Abstract
Dinoflagellates have some of the largest genomes, and their liquid-crystalline chromosomes (LCCs) have high degrees of non-nucleosomal superhelicity with cation-mediated DNA condensation. It is currently unknown if condensins, pentameric protein complexes containing structural maintenance of chromosomes 2/4, commonly involved in eukaryotic chromosomes condensation in preparation for M phase, may be involved in the LCC structure. We find that CcSMC4p (dinoflagellate SMC4 homolog) level peaked at S/G2 phase, even though LCCs do not undergo global-decondensation for replication. Despite the differences in the chromosomal packaging system, heterologous CcSMC4p expression suppressed conditional lethality of the corresponding fission yeast mutant, suggesting conservation of some canonical condensin functions. CcSMC4p-knockdown led to sustained expression of the S-phase marker PCNAp, S-phase impediment, and distorted nuclei in the early stage of CcSMC4p depletion. Prolonged CcSMC4p-knockdown resulted in aneuploidal cells and nuclear swelling with increasing LCC decompaction–decondensation. Cumulatively, our data suggested CcSMC4p function was required for dinoflagellate S-phase progression, and we propose that condensin-mediated higher-order compaction provisioning is involved in the provision of local rigidity for the replisome.
Highlights
Accumulating evidence suggests chromatin remodeling between interphase and mitosis goes through condensin-dependent stages to their higher-order organization of nucleosomal chromosomes [1]
No global decondensation occurs during dinoflagellate DNA replication, and liquid crystalline chromosomes (LCCs) only undergo local decompaction during S-phase
Nucleosomal chromatin rigidity is contributed by nucleosome–nucleosome interactions [44], reinforced by this condensin-mediated chromosome domain association linker [15,18,45,46,47]
Summary
Accumulating evidence suggests chromatin remodeling between interphase and mitosis goes through condensin-dependent stages to their higher-order organization of nucleosomal chromosomes [1]. Condensin structural maintenance of chromosomes 2 and 4 subunits (SMC2 and SMC4) are essential genes in nucleosomal eukaryotes. Divalent cation-mediated condensation and DNA supercoils are synergistic in nurturing DNA liquid-crystalline phase transitions [8], and LCCs have 2–3 fold higher chromosomal divalent cations when compared to nc-chromosomes [9]. Cation chelation led to the orchestrated remodeling of higher-order structures, contrasted with little changes in nucleosomal chromatin following similar treatment [10,11,12]. LCCs recompacted upon re-introduction of divalent cations after mild chelation [12], implicating cation-mediated superhelical subunit modularity [12,13]
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