Skip to main content
SpringerLink
Log in

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

  • Research Article
  • Published:
Genes & Genomics Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

CCA1:

CIRCADIAN CLOCK-ASSOCIATED 1

ELF:

EARLY FLOWERING

GI:

GIGANTEA

LHY:

LATE ELONGATED HYPOCOTYL

ND:

Neutral-day conditions

TOC1:

TIMING OF CAB EXPRESSION 1

ZT:

Zeitgeber time

References

  • 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 293:880–883

    Article  PubMed  Google Scholar 

  • 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 212:136–149

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cao S, Song Y, Su L (2007) Freezing sensitivity in the gigantea mutant of Arabidopsis is associated with sugar deficiency. Biol Plant 51:359–362

    Article  CAS  Google Scholar 

  • David KM, Armbruster U, Tama N, Putterill J (2006) Arabidopsis GIGANTEA protein is post-transcriptionally regulated by light and dark. FEBS Lett 580:11931–11197

    Article  CAS  Google Scholar 

  • 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 176:1501–1510

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 309:630–633

    Article  CAS  PubMed  Google Scholar 

  • 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 97:903–915

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 7:1703–1712

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Endo M, Shimizu H, Nohales MA, Araki T, Kay SA (2014) Tissue-specific clocks in Arabidopsis show asymmetric coupling. Nature 515:419–422

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 18:4679–4688

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Green RM, Tobin EM (2002) The role of CCA1 and LHY in the plant circadian clock. Dev Cell 2:516–518

    Article  CAS  PubMed  Google Scholar 

  • Green RM, Tingay S, Wang ZY, Tobin EM (2002) Circadian rhythms confer a higher level of fitness to Arabidopsis plants. Plant Physiol 129:576–584

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Iijima M, Matsushita N (2011) A circadian and an ultradian rhythm are both evident in root growth of rice. J Plant Physiol 168:2072–2080

    Article  CAS  PubMed  Google Scholar 

  • 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 322:1832–1835

    Article  CAS  PubMed  Google Scholar 

  • Korenčič A, Košir R, Bordyugov G, Lehmann R, Rozman D, Herzel H (2014) Timing of circadian genes in mammalian tissues. Sci Rep 4:5782

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee HG, Mas P, Seo PJ (2016) MYB96 shapes the circadian gating of ABA signaling in Arabidopsis. Sci Rep 6:17754

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Malamy JE, Benfey PN (1997) Organization and cell differentiation in lateral roots of Arabidopsis thaliana. Development 124:33–44

    CAS  PubMed  Google Scholar 

  • 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 302:1049–1053

    Article  CAS  Google Scholar 

  • Nakamichi N (2011) Molecular mechanisms underlying the Arabidopsis circadian clock. Plant Cell Physiol 52:1709–1718

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nohales MA, Kay SA (2016) Molecular mechanisms at the core of the plant circadian oscillator. Nat Struct Mol Biol 23:1061–1069

    Article  CAS  PubMed  Google Scholar 

  • 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 475:398–402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 106:16883–16888

    Article  Google Scholar 

  • Seo PJ, Mas P (2014) Multiple layers of posttranslational regulation refine circadian clock activity in Arabidopsis. Plant Cell 26:79–87

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 1:15163

    Article  PubMed  Google Scholar 

  • Takahashi N, Hirata Y, Aihara K, Mas P (2015) A hierarchical multi-oscillator network orchestrates the Arabidopsis circadian system. Cell 163:148–159

    Article  CAS  PubMed  Google Scholar 

  • 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 130:102–110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 6:7641

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 34:877–894

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

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.

Author information

Authors and Affiliations

  1. Department of Biological Sciences, Sungkyunkwan University, Suwon, 16419, Republic of Korea

    Hong Gil Lee & Pil Joon Seo

Authors
  1. Hong Gil Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Pil Joon Seo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Pil Joon Seo.

Ethics declarations

Conflict of interest

We have no conflict of interest to declare.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lee, H.G., Seo, P.J. Dependence and independence of the root clock on the shoot clock in Arabidopsis. Genes Genom 40, 1063–1068 (2018). https://doi.org/10.1007/s13258-018-0710-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13258-018-0710-4

Keywords

Search

Navigation