Abstract
Centromere drive model describes an evolutionary process initiated by centromeric repeats expansion, which leads to the recruitment of excess kinetochore proteins and consequent preferential segregation of an expanded centromere to the egg during female asymmetric meiosis. In response to these selfish centromeres, the histone protein CenH3, which recruits kinetochore components, adaptively evolves to restore chromosomal parity and counter the detrimental effects of centromere drive. Holocentric chromosomes, whose kinetochores are assembled along entire chromosomes, have been hypothesized to prevent expanded centromeres from acquiring a selective advantage and initiating centromere drive. In such a case, CenH3 would be subjected to less frequent or no adaptive evolution. Using codon substitution models, we analyzed 36 CenH3 sequences from 35 species of the holocentric family Cyperaceae. We found 10 positively selected codons in the CenH3 gene [six codons in the N-terminus and four in the histone fold domain (HFD)] and six branches of its phylogeny along which the positive selection occurred. One of the positively selected codons was found in the centromere targeting domain (CATD) that directly interacts with DNA and its mutations may be important in centromere drive suppression. The frequency of these positive selection events was comparable to the frequency of positive selection in monocentric clades with asymmetric female meiosis. Taken together, these results suggest that preventing centromere drive is not the primary adaptive role of holocentric chromosomes, and their ability to suppress it likely depends on their kinetochore structure in meiosis.
Highlights
During cell division, kinetochore assembly and microtubule attachment are typically limited to a small chromosomal region known as the centromere
Four positively selected codons were in the histone fold domain (HFD), including one codon in the loop-1 region of the centromere targeting domain (CATD; Figure 1), which directly interacts with the DNA (Dalal et al, 2007)
This comparison showed that the frequency of positive selection acting on the CenH3 gene in Cyperaceae is similar to that in lineages with monocentric chromosomes and asymmetric female meiosis, where centromere drive takes place (Zedek and Bureš, 2016b)
Summary
Kinetochore assembly and microtubule attachment are typically limited to a small chromosomal region known as the centromere. Centromere drive model describes an evolutionary process during which “selfish” centromeres exploit asymmetric female meiosis to end up in the animal egg (or seed-plant megaspore, which is the only surviving meiotic product) and spread through the population (Henikoff et al, 2001). It begins with an expansion of the centromeric satellite array, which gains the ability to attract more CenH3 nucleosomes than its counterpart on the homologous chromosome. Summarized, (i) it has been shown that centromeric satellites can affect the positioning of CenH3 (Zhang et al, 2013; Akera et al, 2017) and that centromeres with more satellite repeats recruit more CenH3 and increase their transmission to the egg relative to homologous centromeres with fewer repeats (Iwata-Otsubo et al, 2017); (ii) the meiotic spindle asymmetry (the key assumption) based on differential tyrosination of microtubules (emanating from polar body and egg pole) has been directly linked with size-dependent centromere competition (Akera et al, 2017) and recently even characterized on the molecular level (Akera et al, 2019); (iii) the negative effects of centromere drive on fitness have been documented in monkeyflowers population (Fishman and Kelly, 2015; Finseth et al, 2020), which was shown (iv) to be counterbalanced by selective sweep in CenH3, proving evolutionary arms race between selfish centromeres and the key kinetochore protein (Finseth et al, 2020)
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