Natural diversity in daily rhythms of gene expression contributes to phenotypic variation

Abstract

Daily rhythms of gene expression provide a benefit to most organisms by ensuring that biological processes are activated at the optimal time of day. Although temporal patterns of expression control plant traits of agricultural importance, how natural genetic variation modifies these patterns during the day and how precisely these patterns influence phenotypes is poorly understood. The circadian clock regulates the timing of gene expression, and natural variation in circadian rhythms has been described, but circadian rhythms are measured in artificial continuous conditions that do not reflect the complexity of biologically relevant day/ night cycles. By studying transcriptional rhythms of the eveningexpressed gene GIGANTEA (GI) at high temporal resolution and during day/night cycles, we show that natural variation in the timing of GI expression occurs mostly under long days in 77 Arabidopsis accessions. This variation is explained by natural alleles that alter light sensitivity of GI, specifically in the evening, and that act at least partly independent of circadian rhythms. Natural alleles induce precise changes in the temporal waveform of GI expression, and these changes have detectable effects on PHYTOCHROME INTERACTING FACTOR 4 expression and growth. Our findings provide a paradigm for how natural alleles act within day/night cycles to precisely modify temporal gene expression waveforms and cause phenotypic diversity. Such alleles could confer an advantage by adjusting the activity of temporally regulated processes without severely disrupting the circadian system. diurnal | circadian | rhythms | Arabidopsis | GIGANTEA

New mechanistic links between sugar and hormone signalling networks

“…Consistent with this central role at the crossroads of environment and growth responses, the activity of PIF4 and PIF5 have also recently been linked to darkinduced senescence [63]. Evolution may be using the PIF subnetwork to optimize growth responses in new environments, as a recent study of natural variation in 77 Arabidopsis accessions revealed a clear link between variation in clock-regulated expression of PIF4 and growth rate [64].…”

Correlations between Circadian Rhythms and Growth in Challenging Environments

“…For example, the evening-expressed HvELF3 represses the floral promoters GIBBERELLIN20 OXIDASE2 and FLOWERING LOCUS T (Faure et al, 2012;Boden et al, 2014); thus, plants with long period rhythms and delayed HvELF3 expression may show accelerated flowering. However, under diel conditions, the regulation of photoperiod components can be complex, since rhythms are modified by light signals (de Montaigu et al, 2015).…”

Natural variation in transcriptional rhythms modulates photoperiodic responses

“…To more accurately examine the effects of variation of rhythmic expression on photoperiodic responses, measuring precise temporal gene expression profiles among large populations is required. A recent work circumvented this technical issue by employing quantitative live luciferase bioluminescence imaging assay [7]. …”

“…analyzed allelic variation in detailed transcriptional profiles of the evening clock gene GIGANTEA ( GI ) among 77 Arabidopsis accessions using the GI promoter-fused luciferase reporter under different day-length conditions [7]. The phases of GI peaks within these accessions varied more in long days than in short days.…”