Altered circadian rhythms regulate growth vigour in hybrids and allopolyploids

Abstract

Segregating hybrids and stable allopolyploids display morphological vigor1,2,3, and Arabidopsis allotetraploids are larger than the parents Arabidopsis thaliana and A. arenosa1,4. The mechanisms are unknown. Circadian clocks mediate metabolic pathways and increase fitness in animals and plants5,6,7,8. Here we report that epigenetic modifications of the circadian clock genes CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) and LATE ELONGATED HYPOCOTYL (LHY)9,10 and their reciprocal regulators TIMING OF CAB EXPRESSION 1 (TOC1) and GIGANTEA (GI)10,11,12 mediate expression changes in downstream genes and pathways. During the day, epigenetic repression of CCA1 and LHY induced expression of TOC1, GI and downstream genes that contain CCA1 binding site (CBS)13 in chlorophyll and starch metabolic pathways in allotetraploids and F1 hybrids, which produced more chlorophyll and starch than the parents in the same environment. Mutations in cca1 and cca1 lhy and daily repression of cca1 in TOC1:cca1-RNAi transgenic plants increased expression of downstream genes and chlorophyll and starch content, whereas constitutively expressing CCA1 or ectopically expressing TOC1:CCA1 had the opposite effects. 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 vigor and increased biomass.

Cis- and trans-regulatory divergence between progenitor species determines gene-expression novelty in Arabidopsis allopolyploids

“…The genes with cis but not trans effects were underrepresented in G9 that was associated with DNA methylation, which predominantly occurs at heterochromatin and repetitive elements such as transposons. The genome-wide chromatin data are consistent with the experimental data in which protein-coding genes and transposons are epigenetically modified in allopolyploids of Arabidopsis [28][29][30][31] and wheat 32 . These data collectively support a role for chromatin modifications in cis and trans regulation of allelic expression divergence between A. thaliana and A. arenosa.…”

“…arenosa miR163 is more downregulated than A. thaliana miR163 in allotetraploids 33 . For many genes involved in photosynthesis, starch metabolism and circadian pathways, A. thaliana alleles are preferentially upregulated in the allotetraploids, leading to hybrid vigour 29 .…”

A Role for CHH Methylation in the Parent-of-Origin Effect on Altered Circadian Rhythms and Biomass Heterosis inArabidopsisIntraspecific Hybrids

“…This is consistent with the recent finding of the circadian regulation of gene expression and photosynthetic activities in chloroplasts (Noordally et al, 2013). Indeed, altering the expression of circadian regulators increases chlorophyll biosynthesis and sugar and starch metabolism in Arabidopsis hybrids and allopolyploids (Ni et al, 2009). Hybrids can synthesize more starch during the day and degrade more starch at night.…”

“…Thus, this positive correlation of daytime starch accumulation with growth vigor and the negative association of morning residual starch levels with growth are not contradictory (Chen, 2013). The growth vigor in Arabidopsis hybrids and allotetraploids is partly controlled by the epigenetic regulation of central circadian clock oscillator components, including CCA1 (Ni et al, 2009). Notably, the association of increased biomass with CCA1 repression during the day has been independently demonstrated in Arabidopsis intraspecific hybrids (Miller et al, 2012;Shen et al, 2012).…”

Epigenomic plasticity within populations: its evolutionary significance and potential

“…The advantages of changes in gene expression (Ni et al, 2009) and restructuring in hybrids (Pennington et al, 2008) and stable allopolyploid plants, Leitch and Leitch (2008) argue, are responsible for much of their diversity and success. If epigenomic cryptic variation is revealed in response to shock or challenge, it should lead to rapid adaptation and increased population evolvability (sensu Hansen (2006)).…”