Abstract
Plant experience diurnal changes in their environment that can be anticipated and responded to via the circadian clock. Integration of external signals by this clock ensures metabolic homeostasis and ultimately enhances fitness. TIME FOR COFFEE (TIC) is known to be associated to the circadian clock, being required to maintain rhythmic period and amplitude, and to regulate clock-driven physiological responses. The molecular function of TIC has so far only been studied with loss-of-function mutants. The biochemical activity of TIC remains elusive. To learn more about TIC in diverse physiological processes, here we generated TIC overexpressing plants (TICox) and characterized their impact on plant growth, development, and circadianclock activity. TICox plants displayed phenotypic similarity with tic mutants. This included defects in leaf morphology, the developmental transition from the vegetative to reproductive phase, and circadian-clock function. These observations allowed us to hypothesize that TIC is an element of protein complexes that are involved in global biological processes.
Similar content being viewed by others
References
Alabadi D, Oyama T, Yanovsky MJ, Harmon FG, Mas P, Kay SA (2001) Reciprocal regulation between TOC1 and LHY/CCA1 within the Arabidopsis circadian clock. Science 293:880–883
Arana MV, Marin-de la Rosa N, Maloof JN, Blazquez MA, Alabadi D (2011) Circadian oscillation of gibberellin signaling in Arabidopsis. Proc Natl Acad Sci USA 108:9292–9297
Bujdoso N, Davis SJ (2013) Mathematical modeling of an oscillating gene circuit to unravel the circadian clock network of Arabidopsis thaliana. Front Plant Sci 4:3
Castelli F, Contillo R, Miceli F (1996) Non-destructive determination of leaf chlorophyll content in four crop species. Journal of Agronomy and Crop Science-Zeitschrift Fur Acker Und Pflanzenbau 177:275–283
Czechowski T, Stitt M, Altmann T, Udvardi MK, Scheible WR (2005) Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol 139:5–17
Davis AM, Hall A, Millar AJ, Darrah C, Davis SJ (2009) Protocol: Streamlined sub-protocols for floral-dip transformation and selection of transformants in Arabidopsis thaliana. Plant Methods 5:3
Davis SJ (2009) Integrating hormones into the floral-transition pathway of Arabidopsis thaliana. Plant Cell Environ 32:1201–1210
Ding Z, Millar AJ, Davis AM, Davis SJ (2007) TIME FOR COFFEE encodes a nuclear regulator in the Arabidopsis thaliana circadian clock. Plant Cell 19:1522–1536
Dodd AN, Salathia N, Hall A, Kevei E, Toth R, Nagy F, Hibberd JM, Millar AJ, Webb AA (2005) Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science 309:630–633
Domagalska MA, Sarnowska E, Nagy F, Davis SJ (2010) Genetic analyses of interactions among gibberellin, abscisic acid, and brassinosteroids in the control of flowering time in Arabidopsis thaliana. PLoS One 5:e14012
Domagalska MA, Schomburg FM, Amasino RM, Vierstra RD, Nagy F, Davis SJ (2007) Attenuation of brassinosteroid signaling enhances FLC expression and delays flowering. Development 134:2841–2850
Duc C, Cellier F, Lobreaux S, Briat JF, Gaymard F (2009) Regulation of iron homeostasis in Arabidopsis thaliana by the clock regulator time for coffee. J Biol Chem 284:36271–36281
Fukushima A, Kusano M, Nakamichi N, Kobayashi M, Hayashi N, Sakakibara H, Mizuno T, Saito K (2009) Impact of clock-associated Arabidopsis pseudo-response regulators in metabolic coordination. Proc Natl Acad Sci USA 106:7251–7256
Gendron JM, Pruneda-Paz JL, Doherty CJ, Gross AM, Kang SE, Kay SA (2012) Arabidopsis circadian clock protein, TOC1, is a DNA-binding transcription factor. Proc Natl Acad Sci USA 109: 3167–3172
Hall A, Bastow RM, Davis SJ, Hanano S, McWatters HG, Hibberd V, Doyle MR, Sung S, Halliday KJ, Amasino RM, Millar AJ (2003) The TIME FOR COFFEE gene maintains the amplitude and timing of Arabidopsis circadian clocks. Plant Cell 15:2719–2729
