SiPRR37 exerts dual functions in the regulation of photoperiodic flowering and contributes to the ecological adaption of foxtail millet

Foxtail millet ( Setaria italica ) is an important crop and an emerging model plant. Photoperiodic flowering is a key determinant of its production and geographic expansion. In this study, we found that SiPRR37 is responsible for the major quantitative trait locus (QTL) Heading date 2 ( Hd2 ) identified in 680 foxtail millets using a genome-wide association study. Overexpression of SiPRR37 in foxtail millet significantly delayed the heading date under both natural long-day and short-day conditions. CRISPR/Cas9-induced Siprr37 mutants exhibited earlier flowering in long-day conditions but later flowering in short-day conditions. The critical day length (CDL) for the reversal of Siprr37 ’s function was around 14.3 h. Haplotype analysis revealed that accessions with the Tc1-Mariner transposon insertion in SiPRR37 (Hap 1) flowered significantly earlier at higher latitudes, and later at lower latitudes, indicating that natural variants of SiPRR37 exert dual functions in flowering regulation according to geographic latitude. The gradual, successive decrease in the frequency of Hap 2 from low to high latitudes, with the concurrent increase of Hap 1, demonstrates that these haplotypes have undergone artificial selection. Further F ST analysis demonstrated that SiPRR37 has contributed to the ecological adaption of foxtail millet. Additionally, we reveal that OsPRR37 promotes flowering in rice, while GmPRR37 may only inhibit flowering in soybean. Further diurnal expression and transgenic analyses suggest that the dual function of SiPRR37 might depend on SiHd1 . Our study uncovered the distinct functional reversal of SiPRR37 and functional diversification of PRR37 homologs in SD crops. These findings not only enrich knowledge about the regulation of photoperiodic flowering, but also contribute to genetic improvement of crops’ regional adaptability.