Mega-sized pericentromeric blocks of simple telomeric repeats and their variants reveal patterns of chromosome evolution in ancient Cycadales genomes

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Authors

VOZÁROVÁ Radka WANG Wencai LUNEROVÁ Jana SHAO Fengqing PELLICER Jaume LEITCH Ilia J. LEITCH Andrew R. KOVAŘÍK Aleš

Year of publication 2022
Type Article in Periodical
Magazine / Source The Plant Journal
MU Faculty or unit

Faculty of Science

Citation
Web https://onlinelibrary.wiley.com/doi/10.1111/tpj.15969
Doi http://dx.doi.org/10.1111/tpj.15969
Keywords Telomeres; genome evolution; chromosome rearrangements; Cycadaceae; gymnosperms; centromeres; epigenetics
Description Simple telomeric repeats composed of 6-7 iterating nucleotide units are important sequences typically found at the ends of chromosomes. Here we analyzed their abundance and homogeneity in 42 gymnosperm (29 newly sequenced), 29 angiosperm (1 newly sequenced) and 8 bryophytes using bioinformatics, conventional cytogenetic and molecular biology approaches to explore their diversity across land plants. We found more than 10,000-fold variation in the amounts of telomeric repeats among the investigated taxa. Repeat abundance was positively correlated with increasing intragenomic sequence heterogeneity and occurrence at non-telomeric positions, but there was no correlation with genome size. The highest abundance/heterogeneity was found in the gymnosperm genus Cycas (Cycadaceae), in which megabase-sized blocks of telomeric repeats (i.e. billions of copies) were identified. Fluorescent in situ hybridization (FISH) experiments using variant-specific probes revealed canonical Arabidopsis-type telomeric TTTAGGG repeats at chromosome ends, while pericentromeric blocks comprised at least four major telomeric variants with decreasing abundance: TTTAGGG>TTCAGGG >TTTAAGG>TTCAAGG. Such a diversity of repeats was not found in the sister cycad family Zamiaceae or in any other species analyzed. Using immunocytochemistry, we showed that the pericentromeric blocks of telomeric repeats overlapped with histone H3 serine 10 phosphorylation signals. We show that species of Cycas have amplified their telomeric repeats in centromeric and telomeric positions on telocentric chromosomes to extraordinary high levels. Ancestral chromosome number reconstruction suggests their occurrence is unlikely to be the product of ancient Robertsonian chromosome fusions. We speculate as to how the observed chromosome dynamics may be associated with the diversification of cycads.
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