Regulation of Meiotic Chromosome Condensation Progression by the Arabidopsis MMD1 Protein and Its Interacting Protein

Chromosome condensation is required for proper chromosome segregation during cell division and depends on the function of the condensin complex. Although mitotic chromosome condensation and the function of mitotic condensins have been studied extensively, the knowledge for meiotic condensin function and regulation is largely unknown. During meiosis, chromosome condensation occurs in parallel to homolog interactions, including pairing, synapsis and recombination. Meiotic chromosome condensation must be coordinated with such homolog interactions and can be separated into three stages: (1) early prophase I condensation forming axial elements; (2) late prophase I condensation resulting in bivalents; (3) from prometaphase I to metaphase I ending with highly compacted chromosome pairs aligned at the equatorial plate. Therefore, meiotic chromosome condensation likely requires more regulatory mechanisms than mitotic condensation. The Arabidopsis MMD1 protein contains a PHD finger and was previously found to be critical for normal meiotic progression. Our recent analysis indicated that the mutant meiotic chromosomes undergo condensation through the pachytene stage of prophase I without obvious defects, suggesting that the formation of axial elements and synapsis are normal. However, metaphase I chromosomes appeared to be under-condensed, suggesting that the late stage condensation is abnormal. We further demonstrated that role of MMD1 in chromosome condensation requires the PHD finger, which binds to histone H3 tails. Conserved MMD1 sequences outside the PHD domain was found to interact with a histone demethaylase. In addition, MMD1 binds to the promoter of CAP-D3 encoding a condensing subunit, and enhances the binding of JMJ16 to the same promoter. The expression of CAP-D3 was reduced in the mmd1 mutant, and the cap-d3 mutant meiocytes exhibit similar defects to those of the mmd1 mutant. We propose that MMD1 constitutes a novel class of histone readers that is specifically required for meiotic chromosome condensation in plants.