EARLY FLOWERING 3 alleles affect the temperature responsiveness of the circadian clock in Chinese cabbage

Abstract

Temperature is an environmental cue that entrains the circadian clock, adapting it to local thermal and photoperiodic conditions that characterize different geographic regions. Circadian clock thermal adaptation in leafy vegetables such as Chinese cabbage (Brassica rapa ssp. pekinensis) is poorly understood but essential to sustain and increase vegetable production under changing climates. We investigated circadian rhythmicity in natural Chinese cabbage accessions grown at 14, 20, and 28 °C. The circadian period was significantly shorter at 20 °C than at either 14 or 28 °C, and the responses to increasing temperature and temperature compensation (Q10) were associated with population structure. Genome-wide association studies mapping identified variation responsible for temperature compensation as measured by Q10 value for temperature increase from 20 to 28 °C. Haplotype analysis indicated that B. rapa EARLY FLOWERING 3 H1 Allele (BrELF3H1) conferred a significantly higher Q10 value at 20 to 28 °C than BrELF3H2. Co-segregation analyses of an F2 population derived from a BrELF3H1 × BrELF3H2 cross revealed that variation among BrELF3 alleles determined variation in the circadian period of Chinese cabbage at 20 °C. However, their differential impact on circadian oscillation was attenuated at 28 °C. Transgenic complementation in Arabidopsis thaliana elf3-8 mutants validated the involvement of BrELF3 in the circadian clock response to thermal cues, with BrELF3H1 conferring a higher Q10 value than BrELF3 H2 at 20 to 28 °C. Thus, BrELF3 is critical to the circadian clock response to ambient temperature in Chinese cabbage. These findings have clear implications for breeding new varieties with enhanced resilience to extreme temperatures.