Cryptochromes and the Circadian Clock: The Story of a Very Complex Relationship in a Spinning World

Abstract

Cryptochromes are flavin-containing blue light photoreceptors, present in most kingdoms, including archaea, bacteria, plants, animals and fungi. They are structurally similar to photolyases, a class of flavoproteins involved in light-dependent repair of UV-damaged DNA. Cryptochromes were first discovered in Arabidopsis thaliana in which they control many light-regulated physiological processes like seed germination, de-etiolation, photoperiodic control of the flowering time, cotyledon opening and expansion, anthocyanin accumulation, chloroplast development and root growth. They also regulate the entrainment of plant circadian clock to the phase of light-dark daily cycles. Here, we review the molecular mechanisms by which plant cryptochromes control the synchronisation of the clock with the environmental light. Furthermore, we summarise the circadian clock-mediated changes in cell cycle regulation and chromatin organisation and, finally, we discuss a putative role for plant cryptochromes in the epigenetic regulation of genes.

Keywords: Arabidopsis; cell cycle; chromatin; circadian clock; cryptochromes; epigenetic; gene expression regulation; light.

Figure 1

Schematic representation of the Arabidopsis circadian clock, depicting the three principal components of the circadian machinery: The INPUT system—cryptochromes (CRYs) and phytochromes (PHYs)—that receives light stimuli and entrains the clock; the CLOCK CORE that generates 24-h self-sustained oscillations, also in absence of environmental stimuli; the OUTPUT system that adapts the developmental and physiological responses of the plant to the circadian fluctuations. Images from: https://commons.wikimedia.org/wiki/File:Arabidopsis_thaliana_sl10.jpg; https://commons.wikimedia.org/wiki/File:Metabolic_pathway-_pyridoxal_5%27-phosphate_biosynthesis_I_v_2.0.svg; https://commons.wikimedia.org/wiki/File:Arabidopsis_thaliana_JdP_2013-04-28.jpg; https://commons.wikimedia.org/wiki/File:Plants_that_change_color_and_mark_buried_explosives.jpg (accessed on 18 March 2021).

Figure 2

Epigenetic regulation of clock components and their role during cell cycle. (Left) Histone modifications modulate the rhythmic expression of clock genes: at dusk TIMING OF CAB EXPRESSION 1 (TOC1) expression increases due to hyperacetylation. Once TOC1 reaches its peak, the downregulation is accompanied by the action of the histone deacetylase HDA9 which facilitates CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) mediated repression at the end of the day. (Right) At the transition between Gap 1 (G1) and duplication of DNA (S) phase, TOC1 regulates the progression of the cell cycle by repressing the expression of CELL DIVISION CONTROL 6 (CDC6) responsible for DNA replication.