Reproductive mode and ploidy are associated with distinct organization of clustered centromeric regions in...

In most eukaryotes, chromosomes are monocentric, each containing a single centromeric region. However, plant-parasitic nematodes of the genus Meloidogyne display a unique, repeat-based and clustered centromere organization. This unusual centromere structure, together with their asexual reproductive strategies, provides an opportunity to investigate the diversity and evolution of centromere organization.

Using high-quality genome assemblies, we examine the genome organization and evolutionary patterns of centromeres in six Meloidogyne species differing in reproductive strategies (mitotic parthenogenesis vs. meiotic reproduction) and ploidy (polyploid vs. diploid). All species possess conserved CenH3 and 19-bp box-containing tandem repeats in their centromeres. Centromeric regions in three closely related and one distantly related mitotic/polyploid species exhibit a complex organization, predominantly consisting of higher-order arrangements of centromeric arrays associated with both autonomous and non-autonomous Helitron transposons, leading to longer and more dispersed centromeric regions. In contrast, meiotic/diploid species have simpler, less expanded centromeres that lack Helitron elements, highlighting the role of Helitron-mediated amplification and spread of centromeres in mitotic/polyploid species.

These findings suggest that reproductive strategy and/or genome ploidy may influence centromere organization, although it remains to be determined whether these factors are causative or simply correlated with differences in centromere organization. We suggest that the expansion-prone centromeric regions in mitotic/polyploid Meloidogyne may drive rapid chromosome evolution, potentially influencing their adaptability to environmental changes.