Resources
The Arabidopsis thaliana clock consists of a central loop and two peripheral (morning and evening) loops. The central loop includes transcription factors CIRCADIAN CLOCK ASSOCIATED 1 (CCA1), LATE ELONGATED HYPOCOTYL (LHY), CCA1 HIKING EXPEDITION (CHE), and TIMING OF CAB EXPRESSION 1 (TOC1). TOC1 positively regulates expression of CCA1 and LHY that have redundant but non-overlapping functions, while CCA1 and LHY bind to the promoter of TOC1 and inhibit its expression. CHE interacts with TOC1 and binds to CCA1 promoter and promotes its expression, whereas CCA1 and LHY repress CHE expression.
Our study underscores the complex interplay between circadian rhythms and chromatin modifications, revealing how histone marks and protein interactions regulate rhythmic gene expression in plants. In Arabidopsis hybrids or allopolyploids, expression changes of circadian clock genes are associated with chromatin modifications and DNA methylation. We found CHH methylation is associated with altered expression of CCA1 in Arabidopsis hybrids.
Further studies show that the circadian oscillators CCA1 and LHY regulate the expression of chromatin modifiers like JMJ14 and SDG2. CCA1 and LHY directly regulate JMJ14 (an H3K4me3 eraser) and indirectly affect SDG2 (an H3K4me3 writer), leading to rhythmic changes in H3K4me3 levels at target genes. In the sdg2 mutant, circadian oscillator gene expression decreases, while it increases in the jmj14 mutant. The results indicate a reciprocal and/or feedback relationship between circadian clock genes and chromatin modification regulators. At the genome-wide level, Diurnal rhythms of H3K4me3 and H3K9ac marks are associated with the expression of 20-30% of expressed genes. However, only 13% of morning-phased and 22% of evening-phased genes show peaks in both H3K4me3 and H3K9ac, suggesting these marks have specific roles in circadian regulation. In allotetraploids, heterologous protein interactions between CHE and AtHD1 in trans with a preference of binding to the cis-acting elements of AtCCA1 to reduce AtCCA1 expression. This highlights how heterologous protein interactions can modulate circadian clock components in hybrid and polyploid plants.
Moreover, sugars exhibit feedback regulation of CCA1 expression through strigolactone signaling pathway to modulate tiller and panicle development in rice. Collaborative work led by Dr. Ed Marcotte has developed a pan-plant interactome map, detailing chromatin complex interactions across different plant species, indicating a complex establishment mechanism between circadian regulators and multiple chromatin factors, which remains to be tested in the future.
Five Selected Publications
- Ng, D. W-K., Miller, M., Yu, H. H., Huang, T-Y., Kim, E-D., Lu, J., Xie, Q., McClung, C. R., and Chen, Z. J. (2014) A role for CHH methylation in the parent-of-origin effect on altered circadian rhythms and biomass heterosis in plant hybrids. Plant Cell 26:2430-2440.
- Song, Q., Huang, T. Y., Chen, H. H., Mass, P., Ha, M., Chen, Z. J. (2019) Diurnal regulation of SDG2 and JMJ14 by circadian clock oscillators orchestrates histone modification rhythms in Arabidopsis. Genome Biology 20:170.
- Chen, Z. J., Mas, P. (2019) Interactive roles of chromatin regulation and circadian clock function in plants. Genome Biology 20:62.
- McWhite, C. D., Papoulas, O., Drew, K., Cox, R. M., June, V., Dong, O. X., Kwon, T., Wan, C, Salmi, M. L., Roux, S. J., Browning, K. S., Chen, Z. J., Ronald, P. C., Marcotte, E. M. (2019) A pan-plant protein complex map reveals deep conservation and novel assemblies. Cell 181:460-474.e14.
- Wang, F., Han, T., Song, Q., Ye, W., Song, X., Chu, J., Li., J., Chen, Z. J. (2020) The rice circadian clock regulates tiller growth and panicle development through strigolactone signaling and sugar sensing. Plant Cell 32:3124-3138.
