Abstract
Tight regulation of gene transcription and mRNA splicing is essential for plant growth and development. Here we demonstrate that a plant-specific protein, EMBRYO DEFECTIVE 1579 (EMB1579), controls multiple growth and developmental processes in Arabidopsis. We demonstrate that EMB1579 forms liquid-like condensates both in vitro and in vivo, and the formation of normal-sized EMB1579 condensates is crucial for its cellular functions. We found that some chromosomal and RNA-related proteins interact with EMB1579 compartments, and loss of function of EMB1579 affects global gene transcription and mRNA splicing. Using floral transition as a physiological process, we demonstrate that EMB1579 is involved in FLOWERING LOCUS C (FLC)-mediated repression of flowering. Interestingly, we found that EMB1579 physically interacts with a homologue of Drosophila nucleosome remodeling factor 55-kDa (p55) called MULTIPLE SUPPRESSOR OF IRA 4 (MSI4), which has been implicated in repressing the expression of FLC by forming a complex with DNA Damage Binding Protein 1 (DDB1) and Cullin 4 (CUL4). This complex, named CUL4-DDB1MSI4, physically associates with a CURLY LEAF (CLF)-containing Polycomb Repressive Complex 2 (CLF-PRC2). We further demonstrate that EMB1579 interacts with CUL4 and DDB1, and EMB1579 condensates can recruit and condense MSI4 and DDB1. Furthermore, emb1579 phenocopies msi4 in terms of the level of H3K27 trimethylation on FLC. This allows us to propose that EMB1579 condensates recruit and condense CUL4-DDB1MSI4 complex, which facilitates the interaction of CUL4-DDB1MSI4 with CLF-PRC2 and promotes the role of CLF-PRC2 in establishing and/or maintaining the level of H3K27 trimethylation on FLC. Thus, we report a new mechanism for regulating plant gene transcription, mRNA splicing, and growth and development.
Highlights
Plant growth and development are tightly regulated in response to many endogenous and environmental signals by genetic and cellular programs that determine plant form
Subnuclear compartmentalization might be especially important in mediating rapid changes in gene transcription and mRNA splicing in response to intrinsic and environmental variations, as proteins associated with transcription and mRNA splicing are often localized to nuclear speckles or dots [21,22]
We found that the number of meristematic cells was decreased significantly in emb1579 mutants compared to wild type (WT) (Fig 1G)
Summary
Plant growth and development are tightly regulated in response to many endogenous and environmental signals by genetic and cellular programs that determine plant form. Subnuclear compartmentalization might be especially important in mediating rapid changes in gene transcription and mRNA splicing in response to intrinsic and environmental variations, as proteins associated with transcription and mRNA splicing are often localized to nuclear speckles or dots [21,22] Those proteins often exhibit multivalent features that are contributed by repetitive folded domains and/or disordered regions ( referred to as intrinsically disordered protein regions [IDRs]) [23], and they are able to undergo liquid-liquid phase separation (LLPS). The emerging scenario is that MSI4 forms the CUL4-DDB1MSI4 complex, which physically interacts with CLF-PRC2 to establish and/or maintain the level of H3K27me on the FLC locus to control the expression of FLC [36]. We propose that EMB1579 condensates condense important biomolecules in the Arabidopsis nucleus to regulate their functions in controlling key nuclear events, such as gene transcription and mRNA splicing. Our study reveals a new mechanism for the regulation of plant growth and development through LLPS of EMB1579
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