Parallel Evolution of X Chromosome-Specific Structural Maintenance of Chromosomes Complexes in Two Nematode Lineages

Area of Science:

• Evolutionary biology
• Genetics
• Molecular biology

Background:

• X chromosome dosage compensation mechanisms vary across species.
• Understanding the evolution of these mechanisms is crucial for comprehending gene regulation diversity.
• Nematodes offer a unique system to study sex chromosome evolution due to their distinct ancestry.

Purpose of the Study:

• To investigate the evolutionary history of X chromosome dosage compensation in nematodes.
• To identify the role of structural maintenance of chromosomes (SMC) complexes in dosage compensation.
• To explore the co-evolution of epigenetic modifications and dosage compensation mechanisms.

Main Methods:

• Phylogenetic analysis of Caenorhabditis elegans dosage compensation complex.
• Comparative analysis of epigenetic signatures, including X-specific topologically associating domains and H4K20me1 enrichment.
• Differential gene expression analysis between sexes in multiple nematode species.

Main Results:

• Condensin-mediated dosage compensation evolved recently in Caenorhabditis following SMC-4 duplication.
• Independent SMC-4 duplication and similar epigenetic signatures in Pristionchus pacificus suggest convergent evolution of condensin-mediated dosage compensation.
• Dosage compensation predates X-specific condensins, with H4K20 methylation playing a role in some species.
• Steinernema hermaphroditum lacks key features of condensin-mediated dosage compensation.

Conclusions:

• Condensin-mediated dosage compensation has evolved at least twice independently in nematodes.
• The evolution of X-specific condensins is not a prerequisite for dosage compensation.
• Epigenetic modifications like H4K20 methylation may facilitate the evolution of dosage compensation.
• SMC complexes have been co-opted multiple times, highlighting constraints in evolving chromosome-wide gene regulatory mechanisms.