cell Rep. 24: 683-690, 2005. Go to original source...
  7. Chen, J., Tsuda, Y., Stocks, M., Källman, T., Xu, N., Kärkkäinen, K., Huotari, T., Semerikov, V.L., Vendramin, G.G., Lascoux, M.: Clinal variation at phenology-related genes in spruce: parallel evolution in FTL2 and Gigantea? - Genetics 197: 1025-1038, 2014. Go to original source...
  8. Chen, Y., Jiang, P., Thammannagowda, S., Liang, H., Wilde, H.D: Characterization of peach TFL1 and comparison with FT/TFL1 gene families of the Rosaceae. - J. amer. Soc. hort. Sci. 138: 12-17, 2013. Go to original source...
  9. Egea, J., Ortega, E., Martínez-Gómez, P., Dicenta, F.: Chilling and heat requirements of almond cultivars for flowering. - Environ. exp. Bot. 50: 79-85. 2003. Go to original source...
  10. Felipe, A.J.: [Almond. Phenological Stages.] - Inf. Técn. Econ. Agrar. 27: 8-9, 1977. [In Span.]
  11. Fowler, S., Lee, K., Onouchi, H., Samach, A., Richardson, K., Morris, B., Coupland, G., Putterill, J.: GIGANTEA: a circadian clock-controlled gene that regulates photoperiodic flowering in Arabidopsis and encodes a protein with several possible membrane-spanning domains. - EMBO J. 18: 4679-4688, 1999. Go to original source...
  12. Frohman, M.A., Dush, M.K., Martin, G.R.: Rapid production of full-length cDNAs from rare transcripts: Amplification using a single gene-specific oligonucleotide primer. - Proc. nat. Acad. Sci. USA 85: 8998-9002, 1988. Go to original source...
  13. Griffiths, S., Dunford, R.P., Coupland, G., Laurie, D.A.: The evolution of CONSTANS-like gene families in barley, rice, and Arabidopsis. - Plant Physiol. 131: 1855-1867, 2003. Go to original source...
  14. Hayama, R., Izawa, T., Shimamoto, K.: Isolation of rice genes possibly involved in the photoperiodic control of flowering by a fluorescent differential display method. - Plant Cell Physiol. 43: 494-504, 2002. Go to original source...
  15. Holefors, A., Opseth, L., Rosnes, A.K.R., Ripel, L., Snipen, L., Fossdal, C.G., Olsen, J.E.: Identification of PaCOL1 and PaCOL2, two CONSTANS-like genes showing decreased transcript levels preceding short day induced growth cessation in Norway spruce. - Plant Physiol. Biochem. 47: 105-115, 2009. Go to original source...
  16. Hong, S.-Y., Lee, S., Seo, P.J., Yang, M.S., Park, C.M.: Identification and molecular characterization of a Brachypodium distachyon GIGANTEA gene: functional conservation in monocot and dicot plants. - Plant mol. Biol. 72: 485-497, 2010. Go to original source...
  17. Horvath, D.: Common mechanisms regulate flowering and dormancy. - Plant Sci. 177: 523-531, 2009. Go to original source...
  18. Hsu, C.-Y., Adams, J.P., No, K., Liang, H., Meilan, R., Pechanova, O., Barakat, A., Carlson, J.E., Page, G.P., Yuceer, C.: Overexpression of Constans homologs CO1 and CO2 fails to alter normal reproductive onset and fall bud set in woody perennial poplar. - PLoS ONE 7: e45448, 2012. Go to original source...
  19. Hsu, C.-Y., Liu, Y., Luthe, D.S., Yuceer, C.: Poplar FT2 shortens the juvenile phase and promotes seasonal flowering. - Plant Cell 18: 1846-1861, 2006. Go to original source...
  20. Huq, E., Tepperman, J.M., Quail, P.H.: GIGANTEA is a nuclear protein involved in phytochrome signaling in Arabidopsis. - Proc. nat. Acad. Sci. USA 97: 9789-9794, 2000. Go to original source...
  21. Ibáñez, C.C., Kozarewa, I.I., Johansson, M., Ogren, E., Rohde, A., Eriksson, M.E.: Circadian clock components regulate entry and affect exit of seasonal dormancy as well as winter hardiness in Populus trees. - Plant Physiol. 153: 1823-1833, 2010. Go to original source...
