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

Abstract

A spectacular but poorly recognized nuclear repatterning is the association of heterochromatic domains during interphase. Using basespecific 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.

Migration of repetitive DNAs during evolution of the permanent translocation heterozygosity in the oyster plant (Tradescantia section Rhoeo)

“…The strongly reshuffled PTH genomes express an extraordinary high degree of nuclear order and compartmentation (Golczyk et al 2014 , 2020 ). Both in the oyster plant and in Oenothera species, pericentromeric regions remain clustered and generate strong Rabl-polarization in cells of the root tip meristem and during pachytene (Golczyk 2011b , c ; Golczyk et al 2005 , 2008 , 2014 , 2020 ).…”

“…The strongly reshuffled PTH genomes express an extraordinary high degree of nuclear order and compartmentation (Golczyk et al 2014 , 2020 ). Both in the oyster plant and in Oenothera species, pericentromeric regions remain clustered and generate strong Rabl-polarization in cells of the root tip meristem and during pachytene (Golczyk 2011b , c ; Golczyk et al 2005 , 2008 , 2014 , 2020 ). Moreover, in the oyster plant, strikingly, regular non-random Rabl-polarized spatial chromatin dispositions were observed, including rings or chains of side-by-side juxtaposed pericentromeres in somatic interphase and during pachytene (Golczyk et al 2020 ).…”

“…Both in the oyster plant and in Oenothera species, pericentromeric regions remain clustered and generate strong Rabl-polarization in cells of the root tip meristem and during pachytene (Golczyk 2011b , c ; Golczyk et al 2005 , 2008 , 2014 , 2020 ). Moreover, in the oyster plant, strikingly, regular non-random Rabl-polarized spatial chromatin dispositions were observed, including rings or chains of side-by-side juxtaposed pericentromeres in somatic interphase and during pachytene (Golczyk et al 2020 ). Clustering of pericentromeric regions and the strong telomere-centromere polarization may have been an excellent framework for the whole arm translocations, subtelomere-pericentromere sequence migration and the resultant homogenization of all the pericentromeric domains by subtelomeric sequences (see Introduction ).…”

“…On the other hand, the remarkable potential of the oyster plant for Rabl-based nuclear constraints is likely to be also of a functional importance, presumably because it may help in regular pairing and disjunction in face of multiple homologies and other structural complications on chromosomes that resulted from extensive rearrangements. Indeed, the untypical aggregation of pericentromeric heterochromatin (from leptotene until late pachytene) coupled with the strong centromere-telomere polarization in the oyster plant (Golczyk 2011b , c ; Stack and Soulliere 1984 ; Golczyk et al 2020 ) resembles the meiotic behavior in allopolyploids (Naranjo and Corredor 2004 ). This similarity to hybrid species does suggest the potential danger of extensive homology search errors that could prevent proper meiotic pairing and a regular segregation of the Renner complexes.…”

“…Such exchanges could have been facilitated by the so-called Rabl configuration (Rabl 1885 ; Pouokam et al 2019 ), a remnant of the anaphase orientation of chromosomes from the preceding mitoses that is featured by polar clustering/association of the centromeres at interphase (Therizols et al 2010 ). Indeed, it was well-documented that the polarized centromere association occurs on a large scale in cycling meiotic and somatic cells and during development in oyster plant (Golczyk et al 2020 ). However, whole-arm inversions due to breakpoints at subtelomeric and pericentromeric area seem another interesting evolutionary scenario for verification (Golczyk 2011b , 2013 ; Golczyk et al 2010 ).…”