Hanano S, Domagalska MA, Nagy F, Davis SJ (2006) Multiple phytohormones influence distinct parameters of the plant circadian clock. Genes Cells 11:1381–1392
Hanano S, Stracke R, Jakoby M, Merkle T, Domagalska MA, Weisshaar B, Davis SJ (2008) A systematic survey in Arabidopsis thaliana of transcription factors that modulate circadian parameters. BMC Genomics 9:182
Helfer A, Nusinow DA, Chow BY, Gehrke AR, Bulyk ML, Kay SA (2011) LUX ARRHYTHMO encodes a nighttime repressor of circadian gene expression in the Arabidopsis core clock. Curr Biol 21:126–133
Herrero E, Kolmos E, Bujdoso N, Yuan Y, Wang M, Berns MC, Uhlworm H, Coupland G, Saini R, Jaskolski M, Webb A, Goncalves J, Davis SJ (2012) EARLY FLOWERING4 recruitment of EARLY FLOWERING3 in the nucleus sustains the Arabidopsis circadian clock. Plant Cell 24:428–443
Huang W, Perez-Garcia P, Pokhilko A, Millar AJ, Antoshechkin I, Riechmann JL, Mas P (2012) Mapping the core of the Arabidopsis circadian clock defines the network structure of the oscillator. Science 336:75–79
Kim WY, Fujiwara S, Suh SS, Kim J, Kim Y, Han L, David K, Putterill J, Nam HG, Somers DE (2007) ZEITLUPE is a circadian photoreceptor stabilized by GIGANTEA in blue light. Nature 449:356–360
Kolmos E, Herrero E, Bujdoso N, Millar AJ, Toth R, Gyula P, Nagy F, Davis SJ (2011) A reduced-function allele reveals that EARLY FLOWERING3 repressive action on the circadian clock is modulated by phytochrome signals in Arabidopsis. Plant Cell 23:3230–3246
Kolmos E, Nowak M, Werner M, Fischer K, Schwarz G, Mathews S, Schoof H, Nagy F, Bujnicki JM, Davis SJ (2009) Integrating ELF4 into the circadian system through combined structural and functional studies. HFSP Journal 3:350–366
Lai AG, Doherty CJ, Mueller-Roeber B, Kay SA, Schippers JH, Dijkwel PP (2012) CIRCADIAN CLOCK-ASSOCIATED 1 regulates ROS homeostasis and oxidative stress responses. Proc Natl Acad Sci USA 109:17129–17134
McClung CR, Davis SJ (2010) Ambient thermometers in plants: from physiological outputs towards mechanisms of thermal sensing. Curr Biol 20:1086–1092
Michael TP, Breton G, Hazen SP, Priest H, Mockler TC, Kay SA, Chory J (2008) A morning-specific phytohormone gene expression program underlying rhythmic plant growth. PLoS Biol 6:e225
Nakamichi N, Kiba T, Henriques R, Mizuno T, Chua NH, Sakakibara H (2010) PSEUDO-RESPONSE REGULATORS 9, 7, and 5 are transcriptional repressors in the Arabidopsis circadian clock. Plant Cell 22:594–605
Nozue K, Covington MF, Duek PD, Lorrain S, Fankhauser C, Harmer SL, Maloof JN (2007) Rhythmic growth explained by coincidence between internal and external cues. Nature 448:358–361
Rawat R, Schwartz J, Jones MA, Sairanen I, Cheng Y, Andersson CR, Zhao Y, Ljung K, Harmer SL (2009) REVEILLE1, a Myblike transcription factor, integrates the circadian clock and auxin pathways. Proc Natl Acad Sci USA 106:16883–16888
Rohila JS, Chen M, Cerny R, Fromm ME (2004) Improved tandem affinity purification tag and methods for isolation of protein heterocomplexes from plants. Plant J 38:172–181
Salome PA, McClung CR (2005) What makes the Arabidopsis clock tick on time? A review on entrainment. Plant Cell and Environment 28:21–38
Sanchez A, Shin J, Davis SJ (2011) Abiotic stress and the plant circadian clock. Plant Signal Behav 6:223–231
Sawa M, Nusinow DA, Kay SA, Imaizumi T (2007) FKF1 and GIGANTEA complex formation is required for day-length measurement in Arabidopsis. Science 318:261–265
Shin J, Heidrich K, Sanchez-Villarreal A, Parker JE, Davis SJ (2012) TIME FOR COFFEE represses accumulation of the MYC2 transcription factor to provide time-of-day regulation of jasmonate signaling in Arabidopsis. Plant Cell 24:2470–2482
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Shin, J., Du, S., Bujdoso, N. et al. Overexpression and loss-of-function at TIME FOR COFFEE results in similar phenotypes in diverse growth and physiological responses. J. Plant Biol. 56, 152–159 (2013). https://doi.org/10.1007/s12374-013-0091-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12374-013-0091-9