Genes & Genomics

, Volume 40, Issue 10, pp 1063–1068 | Cite as

Dependence and independence of the root clock on the shoot clock in Arabidopsis

  • Hong Gil Lee
  • Pil Joon Seo
Research Article


Temporal and spatial compartmentalization of biological processes is facilitated by tissue-specific uncoupled circadian clocks in plants. However, interactions among tissue-specific circadian clocks have not been well established. The primary objective of this study was to describe both organ-specific circadian behaviors and centralized actions of the root clock. We analyzed transcript accumulation of circadianly-oscillating genes in roots and shoots. Expression of many clock components was different in roots and shoots. In particular, evening-expressed clock components were highly expressed in roots and likely play important roles in oscillation of the root clock. Consistent with this, the root and shoot clocks responded differentially to circadian gene mutations. The root clock was even dampened in gi-2 mutant. Circadian clocks basically oscillate in an organ-specific manner in plants, but the root clock also requires shoot-derived signals for organism-level coordination of circadian activity.


Arabidopsis Circadian clock GIGANTEA Organ specificity Root clock 











Neutral-day conditions




Zeitgeber time



This work was supported by the Basic Science Research (NRF-2016R1D1A1B03931139) and Basic Research Laboratory (NRF-2017R1A4A1015620) programs provided by the National Research Foundation of Korea and by the Cooperative Research Program for Agriculture Science and Technology Development (PJ01261303) provided by the Rural Development Administration.

Compliance with ethical standards

Conflict of interest

We have no conflict of interest to declare.


