GAF-dependent chromatin plasticity determines promoter usage to mediate locust gregarious behavior

Locusts, as devastating pests, can reversibly transform between solitary individuals and gregarious swarms with markedly different behaviors. Epigenetic regulation orchestrated by changes in chromatin openness modulates behavioral plasticity by controlling gene expression. However, the gene regulation mechanisms by which chromatin openness controls behavioral changes remain largely unknown. Here, we explored the regulatory function of chromatin openness in modulating behavioral plasticity, in which the remodeler GAF regulated brain-specific promoter usage in locusts. The increased chromatin openness in gregarious locusts initiated transcription of the brain-specific promoter of henna, a critical gene in dopamine synthesis and gregarious behavior mediation. Furthermore, GAF-dependent chromatin openness responded coordinately to population density changes. Fragment mutagenesis abolished henna promoter activity due to the dysfunction of the GAF-binding site. Mechanistically, the three GAF-binding sites played a synergetic role in remodeling chromatin openness and activating transcription initiation. Our study reveals a novel epigenetic mechanism linking chromatin regulation with behavioral polyphenism in insects during environmental changes.