Pericentromere clustering in Tradescantia section Rhoeo involves self-associations of AT- and GC-rich heterochromatin fractions, is developmentally regulated, and increases during differentiation

Arleta Limanówka,Hieronim Golczyk,Anna Uchman-Książek

doi:10.1007/s00412-020-00740-x

Arleta Limanówka, Hieronim Golczyk + Show 1 more

Open Access

https://doi.org/10.1007/s00412-020-00740-x

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Abstract

A spectacular but poorly recognized nuclear repatterning is the association of heterochromatic domains during interphase. Using base-specific fluorescence and extended-depth-of-focus imaging, we show that the association of heterochromatic pericentromeres composed of AT- and GC-rich chromatin occurs on a large scale in cycling meiotic and somatic cells and during development in ring- and bivalent-forming Tradescantia spathacea (section Rhoeo) varieties. The mean number of pericentromere AT-rich domains per root meristem nucleus was ca. half the expected diploid number in both varieties, suggesting chromosome pairing via (peri)centromeric regions. Indeed, regular pairing of AT-rich domains was observed. The AT- and GC-rich associations in differentiated cells contributed to a significant reduction of the mean number of the corresponding foci per nucleus in relation to root meristem. Within the first 10 mm of the root, the pericentromere attraction was in progress, as if it was an active process and involved both AT- and GC-rich associations. Complying with Rabl arrangement, the pericentromeres preferentially located on one nuclear pole, clustered into diverse configurations. Among them, a strikingly regular one with 5–7 ring-arranged pericentromeric AT-rich domains may be potentially engaged in chromosome positioning during mitosis. The fluorescent pattern of pachytene meiocytes and somatic nuclei suggests the existence of a highly prescribed ring/chain type of chromocenter architecture with side-by-side arranged pericentromeric regions. The dynamics of pericentromere associations together with their non-random location within nuclei was compared with nuclear architecture in other organisms, including the widely explored Arabidopsis model.

Highlights

IntroductionSpatial arrangement of chromosome domains during interphase is important for biology since it is intimately and functionally linked to gene expression and other essential cellular processes (Kosak et al 2007; Lanctôt et al 2007; Schneider and Grosschedl 2007; Fedorova and Zink 2009; Göndör and Ohlsson 2009; Misteli and Soutoglou 2009; Padeken and Heun 2014; Cabianca and Gasser 2016; Poulet et al 2017; Maass et al 2018)
Heterochromatin is a genome part that remains condensed during interphase, detected as deeply staining nuclear bodies—chromocenters, which can associate into higher-order aggregates—collective
The results indicate that the heterochromatin of a collective chromocenter comprises separate higher-order domains consisting of one to several pericentromeres (Fig. 1b) and that these domains are connected via chromatin fibers (Fig. 3b, c)

Summary

Introduction

Spatial arrangement of chromosome domains during interphase is important for biology since it is intimately and functionally linked to gene expression and other essential cellular processes (Kosak et al 2007; Lanctôt et al 2007; Schneider and Grosschedl 2007; Fedorova and Zink 2009; Göndör and Ohlsson 2009; Misteli and Soutoglou 2009; Padeken and Heun 2014; Cabianca and Gasser 2016; Poulet et al 2017; Maass et al 2018). Among others, creating nuclear order/constraints, arranging of chromosome territories and nuclear compartmentation, regulating the functional activity of the nucleus, genome guarding and packaging, and meiotic segregation, and facilitating homologous chromosome recognition and juxtaposition have been postulated (Fussell 1987; Dernburg et al 1996; Ceccarelli et al 1998; Chubykin 2001; Wijchers et al 2015; Ostromyshenskii et al 2018 and literature therein; Jagannathan et al 2018; Falk et al 2019). It is widely accepted that as a PTH species, it had undergone a series of reciprocal translocations as a result of which one complete meiotic ring is formed and there are no two fully homologous chromosomes in the karyotype. To assemble a complete ring, it is enough that only one of the genomes has been altered by segmental interchanges, more likely is the Oenothera scenario, where most or all the members of the karyotype are segmental interchange chromosomes (Cleland 1972; Golczyk 2013 and literature therein)

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