Core circadian clock and light signaling genes brought into genetic linkage across the green lineage

Abstract

AbstractThe circadian clock ensures that biological processes are phased to the correct time of day. In plants the circadian clock is conserved at both the level of transcriptional networks as well as core genes. In the model plant Arabidopsis thaliana, the core circadian singleMYB (sMYB) genes CCA1 and RVE4 are in genetic linkage with the PSEUDO-RESPONSE REGULATOR (PRR) genes PRR9 and PRR7 respectively. Leveraging chromosome-resolved plant genomes and syntenic ortholog analysis it was possible to trace this genetic linkage back to the basal angiosperm Amborella and identify an additional evolutionarily conserved genetic linkage between PIF3 and PHYA. The LHY/CCA1-PRR5/9, RVE4/8-PRR3/7 and PIF3-PHYA genetic linkages emerged in the bryophyte lineage and progressively moved within several genes of each other across an array of higher plant families representing distinct whole genome duplication and fractionation events. Soybean maintains all but two genetic linkages, and expression analysis revealed the PIF3-PHYA linkage overlapping with the E4 maturity group locus was the only pair to robustly cycle with an evening phase in contrast to the sMYB-PRR morning and midday phase. While most monocots maintain the genetic linkages, they have been lost in the economically important grasses (Poaceae) such as maize where the genes have been fractionated to separate chromosomes and presence/absence variation results in the segregation of PRR7 paralogs across heterotic groups. The evolutionary conservation of the genetic linkage as well as its loss in the grasses provides new insight in the plant circadian clock, which has been a critical target of breeding and domestication.Summary SentenceThe genetic linkage of the core circadian clock components has evolutionary origins in bryophytes and sheds light on the current functioning and selection on the circadian clock in crops.