Abstract
The genome’s adaptability to environmental changes, especially during rapid climatic fluctuations, underlies the existence and evolution of species. In the wild, genetic and epigenetic genomic changes are accompanied by significant alterations in the complex nuclear repetitive DNA fraction. Current intraspecific polymorphism of repetitive DNA is closely related to ongoing chromosomal rearrangements, which typically result from erroneous DNA repair and recombination. In this study, we addressed tandem repeat patterns and interaction/reshuffling both in pollen mother cell (PMC) development and somatogenesis in the wild diploid cereal Aegilops speltoides, with a focus on genome repatterning and stabilization. Individual contrasting genotypes were investigated using the fluorescent in situ hybridization (FISH) approach by applying correlative fluorescence and electron microscopy. Species-specific Spelt1 and tribe-specific Spelt52 tandem repeats were used as the markers for monitoring somatic and meiotic chromosomal interactions and dynamics in somatic interphase nuclei. We found that, the number of tandem repeat clusters in nuclei is usually lower than the number on chromosomes due to the associations of clusters of the same type in common blocks. In addition, tightly associated Spelt1–Spelt52 clusters were revealed in different genotypes. The frequencies of nonhomologous/ectopic associations between tandem repeat clusters were revealed in a genotype-/population-specific manner. An increase in the number of tandem repeat clusters in the genome causes an increase in the frequencies of their associations. The distal/terminal regions of homologous chromosomes are separated in nuclear space, and nonhomologous chromosomes are often involved in somatic recombination as seen by frequently formed interchromosomal chromatin bridges. In both microgametogenesis and somatogenesis, inter- and intrachromosomal associations are likely to lead to DNA breaks during chromosome disjunction in the anaphase stage. Uncondensed/improperly packed DNA fibers, mainly in heterochromatic regions, were revealed in both the meiotic and somatic prophases that might be a result of broken associations. Altogether, the data obtained showed that intraorganismal dynamics of repetitive DNA under the conditions of natural out-crossing and artificial intraspecific hybridization mirrors the structural plasticity of the Ae. speltoides genome, which is interlinked with genetic diversity through the species distribution area in contrasting ecogeographical environments in and around the Fertile Crescent.
Highlights
In the wild, the genome’s ability to adapt to changing environments, especially in a period of significant climatic changes, underlies the existence of the species and its evolution (Grant, 1981; Tchernov, 1988)
We addressed repetitive DNA dynamics in the Ae. speltoides genome, both during pollen mother cell (PMC) development and in somatogenesis, with a focus on genome repatterning and stabilization
We found that Spelt1 and Spelt52 demonstrated sequence-specific and genotype-/populationspecific abundances and dynamics in interphase nuclei
Summary
The genome’s ability to adapt to changing environments, especially in a period of significant climatic changes, underlies the existence of the species and its evolution (Grant, 1981; Tchernov, 1988). Genetic changes and epigenetic modifications are accompanied by significant diversification in the abundances and patterns of repetitive DNA, which is the prevailing genomic fraction in cereals (Bennetzen, 1996; Feschotte et al, 2002). Plants with intermediate ligustica/aucheri phenotypes have been observed in the wild, suggesting genetic changes in the linked group of genes (Belyayev and Raskina, 2013). The Ae. speltoides genome is characterized by high intraspecific polymorphism in abundance and patterns of different types of repetitive DNA, TEs (Middleton et al, 2013; Yaakov et al, 2013) and tandem repeats (Badaeva et al, 1996; Raskina et al, 2011; Molnár et al, 2014; Raskina, 2017), which underlie permanent intraorganismal and intraspecific genome reshuffling (Belyayev et al, 2010; Shams and Raskina, 2018). The current intraspecific polymorphism and intraorganismal dynamics of the highly repetitive DNA fraction in the genome of Ae. speltoides is largely caused by ongoing chromosomal rearrangements, which are typical results of erroneous DNA repair and recombination (Andersen and Sekelsky, 2010; Knoll et al, 2014; Zeman and Cimprich, 2015)
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