A module involving SEED SHATTERING 1 facilitates seed shattering by suppressing lignin biosynthesis in rice

Abstract

Reduced seed shattering is a key goal in crop domestication and improvement. Seed shattering 1 (Sh1) was parallel selected during the domestication of the Poaceae family. Investigating the regulatory network of OsSh1 in controlling seed shattering in rice (Oryza sativa L.) offers biological insights and potential for agricultural applications. Here, we identified a transcription factor of CONSTANS, CONSTANS-LIKE, and TOC1(CCT) family, OsCCT22, that physically interacts with OsSh1 in rice. oscct22 mutants exhibited a phenotype similar to ossh1 mutants, characterized by incomplete development of abscission layers and reduced seed shattering ability. Transcriptomic analysis revealed that OsSh1 and OsCCT22 jointly regulate the expression of genes involved in lignin biosynthesis. Notably, transcription of the cinnamyl alcohol dehydrogenase (CAD) gene OsCAD2, caffeic acid O-methyltransferase (OsCOMT), and O-methyltransferase 16 (ROMT-16) was directly inhibited by OsSh1 binding to their key binding motif. This repression was enhanced by the interaction between OsCCT22 and OsSh1. Additionally, our study suggests that OsSh1 regulates the transcription of OsCAD2 by modulating histone methylation modifications near the first intron. Loss-of-function mutations in OsCAD2 led to the formation of more extensive abscission layers and a significant reduction in lignin deposition, resulting in natural seed shattering. Our findings reveal that the OsCCT22-OsSh1-OsCAD2 module affects the lignin deposition of the abscission zone and seed shattering in rice and provide a target for the genetic improvement of seed shattering in crop breeding.