  22. Imaizumi, T., Tran, H.G., Swartz, T.E., Briggs, W.R., Kay, S.A.: FKF1 is essential for photoperiodic-specific light signalling in Arabidopsis. - Nature 426: 302-306, 2003. Go to original source...
  23. Jung, J.-H., Seo, P.J., Park, C.-M.: The E3 ubiquitin ligase HOS1 regulates Arabidopsis flowering by mediating CONSTANS degradation under cold stress. - J. biol. Chem. 287: 43277-43287, 2012. Go to original source...
  24. Kim, W.-Y., Fujiwara, S., Suh, S.-S., Kim, J., Kim, Y., Han, L., David, K., Putterill, J., Nam, H.G., Somers, D.E.: ZEITLUPE is a circadian photoreceptor stabilized by GIGANTEA in blue light. - Nature 449: 356-360, 2007. Go to original source...
  25. Kobayashi, Y., Kaya, H., Goto, K., Iwabuchi, M., Araki, T.: A pair of related genes with antagonistic roles in mediating flowering signals. - Science 286: 1960-1962, 1999. Go to original source...
  26. Kumar, S., Stecher, G., Tamura, K.: MEGA7: Molecular evolutionary genetics analysis. Version 7.0 for bigger datasets. - Mol. Biol. Evol. 33: 1870-1874, 2016. Go to original source...
  27. Lamp, B.M., Connell, J.H., Duncan, R.A., Viveros, M., Polito, V.S.: Almond flower development: floral initiation and organogenesis. - J. amer. Soc. hort. Sci. 126: 689-696, 2001. Go to original source...
  28. Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H., Valentin, F., Wallace, I.M., Wilm, A., Lopez, R., Thompson, J.D., Gibson, T.J., Higgins, D.G.: Clustal W and Clustal X version 2.0. - Bioinformatics 23: 2947-2948, 2007. Go to original source...
  29. Lazaro, A., Valverde, F., Piñeiro, M., Jarillo, J.A.: The Arabidopsis E3 ubiquitin ligase HOS1 negatively regulates CONSTANS abundance in the photoperiodic control of flowering. - Plant Cell 24: 982-999, 2012. Go to original source...
  30. Li, C., Gu, M., Shi, N., Zhang, H., Yang, X., Osman, T., Liu, Y., Wang, H., Vatish, M., Jackson, S., Hong, Y.: Mobile FT mRNA contributes to the systemic florigen signalling in floral induction. - Sci. Rep. 1: 73-73. 2011. Go to original source...
  31. Lifschitz, E., Eshed, Y.: Universal florigenic signals triggered by FT homologues regulate growth and flowering cycles in perennial day-neutral tomato. - J. exp. Bot. 57: 3405-3414, 2006. Go to original source...
  32. Lin, M.-K., Belanger, H., Lee, Y.-J., Varkonyi-Gasic, E., Taoka, K., Miura, E., Xoconostle-Cázares, B., Gendler, K., Jorgensen, R.A., Phinney, B., Lough, T.J., Lucas, W.J.: FLOWERING LOCUS T protein may act as the longdistance florigenic signal in the cucurbits. - Plant Cell 19: 1488-1506, 2007. Go to original source...
  33. Martins, M., Tenreiro, R., Oliveira, M.M.: Genetic relatedness of Portuguese almond cultivars assessed by RAPD and ISSR markers. - Plant Cell Rep. 22: 71-78, 2003. Go to original source...
  34. Miguel, C.M., Druart, P., Oliveira, M.M.: Shoot regeneration from adventitious buds induced on juvenile and adult almond (Prunus dulcis Mill) explants. - In Vitro cell. dev. Biol. Plant 32: 148-153, 1996. Go to original source...
  35. Mizoguchi, T., Wright, L., Fujiwara, S., Cremer, F., Lee, K., Onouchi, H., Mouradov, A., Fowler, S., Kamada, H., Putterill, J., Coupland, G.: Distinct roles of GIGANTEA in promoting flowering and regulating circadian rhythms in Arabidopsis. - Plant Cell 17: 2255-2270, 2005. Go to original source...
  36. Oliveira, M.M., Miguel, C.M., Costa, M: Almond. - In Kole, C., Hall, T.C. (ed.): Transgenic Temperate Fruits and Nuts. Vol. 4. Pp. 259-283. Wiley-Blackwell, Oxford 2008. Go to original source...
