Abstract
Centromere protein A (CENP-A) is a histone H3 variant that defines centromeric chromatin and is essential for centromere function. In most eukaryotes, CENP-A-containing chromatin is epigenetically maintained, and centromere identity is inherited from one cell cycle to the next. In the germ line of the holocentric nematode Caenorhabditis elegans, this inheritance cycle is disrupted. CENP-A is removed at the mitosis-to-meiosis transition and is reestablished on chromatin during diplotene of meiosis I. Here, we show that the N-terminal tail of CENP-A is required for the de novo establishment of centromeres, but then its presence becomes dispensable for centromere maintenance during development. Worms homozygous for a CENP-A tail deletion maintain functional centromeres during development but give rise to inviable offspring because they fail to reestablish centromeres in the maternal germ line. We identify the N-terminal tail of CENP-A as a critical domain for the interaction with the conserved kinetochore protein KNL-2 and argue that this interaction plays an important role in setting centromere identity in the germ line. We conclude that centromere establishment and maintenance are functionally distinct in C. elegans.
Highlights
Centromeres are crucial for the segregation of chromosomes into the daughter cells during cell division
Our results suggest that in C. elegans, the centromere protein A (CENP-A) N-terminal tail has acquired an important function in reestablishing the centromere in each generation in the adult germ line, but its presence becomes dispensable for centromere maintenance during development
The CENP-A N-terminal tail interacts with the central domain of KNL-2 In C. elegans, CENP-A is chromatin associated in dividing cells throughout development but is removed and reestablished, respectively, during different stages of the adult hermaphrodite germ line [27] (Fig 1)
Summary
Centromeres are crucial for the segregation of chromosomes into the daughter cells during cell division. They hold the sister chromatids together after DNA replication and serve as the sites of kinetochore formation. The centromere is defined by the histone variant centromere protein A (CENP-A), which forms the chromatin foundation for building the kinetochore and acts as an epigenetic mark to maintain centromere identity [1,2]. CENP-A is almost universally conserved but differs in amino acid sequence between different taxa, especially in the N-terminal tail [3,4,5,6]. The C-terminal histone fold domain (HFD) is more conserved, since it incorporates into the histone octamer and is under structural constraints [7]
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