Altered circadian rhythms regulate growth vigour in hybrids and allopolyploids

Abstract

Polyploidy, or whole-genome duplication, is an evolutionary innovation common in plants. Several major crops, including wheat, cotton and canola, are allopolyploids, containing two or more divergent genomes and some plants exist as intra- and interspecific hybrids. Such plants can display vigorous growth. A study of hybrids of Arabidopsis thaliana and A. arenosa sheds light on the mechanistic basis of this increased vigour. Epigenetic modulation of circadian clock regulators is shown to mediate the expression of genes in photosynthetic and starch metabolic pathways in allopolyploids. As a result, they accumulate more chlorophyll, produce more starch, and grow larger than the parents. Thus the hybrid and allopolyploid plants appear to gain advantages from the control of physiological and metabolic pathways by reversibly adjusting circadian clock regulators to make better use of the daylight hours. Polploidy is a common feature of many plants, and in addition some plants exist as intra- and interspecific hybrinds. Such plants display growth vigour, and genes involved in metabolism and energy, photosynthesis and starch accumulation are upregulated compared to the parents. This study examines the mechanistic basis of increased growth, and reports that epigenetic modifications of circadian clock regulators mediates the expression of genes in photosynthetic and metabolic pathways. Segregating hybrids and stable allopolyploids display morphological vigour1,2,3, and Arabidopsis allotetraploids are larger than the parents Arabidopsis thaliana and Arabidopsis arenosa1,4—the mechanisms for this 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)9,10,11 and their reciprocal regulators TIMING OF CAB EXPRESSION 1 (TOC1) and GIGANTEA (GI)10,12,13 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 elements14 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 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.