Antagonistic regulation of target genes by the SISTER OF TM3-JOINTLESS2 complex in tomato inflorescence branching

The MADS-box transcription factors SISTER OF TM3 and JOINTLESS 2 affect each other's binding to FRUITFULL1 in an antagonistic regulatory module controlling tomato inflorescence branch number. Inflorescence branch number is a yield-related trait controlled by cell fate determination in meristems. Two MADS-box transcription factors (TFs)-SISTER OF TM3 (STM3) and JOINTLESS 2 (J2)-have opposing regulatory roles in inflorescence branching. However, the mechanisms underlying their regulatory functions in inflorescence determinacy remain unclear. Here, we characterized the functions of these TFs in tomato (Solanum lycopersicum) floral meristem and inflorescence meristem (IM) through chromatin immunoprecipitation and sequencing analysis of their genome-wide occupancy. STM3 and J2 activate or repress the transcription of a set of common putative target genes, respectively, through recognition and binding to CArG box motifs. FRUITFULL1 (FUL1) is a shared putative target of STM3 and J2 and these TFs antagonistically regulate FUL1 in inflorescence branching. Moreover, STM3 physically interacts with J2 to mediate its cytosolic redistribution and restricts J2 repressor activity by reducing its binding to target genes. Conversely, J2 limits STM3 regulation of target genes by transcriptional repression of the STM3 promoter and reducing STM3-binding activity. Our study thus reveals an antagonistic regulatory relationship in which STM3 and J2 control tomato IM determinacy and branch number.

Automated summary

The MADS-box transcription factors STM3 and J2 control tomato inflorescence branch number by mutually affecting each other's binding to FUL1. They activate or repress a set of common target genes through recognition and binding to CArG box motifs. STM3 physically interacts with J2 to mediate its cytosolic redistribution and inhibits its binding to target genes, while J2 limits STM3 regulation of target genes by transcriptional repression of the STM3 promoter and reducing STM3-binding activity.