Loss of Photosynthetic Rhythm Thermal Plasticity Under Domestication and RepurposingDrivers of Circadian Clock (DOC) Loci for Adaptive Breeding in Barley

Abstract

Circadian clock rhythms are critical to control physiological and development traits, allowing, plants to adapt to changing environments. Here we show that the circadian rhythms of cultivated barley (Hordeum vulgare) have slowed and amplitude increased under domestication by comparing with its wild ancestor (H. spontaneum). Moreover, we show a significant loss of thermal plasticity during barley evolution for the period and more extensively for amplitude. Our genetic analysis indicates that wild allele at epistatic loci, which mutually condition clock variation and its thermal plasticity in interspecific crosses, are absent in a contemporary barley breeding panel. These epistatic interactions include conditioned effects of Drivers of Circadian (DOC) clock loci on chromosome 3 and 5, which mediate amplitude decrease and period lengthening, respectively, under domestication. Notably, two significant loci, DOC3.1 and DOC5.1, which are not associated with clock diversity in cultivated breeding material, do show pleiotropic effects on flowering time and grain yield at multiple experimental sites across the U.S. in a temperature-dependent manner. We suggest that transition from winter growth of wild barley (H. spontaneum) to spring growth of modern cultivars included the loss and repurposing of circadian clock regulators to yield adaptation by mechanisms yet to be clarified. Significance statementCircadian clock rhythms are crucial factors affecting crop adaptation to changing environments. If faced with increased temperature plants could respond with temperature compensation adaptation and maintain clock rhythms, or they can change period and/or amplitude to adapt. We used a combination of approaches: high-throughput clock analysis under optimal and elevated heat conditions, genome-wide association study (GWAS) with cultivated and wild diversity panels to identify changes under domestication and quantitative trait loci (QTL) that control the clock and its responses, and QTL-environment association for testing environmentally-conditioned effects of these QTLongrain yield and flowering timingacross US. Our findings provide insights into changes of circadian rhythms under domestication and genetic tools for plant breeders to develop better-adapted cultivars to changing environments.