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

Abstract

Cohesin is a multi-unit protein complex from the structural maintenance of chromosomes (SMC) family, required for holding sister chromatids together during mitosis and meiosis. In yeast, the cohesin complex entraps sister DNAs within tripartite rings created by pairwise interactions between the central ring units SMC1 and SMC3 and subunits such as the α-kleisin SCC1 (REC8/SYN1 in meiosis). The complex is an indispensable regulator of meiotic recombination in eukaryotes. In Arabidopsis and maize, the SMC1/SMC3 heterodimer is a key determinant of meiosis. In Arabidopsis, several kleisin proteins are also essential: SYN1/REC8 is meiosis-specific and is essential for double-strand break repair, whereas AtSCC2 is a subunit of the cohesin SCC2/SCC4 loading complex that is important for synapsis and segregation. Other important meiotic subunits are the cohesin EXTRA SPINDLE POLES (AESP1) separase, the acetylase ESTABLISHMENT OF COHESION 1/CHROMOSOME TRANSMISSION FIDELITY 7 (ECO1/CTF7), the cohesion release factor WINGS APART-LIKE PROTEIN 1 (WAPL) in Arabidopsis (AtWAPL1/AtWAPL2), and the WAPL antagonist AtSWITCH1/DYAD (AtSWI1). Other important complexes are the SMC5/SMC6 complex, which is required for homologous DNA recombination during the S-phase and for proper meiotic synapsis, and the condensin complexes, featuring SMC2/SMC4 that regulate proper clustering of rDNA arrays during interphase. Meiotic recombination is the key to enrich desirable traits in commercial plant breeding. In this review, I highlight critical advances in understanding plant chromatid cohesion in the model plant Arabidopsis and crop plants and suggest how manipulation of crossover formation during meiosis, somatic DNA repair and chromosome folding may facilitate transmission of desirable alleles, tolerance to radiation, and enhanced transcription of alleles that regulate sexual development. I hope that these findings highlight opportunities for crop breeding.

Structural Maintenance of Chromosome 3 interacts with the Topoisomerase VI complex and contributes to the oxidative stress response inArabidopsis thaliana

“…Among the eleven additional interacting partners, TTN7 (TITAN7) / SMC3 (STRUCTURAL MAINTENANCE OF CHROMOSOMES 3) / AT2G27170 was identified under the two stringency conditions (Table S1). AtSMC3 encodes a subunit of cohesin, a ring shape chromatin architectural protein complex involved in sister chromatid cohesion (Tao et al ., 2007; Schubert et al ., 2009; Bolaños-Villegas et al ., 2013; Morales and Losada, 2018), gene expression (Dorsett and Merkenschlager, 2013), DNA repair (Sjögren and Ström, 2010; Bolaños-Villegas et al ., 2013; da Costa-Nunes et al ., 2014; Pradillo et al ., 2015), loop extrusion (Rowley and Corces, 2018) and many other processes related to chromatin dynamics (Cheng, Zhang and Pati, 2020; Bolaños-Villegas, 2021). The AtSMC3 protein is composed of two globular domains located at the C- and N-terminal extremities, forming an ATPase head necessary for the proper conformation of the cohesin ring during DNA entrapment or release (Arumugam et al ., 2003; Murayama and Uhlmann, 2014; Muir et al ., 2020).…”

Epigenetic histone H3 phosphorylation marks discriminate between univalent- and bivalent-forming chromosomes during canina asymmetrical meiosis

“…It is well established that the cohesin complex plays a central role in the successful transmission of chromosomes through meiosis ( Bolanos-Villegas, 2021 ). The complex includes meiosis-specific subunits, such as the meiotic α-kleisin REC8/SYN1 ( Castellano-Pozo et al , 2020 ), which are deposited on chromatin during leptotene.…”

Crossover interference mechanism: New lessons from plants

“…The sites where the DSB repair is processed using either one of the two polymorphic DNA sequences of the homologous chromosomes as the repair template can enter the pathway to form COs (Figure 1). During meiosis, a specific cohesin complex is installed between sister chromatids and contains REC8 instead of SCC1 (Chelysheva et al, 2005;Golubovskaya et al, 2006;Shao et al, 2011) as well as SMC1/3 (Lam et al, 2005;Bolaños-Villegas, 2021), SCC2 (Wang et al, 2020), SCC3 (Chelysheva et al, 2005), CTF7 (Bolaños-Villegas et al, 2013), and PDS5 (Pradillo et al, 2015). The putative helicase MCM8 (Crismani et al, 2013) and the cohesion-like SMC5/6 complex that favors sister chromatin HR repair in somatic cells are also tightly controlled during meiosis to allow the activity of interhomolog HR (Watanabe et al, 2009;Liu et al, 2014;Knoll et al, 2014;Chen et al, 2021;Zhu et al, 2021;Jiang et al, 2022).…”