Maize Dek15 Encodes the Cohesin-Loading Complex Subunit SCC4 and Is Essential for Chromosome Segregation and Kernel Development

Abstract

Cohesin complexes maintain sister chromatid cohesion to ensure proper chromosome segregation during mitosis and meiosis. In plants, the exact components and functions of the cohesin complex remain poorly understood. Here, we positionally cloned the classic maize (Zea mays) mutant defective kernel 15 (dek15), revealing that it encodes a homolog of SISTER CHROMATID COHESION PROTEIN 4 (SCC4), a loader subunit of the cohesin ring. Developing dek15 kernels contained fewer cells than the wild type, but had a highly variable cell size. The dek15 mutation was found to disrupt the mitotic cell cycle and endoreduplication, resulting in a reduced endosperm and embryo lethality. The cells in the dek15 endosperm and embryo exhibited precocious sister chromatid separation and other chromosome segregation errors, including misaligned chromosomes, lagging chromosomes, and micronuclei, resulting in a high percentage of aneuploid cells. The loss of Dek15/Scc4 function upregulated the expression of genes involved in cell cycle progression and stress responses, and downregulated key genes involved in organic synthesis during maize endosperm development. Our yeast two-hybrid screen identified the chromatin remodeling proteins chromatin remodeling factor 4, chromatin remodeling complex subunit B (CHB)102, CHB105, and CHB106 as SCC4-interacting proteins, suggesting a possible mechanism by which the cohesin ring is loaded onto chromatin in plant cells. This study revealed biological functions for DEK15/SCC4 in mitotic chromosome segregation and kernel development in maize.

The cohesin loader SCC2 contains a PHD finger that is required for meiosis in land plants

“…SCC2 has been reported to interact with SCC4 in several organisms, including humans, maize and Arabidopsis [25,27,35]. Our yeast two-hybrid assay also confirmed their physical interaction (S9A and S9B Fig).…”

“…Recently, SCC4 was also identified in Arabidopsis and maize. Similar to AtSCC2, complete loss of function of SCC4 is also embryonic lethal in both Arabidopsis and maize, consistent with their roles in mitotic cell division [27,35,37]. Nonetheless, the gene expression pattern of AtSCC2 does not fully overlap with AtSCC4 [27].…”

“…The human SCC2-SCC4 complex also interacts with the MCM2-7 complex [34]. In Zea mays (maize), SCC4/Dek15 interacts with several chromatin remodeling proteins [35]. Together, these results suggest that recruitment of SCC2/4 onto chromatin likely depends on SCC4-interacting factors such as Ctf19 and the MCM2-7 complex, while SCC2 is important for loading cohesin.…”

Loss of Function of an RNA Polymerase III Subunit Leads to Impaired Maize Kernel Development

“…Endoreduplication is a specialized type of cell cycle, in which one or more rounds of DNA synthesis are performed without mitosis, resulting in polyploid cells (Larkins et al, 2001). A strong correlation between endoreduplication and cell size has been observed in the maize endosperm (Sabelli et al, 2013;He et al, 2019). In smk7, endoreduplication was affected and the endosperm cells were larger; furthermore, expression of MCM2-7, RBR3, PCNA1, and PCNA2 increased considerably in mutant kernels.…”

“…Dek15 encodes a homolog of SISTER CHROMATID COHESION PROTEIN4. The chromosome separation error in dek15 results in reduced endosperm size and embryo lethality (He et al, 2019). The varied kernel size1 mutant contains a mutation in Zmkin11 that causes impaired spindle assembly, sister chromatid separation, and phragmoplast formation, leading to varying degrees of defective cell proliferation, ultimately resulting in the formation of seeds of different sizes (Huang et al, 2019).…”