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Altered Circadian Rhythms Regulate Growth Vigour in Hybrids and Allopolyploids

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Altered Circadian Rhythms Regulate Growth Vigour in Hybrids and Allopolyploids

Zhongfu Ni et al. Nature.

Abstract

Segregating hybrids and stable allopolyploids display morphological vigour, and Arabidopsis allotetraploids are larger than the parents Arabidopsis thaliana and Arabidopsis arenosa-the mechanisms for this are unknown. Circadian clocks mediate metabolic pathways and increase fitness in animals and plants. Here we report that epigenetic modifications of the circadian clock genes CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) and LATE ELONGATED HYPOCOTYL (LHY) and their reciprocal regulators TIMING OF CAB EXPRESSION 1 (TOC1) and GIGANTEA (GI) mediate expression changes in downstream genes and pathways. During the day, epigenetic repression of CCA1 and LHY induced the expression of TOC1, GI and downstream genes containing evening elements in chlorophyll and starch metabolic pathways in allotetraploids and F(1) hybrids, which produced more chlorophyll and starch than the parents in the same environment. Mutations in cca1 and cca1 lhy and the daily repression of cca1 by RNA interference (RNAi) in TOC1::cca1(RNAi) transgenic plants increased the expression of downstream genes and increased chlorophyll and starch content, whereas constitutively expressing CCA1 or ectopically expressing TOC1::CCA1 had the opposite effect. The causal effects of CCA1 on output traits suggest that hybrids and allopolyploids gain advantages from the control of circadian-mediated physiological and metabolic pathways, leading to growth vigour and increased biomass.

Figures

Figure 1
Figure 1
Locus-specific and chromatin regulation of circadian clock genes in the allotetraploids. a. qRT-PCR analysis of CCA1 expression (n = 3, ACT2 as a control) in a 24-hour period (light/dark cycles) starting from dawn (ZT0, 6 am) (arrows indicate up- and down-regulation, respectively). b. qRT-PCR analysis of TOC1 expression (n = 3). c. Repression of A. thaliana CCA1 and LHY and upregulation of A. thaliana TOC1 and GI in the allotetraploids. RT-PCR products were digested with AvaII (CCA1), AflIII (LHY), SspI (TOC1), and SpeI (GI). d. ChIP analysis of CCA1, LHY, TOC1, and GI using antibodies against H3K9Ac and H3K4Me2 (n = 2). –Ab: no antibodies.
Figure 2
Figure 2
Increase in chlorophyll content and upregulation of the genes involved in chlorophyll and starch biosynthesis in allotetraploids. a. Locations of CCA1 binding site (CBS) or evening element (EE) in the downstream genes (Supplementary Table 1). Lower-case letter: nucleotide variation. b. Increase of chlorophyll (a, b, and total) content in the allotetraploids (n = 3). c. Starch metabolic pathways (modified from that of26) in the chloroplast (circled) and cytoplasm. d. Upregulation of PORA and PORB in the allotetraploids at ZT6 (n = 2). gDNA: Genomic PCR. e. Upregulation of starch metabolic genes in allotetraploids (n = 2) at ZT6. See Supplementary Table 5 for gene names.
Figure 3
Figure 3
CCA1 function and increased amounts of chlorophyll, starch and sugar in allotetraploids and F1 hybrids. a. Starch staining in A. thaliana (At4), A. arenosa (Aa), and allotetraploid (Allo733) at ZT0, ZT6, and ZT15. b. Increased starch content in allotetraploids at ZT6. c. Increased sugar content in allotetraploids at ZT6. d. Morphological vigor in F1 hybrids between A. thaliana Columbia (Col) and C24. e. Increased chlorophyll (ZT6, left) and starch (ZT15, right) accumulation in F1. f. CCA1 protein levels changed at ZT6 and ZT0. g. Specific CCA1 binding activity to EE of downstream genes (TOC1 and PORB) in vitro. Cp: cold probes; Pb:32P-labeled EE-containing probes (Supplementary Table 6). h. ChIP assays of endogenous TOC1 binding to the TOC1 promoter. The levels were normalized using input DNA (n = 2).
Figure 4
Figure 4
A role of CCA1 in growth vigor in allotetraploids and hybrids. a. Relative expression levels (R.E.L.) of CCA1 (ZT6, left) and reduced chlorophyll (ZT9, middle) and starch (ZT15, right) accumulation in TOC1:CCA1 lines (n = 3) (Supplementary Fig. 4). Col(B): Columbia transformed with basta gene. b. Reduced CCA1 expression (ZT6, left) and increased starch content (ZT15, right) in cca1−11 and cca1−11 lhy-21 mutants, (n = 3). WT: Wassilewskija (Ws) or Col. c. Decreased expression of CCA1 mRNA (right, n = 3) and protein (right, n = 2) (ZT0−18, T2) in TOC1:cca1-RNAi transgenic plants. d. Increased starch content in TOC1:cca1-RNAi lines (ZT15, n = 2). e. A model for growth vigor and increased biomass. Chromatin-mediated changes in internal clock regulators (e.g., AtCCA1) in allotetraploids lead to up- and down-regulation (red and black arrows) and normal oscillation (yellow circle) of gene expression and output traits (photosynthesis, starch and sugar metabolism) at noon (sun) and dusk (moon).

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