  1. Alabadí D, Oyama T, Yanovsky MJ, Harmon FG, Más P, Kay SA (2001) Reciprocal regulation between TOC1 and LHY/CCA1 within the Arabidopsis circadian clock. Science 293:880–883CrossRefPubMedGoogle Scholar
  2. Bordage S, Sullivan S, Laird J, Millar AJ, Nimmo HG (2016) Organ specificity in the plant circadian system is explained by different light inputs to the shoot and root clocks. New Phytol 212:136–149CrossRefPubMedPubMedCentralGoogle Scholar
  3. Cao S, Song Y, Su L (2007) Freezing sensitivity in the gigantea mutant of Arabidopsis is associated with sugar deficiency. Biol Plant 51:359–362CrossRefGoogle Scholar
  4. David KM, Armbruster U, Tama N, Putterill J (2006) Arabidopsis GIGANTEA protein is post-transcriptionally regulated by light and dark. FEBS Lett 580:11931–11197CrossRefGoogle Scholar
  5. Ding Z, Doyle MR, Amasino RM, Davis SJ (2007) A complex genetic interaction between Arabidopsis thaliana TOC1 and CCA1/LHY in driving the circadian clock and in output regulation. Genetics 176:1501–1510CrossRefPubMedPubMedCentralGoogle Scholar
  6. Dodd AN, Salathia N, Hall A, Kévei E, Tóth R, Nagy F, Hibberd JM, Millar AJ, Webb AA (2005) Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science 309:630–633CrossRefPubMedGoogle Scholar
  7. Dubrovsky JG, Gambetta GA, Hernández-Barrera A, Shishkova S, González I (2006) Lateral root initiation in Arabidopsis: developmental window, spatial patterning, density and predictability. Ann Bot 97:903–915CrossRefPubMedPubMedCentralGoogle Scholar
  8. Eimert K, Wang SM, Lue WI, Chen J (1995) Monogenic recessive mutations causing both late floral initiation and excess starch accumulation in Arabidopsis. Plant Cell 7:1703–1712CrossRefPubMedPubMedCentralGoogle Scholar
  9. Endo M, Shimizu H, Nohales MA, Araki T, Kay SA (2014) Tissue-specific clocks in Arabidopsis show asymmetric coupling. Nature 515:419–422CrossRefPubMedPubMedCentralGoogle Scholar
  10. Fowler S, Lee K, Onouchi H, Samach A, Richardson K, Morris B, Coupland G, Putterill J (1999) GIGANTEA: a circadian clock-controlled gene that regulates photoperiodic flowering in Arabidopsis and encodes a protein with several possible membrane-spanning domains. EMBO J 18:4679–4688CrossRefPubMedPubMedCentralGoogle Scholar
  11. Green RM, Tobin EM (2002) The role of CCA1 and LHY in the plant circadian clock. Dev Cell 2:516–518CrossRefPubMedGoogle Scholar
  12. Green RM, Tingay S, Wang ZY, Tobin EM (2002) Circadian rhythms confer a higher level of fitness to Arabidopsis plants. Plant Physiol 129:576–584CrossRefPubMedPubMedCentralGoogle Scholar
  13. Iijima M, Matsushita N (2011) A circadian and an ultradian rhythm are both evident in root growth of rice. J Plant Physiol 168:2072–2080CrossRefPubMedGoogle Scholar
  14. James AB, Monreal JA, Nimmo GA, Kelly CL, Herzyk P, Jenkins GI, Nimmo HG (2008) The circadian clock in Arabidopsis roots is a simplified slave version of the clock in shoots. Science 322:1832–1835CrossRefPubMedGoogle Scholar
  15. Korenčič A, Košir R, Bordyugov G, Lehmann R, Rozman D, Herzel H (2014) Timing of circadian genes in mammalian tissues. Sci Rep 4:5782CrossRefPubMedPubMedCentralGoogle Scholar
  16. Lee HG, Mas P, Seo PJ (2016) MYB96 shapes the circadian gating of ABA signaling in Arabidopsis. Sci Rep 6:17754CrossRefPubMedPubMedCentralGoogle Scholar
  17. Malamy JE, Benfey PN (1997) Organization and cell differentiation in lateral roots of Arabidopsis thaliana. Development 124:33–44PubMedGoogle Scholar
  18. Michal TP, Salomé PA, Hannah JY, Spencer TR, Sharp EL, McPeek MA, Alonso JM, Ecker JR, McClung CR (2003) Enhanced fitness conferred by naturally occurring variation in the circadian clock. Science 302:1049–1053CrossRefGoogle Scholar
  19. Nakamichi N (2011) Molecular mechanisms underlying the Arabidopsis circadian clock. Plant Cell Physiol 52:1709–1718CrossRefPubMedPubMedCentralGoogle Scholar
  20. 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 22:594–605CrossRefPubMedPubMedCentralGoogle Scholar
  21. Nohales MA, Kay SA (2016) Molecular mechanisms at the core of the plant circadian oscillator. Nat Struct Mol Biol 23:1061–1069CrossRefPubMedGoogle Scholar
  22. Nusinow DA, Helfer A, Hamilton EE, King JJ, Imaizumi T, Schultz TF, Farré EM, Kay SA (2011) The ELF4-ELF3-LUX complex links the circadian clock to diurnal control of hypocotyl growth. Nature 475:398–402CrossRefPubMedPubMedCentralGoogle Scholar
  23. Rawat R, Schwartz J, Jones MA, Sairanen I, Cheng Y, Andersson CR, Zhao Y, Ljung K, Harmer SL 2009. REVEILLE1, a Myb-like transcription factor, integrates the circadian clock and auxin pathways. Proc Natl Acad Sci USA 106:16883–16888CrossRefGoogle Scholar
  24. Seo PJ, Mas P (2014) Multiple layers of posttranslational regulation refine circadian clock activity in Arabidopsis. Plant Cell 26:79–87CrossRefPubMedPubMedCentralGoogle Scholar
  25. Shimizu H, Katayama K, Koto T, Torii K, Araki T, Endo M (2015) Decentralized circadian clocks process thermal and photoperiodic cues in specific tissues. Nat Plants 1:15163CrossRefPubMedGoogle Scholar
  26. Takahashi N, Hirata Y, Aihara K, Mas P (2015) A hierarchical multi-oscillator network orchestrates the Arabidopsis circadian system. Cell 163:148–159CrossRefPubMedGoogle Scholar
  27. Thain SC, Murtas G, Lynn JR, McGrath RB, Millar AJ (2002) The circadian clock that controls gene expression in Arabidopsis is tissue specific. Plant Physiol 130:102–110CrossRefPubMedPubMedCentralGoogle Scholar
  28. Voß U, Wilson MH, Kenobi K, Gould PD, Robertson FC, Peer WA, Lucas M, Swarup K, Casimiro I, Holman TJ, Wells DM, Péret B, Goh T, Fukaki H, Hodgman TC, Laplaze L, Halliday KJ, Ljung K, Murphy AS, Hall AJ, Webb AA, Bennett MJ (2015) The circadian clock rephases during lateral root organ initiation in Arabidopsis thaliana. Nat Commun 6:7641CrossRefPubMedPubMedCentralGoogle Scholar
  29. Yazdanbakhsh N, Sulpice R, Graf A, Stitt M, Fisahn J (2011) Circadian control of root elongation and C partitioning in Arabidopsis thaliana. Plant Cell Environ 34:877–894CrossRefPubMedGoogle Scholar

Copyright information

© The Genetics Society of Korea and Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.Department of Biological SciencesSungkyunkwan UniversitySuwonRepublic of Korea

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