The H3R2me2a demethylase JMJ10 regulates tomato fruit size through its interaction with the transcription factor BZR1.3.

Abstract

Fruit weight and size are fundamental traits in tomato breeding and critical determinants of yield. Although several histone-modifying enzymes have been implicated in tomato fruit ripening, the role of histone arginine methylation in fruit development remains unknown. Here, we identify the histone H3R2me2a demethylase Jumonji C-domain-containing proteins 10 (JMJ10) as a key regulator of fruit size in tomato (Solanum lycopersicum). Loss of JMJ10 function reduces fruit size, whereas JMJ10 overexpression enhances fruit growth, primarily by promoting pericarp cell expansion. JMJ10 specifically demethylates H3R2me2a at key fruit size-associated genes, including FW11.3, CDF4, EXP2, EXP5, XTH8, and PRE2, thereby promoting their transcription. Furthermore, we show that JMJ10 physically interacts with the transcription factor Brassinazole-Resistant 1.3 (BZR1.3), which recruits JMJ10 to its target genes. The jmj10 bzr1.3 double mutants exhibit a more severe reduction in fruit size compared to either single mutant, confirming a synergistic interaction between JMJ10 and BZR1.3. ChIP-qPCR analysis showed that JMJ10 occupancy at its target loci is significantly reduced in the bzr1.3 mutant, suggesting that JMJ10 binding is BZR1.3-dependent. Additionally, BZR1.3 recruits JMJ10 to enhance the expression of these genes by facilitating H3R2me2a removal. Collectively, our findings reveal a mechanism by which BZR1.3 recruits JMJ10, a H3R2me2a demethylase, to coordinate the epigenetic regulation of fruit size in tomato.