Seedling emergence in monocots depends mainly on mesocotyl elongation, requiring the coordination between developmental signals and environmental stimuli. Strigolactones (SLs) and karrikins are butenolide compounds that regulate various developmental processes; both are able to negatively regulate rice (Oryza sativa) mesocotyl elongation in the dark. Here, we report that a karrikin signaling complex, DWARF 14-LIKE (D14L)-DWARF 3 (D3)-Oryza sativa SUPPRESSOR OF MAX2 1 (OsSMAX1), regulates rice mesocotyl elongation in the dark. We demonstrate that D14L recognizes the karrikin signal and recruits the SCFD3 ubiquitin ligase for the ubiquitination and degradation of OsSMAX1, mirroring the SL-induced and D14- and D3-dependent ubiquitination and degradation of D53. Overexpression of OsSMAX1 promoted mesocotyl elongation in the dark, whereas knockout of OsSMAX1 suppressed the elongated-mesocotyl phenotypes of d14l and d3 but had little effect on their shoot branching phenotype. OsSMAX1 localizes in nucleus and interacts with TOPLESS-RELATED PROTEINs (TPRs), regulating downstream gene expression. Moreover, we showed that the GR24 enantiomers GR245DS and GR24ent-5DS specifically inhibit mesocotyl elongation and regulate downstream gene expression in a D14- and D14L-dependent manner, respectively. Our work revealed that karrikin and SL signaling play parallel and additive roles in modulating downstream genes expression and negatively regulating mesocotyl elongation in the dark.