A satellite explosion in the genome of holocentric nematodes

Abstract

Centromere sequences in the genome are associated with the formation of kinetochores, where spindle microtubules grow in mitosis. Centromere sequences usually have long tandem repeats (satellites). In holocentric nematodes it is not clear how kinetochores are formed during mitosis; they are distributed throughout the chromosomes. For this reason it appeared of interest to study the satellites in nematodes in order to determine if they offer any clue on how kinetochores are assembled in these species. We have studied the satellites in the genome of six nematode species. We found that the presence of satellites depends on whether the nematode chromosomes are holocentric or monocentric. It turns out that holocentric nematodes are unique because they have a large number of satellites scattered throughout their genome. Their number, length and composition are different in each species: they apparently have very little evolutionary conservation. In contrast, no scattered satellites are found in the monocentric nematode Trichinella spiralis. It appears that the absence/presence of scattered satellites in the genome distinguishes monocentric from holocentric nematodes. We conclude that the presence of satellites is related to the holocentric nature of the chromosomes of most nematodes. Satellites may stabilize a higher order structure of chromatin and facilitate the formation of kinetochores. We also present a new program, SATFIND, which is suited to find satellite sequences.

Figure 1. Evolutionary position of the different subphyla of nematodes (adapted from reference 10).

Monocentric species have a single large centromere in each chromosome. Holocentric species have centromeres spread over the whole chromosome. Centromeres nucleate the formation of kinetochores, the attaching point of microtubules during mitosis. The holocentric/monocentric nature of the chromosomes is indicated in different colors at the right side of the figure; kinetochores are indicated as red dots.

Figure 2. Distribution of motif sizes in the satellites of different nematodes.

For sequences longer than 60 bases the data have been merged in bins of 5 bases. The percentage of short motifs (<50 bases) is the largest in all cases, with up to 95% in C.briggsae. Hexadecamer motifs are extremely abundant in this species; their actual frequency is indicated by an arrow in the figure.