  37. Park, D.H., Somers, D.E., Kim, Y.S., Choy, Y.H., Lim, H.K., Soh, M.S., Kim, H.J., Kay, S.A., Nam, H.G.: Control of circadian rhythms and photoperiodic flowering by the Arabidopsis GIGANTEA gene. - Science 285: 1579-1582, 1999. Go to original source...
  38. Ramos, A., Pérez-Solís, E., Ibáñez, C., Casado, R., Collada, C., Gómez, L., Aragoncillo, C., Allona I.: Winter disruption of the circadian clock in chestnut. - Proc. nat. Acad. Sci. USA 102: 7037-7042, 2005. Go to original source...
  39. Reinoso, H., Luna, V., Pharis, R.P., Bottini, R.: Dormancy in peach (Prunus persica) flower buds. V. Anatomy of bud development in relation to phenological stage. - Can. J. Bot. 80: 656-663, 2002. Go to original source...
  40. Rinne, P.L.H., Welling, A., Vahala, J., Ripel, L., Ruonala, R., Kangasjärvi, J., van der Schoot, C.: Chilling of dormant buds hyperinduces FLOWERING LOCUS T and recruits GA-inducible 1,3-beta-glucanases to reopen signal conduits and release dormancy in Populus. - Plant Cell 23:130-146, 2011. Go to original source...
  41. Rose, T.M., Henikoff, J.G., Henikoff, S.: CODEHOP (COnsensus-DEgenerate Hybrid Oligonucleotide Primer) PCR primer design. - Nucl. Acid Res. 31: 3763-3766, 2003 Go to original source...
  42. Ruonala, R., Rinne, P.L.H., Kangasjärvi, J., Van der Schoot, C.: CENL1 expression in the rib meristem affects stem elongation and the transition to dormancy in Populus. - Plant Cell 20: 59-74, 2008. Go to original source...
  43. Samach, A., Onouchi, H., Gold, S.E., et al.: Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. - Science 288: 1613-1616, 2000. Go to original source...
  44. Sánchez-Pérez, R., Dicenta, F., Martínez-Gómez, P.: Inheritance of chilling and heat requirements for flowering in almond and QTL analysis. - Tree Genet. Genomes 8: 379-389, 2011. Go to original source...
  45. Sambrook, J., Fritsch, E.F., Maniatis, T., Nolan C. (ed.): Molecular cloning: a laboratory manual. - Cold Spring Harbor Press, New York 1986.
  46. Sawa, M., Kay, S.A.: GIGANTEA directly activates Flowering Locus T in Arabidopsis thaliana. - Proc. nat. Acad. Sci. USA 108: 11698-11703, 2011. Go to original source...
  47. Sawa, M., Nusinow, D.A., Kay, S.A., Imaizumi, T.: FKF1 and GIGANTEA complex formation is required for day-length measurement in Arabidopsis. - Science 318: 261-265, 2007. Go to original source...
  48. Suárez-López, P., Wheatley, K., Robson, F. et al.: CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis. - Nature 410: 1116-1120, 2001. Go to original source...
  49. Tamaki, S., Matsuo, S., Wong H.L., Yokoi, S., Shimamoto, K.: Hd3a protein is a mobile flowering signal in rice. - Science 316: 1033-1036, 2007. Go to original source...
  50. Taylor, A., Massiah, A.J., Thomas, B.: Conservation of Arabidopsis thaliana photoperiodic flowering time genes in onion (Allium cepa L.). - Plant Cell Physiol. 51: 1638-1647, 2010. Go to original source...
  51. Turck, F., Fornara, F., Coupland, G.: Regulation and identity of florigen: FLOWERING LOCUS T moves center stage. - Annu. Rev. Plant Biol. 59: 573-594, 2008. Go to original source...
  52. Valverde, F., Mouradov, A., Soppe, W., Ravenscroft, D., Samach, A., Coupland, G.: Photoreceptor regulation of CONSTANS protein in photoperiodic flowering. - Science 303: 1003-1006, 2004. Go to original source...
  53. Van der Schoot, C., Rinne, P.L.H.: Dormancy cycling at the shoot apical meristem: transitioning between selforganization and self-arrest. - Plant Sci. 180: 120-131, 2011. Go to original source...