The Cohesin Complex Subunit ZmSMC3 Participates in Meiotic Centromere Pairing in Maize

Abstract

Meiosis consists of two highly conserved nuclear divisions, which allow eukaryotes to maintain their chromosome number through sexual reproduction. The successful completion of meiosis depends on homologous chromosome pairing. Centromere interactions during early meiotic prophase I facilitate homologous chromosome pairing, but the underlying mechanism is unclear. Here, we performed chromatin immunoprecipitation-mass spectrometry analysis of maize (Zea mays) anthers during early meiotic prophase I using anti-centromeric histone H3 (CENH3) antibodies and determined that the cohesin subunit Structural Maintenance of Chromosome3 (SMC3) interacts with CENH3 during this period. SMC3 is enriched at centromeres and along chromosome arms in threads from leptotene to pachytene and might promote interactions between homologous centromeres. We observed dysfunctional SMC3 assembly in meiotic-specific maize mutants with defective centromere pairing. In SMC3 RNAi meiocytes, centromere pairing defects were observed during early meiotic prophase I, SMC3 was weakly associated with centromeres, and SMC3 did not localize to the chromosome arms. In wild-type mitosis, SMC3 is associated with chromatin and is enriched at centromeres from prophase to anaphase. CRISPR-Cas9induced Zmsmc3 mutants showed premature loss of sister chromatid cohesion and mis-segregation of chromosomes in mitotic spreads. Our findings suggest that in addition to sister chromatid cohesion, ZmSMC3 participates in meiotic centromere pairing.

Plant 3D genomics: the exploration and application of chromatin organization

“…This article is protected by copyright. All rights reserved (Liu Cm et al, 2002;Zhang et al, 2020). At the same time, TADs in plants are not as distinct as in animals.…”

“…In mammals, the mechanism of the 3D genome organization has been explored preliminarily (Liu et al ., 2002; Hyman et al ., 2014; Fudenberg et al ., 2016; Boija et al ., 2018; Chong et al ., 2018; Shin et al ., 2019; Zhang et al ., 2020). A phase separation process plays an important role in distinguishing chromatin compartments.…”

The Role of Structural Maintenance of Chromosomes Complexes in Meiosis and Genome Maintenance: Translating Biomedical and Model Plant Research Into Crop Breeding Opportunities

“…New alleles may need to be developed by CRISPR-Cas9 to fully characterize the function of CTF18 in plants. The maize SMC3 homolog has been successfully characterized with genome editing by CRISPR-Cas9 ( Zhang et al, 2020 ). The homolog fulfills a crucial role during the establishment of centromeric pairing during meiosis and sister chromatid cohesion during mitosis (in root tips; Zhang et al, 2020 ).…”

“…The maize SMC3 homolog has been successfully characterized with genome editing by CRISPR-Cas9 ( Zhang et al, 2020 ). The homolog fulfills a crucial role during the establishment of centromeric pairing during meiosis and sister chromatid cohesion during mitosis (in root tips; Zhang et al, 2020 ). So, maize might be amenable to the study of SMC3 acetylation dynamics during meiosis and mitosis and perhaps lead to the discovery of novel phenotypes.…”

“…Of particular interest in modern agriculture is the control of crossover (CO) formation during meiosis, because the low frequency and uneven patterning of COs has traditionally required breeders to work with large populations over many generations to produce desirable haplotypes ( Taagen et al, 2020 ). Fortunately, genome sequencing and advanced genome editing by CRISPR-Cas9 in rice ( Li et al, 2020 ) and maize ( Zhang et al, 2020 ) may enable the translation of knowledge obtained in humans, yeast and Arabidopsis thaliana .…”