The PHD Finger Protein MMD1/DUET Ensures the Progression of Male Meiotic Chromosome Condensation and Directly Regulates the Expression of the Condensin Gene CAP-D3

Abstract

Chromosome condensation, a process mediated by the condensin complex, is essential for proper chromosome segregation during cell division. Unlike rapid mitotic chromosome condensation, meiotic chromosome condensation occurs over a relatively long prophase I and is unusually complex due to the coordination with chromosome axis formation and homolog interaction. The molecular mechanisms that regulate meiotic chromosome condensation progression from prophase I to metaphase I are unclear. Here, we show that the Arabidopsis thaliana meiotic PHD-finger protein MMD1/DUET is required for progressive compaction of prophase I chromosomes to metaphase I bivalents. The MMD1 PHD domain is required for its function in chromosome condensation and binds to methylated histone tails. Transcriptome analysis and qRT-PCR showed that several condensin genes exhibit significantly reduced expression in mmd1 meiocytes. Furthermore, MMD1 specifically binds to the promoter region of the condensin subunit gene CAP-D3 to enhance its expression. Moreover, cap-d3 mutants exhibit similar chromosome condensation defects, revealing an MMD1-dependent mechanism for regulating meiotic chromosome condensation, which functions in part by promoting condensin gene expression. Together, these discoveries provide strong evidence that the histone reader MMD1/DUET defines an important step for regulating the progression of meiotic prophase I chromosome condensation.

TDR INTERACTING PROTEIN 3, encoding a PHD‐finger transcription factor, regulates Ubisch bodies and pollen wall formation in rice

“…Another PHD‐finger protein, MMD1/DUET, is reportedly involved in chromosome organization and progression during male meiosis in Arabidopsis (Reddy et al ., ; Yang, ). Recent studies revealed that MMD1/DUET directly activates its target genes CAP‐D3 and TDM1 to regulate, respectively, chromosome condensation and microtubule organization, cell cycle transitions during male meiosis (Andreuzza et al ., ; Wang et al ., ). However, our results showed that tip3 could normally undergo meiosis and form dyads and tetrads, as observed by DAPI staining (Figure S1).…”

“…MS1 encodes a PHD transcriptional factor and its ortholog in rice PTC1 , barley HvMS1 and maize ZmMs7 , all of which play key roles in regulating transcription during programmed tapetum development and pollen wall formation (Wilson et al ., ; Ito et al ., ; Yang et al ., ; Li et al ., 2011a; Gomez and Wilson, ; Zhang et al ., 2017a). MMD1/DUET, another PHD protein, is required for the organization and progression of chromosomes during male meiosis (Reddy et al ., ; Yang, ; Andreuzza et al ., ; Wang et al ., ). In this work, we identified a PHD‐finger protein (TIP3) in rice by a map‐based cloning strategy.…”

SDG2-Mediated H3K4me3 Is Crucial for Chromatin Condensation and Mitotic Division during Male Gametogenesis in Arabidopsis

“…Loss of MMD1/DUET function causes multiple defects, including cytoplasmic collapse and cell death of meiocytes with possible DNA fragmentation, delay in progression and arrest at metaphase I, and formation of aberrant meiotic products such as dyads and triads (Reddy et al, 2003;Yang et al, 2003;Andreuzza et al, 2015). More recent studies demonstrate that the MMD1/DUET PHD-finger exhibits binding activities to modified histone H3 peptides including H3K4me2 and H3K4me3 and that its mutation compromises MMD1/ DUET biological function (Andreuzza et al, 2015;Wang et al, 2016). Based on these previous studies, one can predict that H3K4me2/me3 might play crucial roles in Arabidopsis male meiosis.…”

Fine mapping of a male sterility gene ms-3 in a novel cucumber (Cucumis sativus L.) mutant

“…The PHD finger can interact with different modified histone peptides and is required for specific binding to H3K3me2 (Patel and Wang 2013 ). A recent study showed that MMD1 is required for progressive compaction of prophase I chromosome to metaphase I bivalents, by ensuring the progression of male meiotic chromosome condensation, a process in which the PHD domain is essential (Wang et al 2016 ). MMD1 regulates the expression of the condensin gene, CAP - D3 , by directly binding to its promoter region in male meiocytes (Wang et al 2016 ).…”

“…A recent study showed that MMD1 is required for progressive compaction of prophase I chromosome to metaphase I bivalents, by ensuring the progression of male meiotic chromosome condensation, a process in which the PHD domain is essential (Wang et al 2016 ). MMD1 regulates the expression of the condensin gene, CAP - D3 , by directly binding to its promoter region in male meiocytes (Wang et al 2016 ). Our analyses suggested that Csa3M006660 and MMD1 may have similar functions.…”