Natural variations of wheat EARLY FLOWERING 3 highlight their contributions to local adaptation through fine-tuning of heading time.

KEY MESSAGE: We identified a large chromosomal deletion containing TaELF-B3 that confers early flowering in wheat. This allele has been preferred in recent wheat breeding in Japan to adapt to the environment. Heading at the appropriate time in each cultivation region can greatly contribute to stabilizing and maximizing yield. Vrn-1 and Ppd-1 are known as the major genes for vernalization requirement and photoperiod sensitivity in wheat. Genotype combinations of Vrn-1 and Ppd-1 can explain the variation in heading time. However, the genes that can explain the remaining variations in heading time are largely unknown. In this study, we aimed to identify the genes conferring early heading using doubled haploid lines derived from Japanese wheat varieties. Quantitative trait locus (QTL) analysis revealed a significant QTL on the long arm of chromosome 1B in multiple growing seasons. Genome sequencing using Illumina short reads and Pacbio HiFi reads revealed a large deletion of a ~ 500 kb region containing TaELF-B3, an orthologue of Arabidopsis clock gene EARLY FLOWERING 3 (ELF3). Plants with the deleted allele of TaELF-B3 (ΔTaELF-B3 allele) headed earlier only under short-day vernalization conditions. Higher expression levels of clock- and clock-output genes, such as Ppd-1 and TaGI, were observed in plants with the ΔTaELF-B3 allele. These results suggest that the deletion of TaELF-B3 causes early heading. Of the TaELF-3 homoeoalleles conferring early heading, the ΔTaELF-B3 allele showed the greatest effect on the early heading phenotype in Japan. The higher allele frequency of the ΔTaELF-B3 allele in western Japan suggests that the ΔTaELF-B3 allele was preferred during recent breeding to adapt to the environment. TaELF-3 homoeologs will help to expand the cultivated area by fine-tuning the optimal timing of heading in each environment.