Fundamentally different repetitive element composition of sex chromosomes in Rumex acetosa

Abstract

Background and Aims Dioecious species with well-established sex chromosomes are rare in the plant kingdom. Most sex chromosomes increase in size but no comprehensive analysis of the kind of sequences which drive this expansion has been presented. Here, we analyse sex chromosome structure in common sorrel (Rumex acetosa), a dioecious plant with XY1Y2 sex determination, and we provide the first chromosome specific repeatome analysis for a plant species possessing sex chromosomes. Methods We flow-sorted and separately sequenced sex chromosomes and autosomes in R. acetosa using the two-dimensional Fluorescence In Situ Hybridization in Suspension (FISHIS) method and Illumina sequencing. We identified and quantified individual repeats using RepeatExplorer, Tandem Repeat Finder and the Tandem Repeats Analysis Program. We employed Fluorescence In Situ Hybridization (FISH) to analyse chromosome localisation of satellites and transposons. Key Results We identified a number of novel satellites, which have, in a fashion similar to previously known satellites, significantly expanded on the Y chromosome but not as much on the X nor on autosomes. Additionally, the size increase of Y chromosomes is caused by non-LTR and LTR retrotransposons, while only the latter ones contribute to the enlargement of the X chromosome. However, the X chromosome is populated by different LTR retrotransposon lineages than Y chromosomes. Conclusions The X and Y chromosomes significantly diverged in terms of repeat composition. The lack of recombination probably contributed to the expansion of diverse satellites and microsatellites and faster fixation of newly inserted transposable elements (TEs) on the Y chromosomes. In addition, X and Y chromosomes, despite similar total counts of TEs, significantly differ in the representation of individual TE lineages, which indicates that transposons proliferate preferentially either in the paternal or maternal lineage.

Chromosome‐scale assembly of the genome of Salixdunnii reveals a male‐heterogametic sex determination system on chromosome 7

“…In diploid organisms, only the Y chromosomes are predicted to degenerate, because X chromosomes recombine in the XX females (reviewed in Charlesworth, 2015 ). However, X‐ as well as Y‐linked regions are expected to accumulate repetitive sequences to a greater extent than nonsex‐linked genome regions, due to their somewhat lower effective population size, and this has been detected in papaya and common sorrel (Jesionek et al, 2020 ; Wang, Na, et al, 2012 ). The S. dunnii X‐LR appears to have done the same, being rich in LTR‐Gypsy elements (Table 3 ; Figures 1a and 3a ).…”

“…The expected accumulation has been detected in both Y‐ and W‐linked regions of several plants with heteromorphic sex chromosome pairs (reviewed by Hobza et al, 2015 ). Repeat accumulation is also expected in X‐ and Z‐linked regions; although this is expected to occur to a much smaller extent, it has been detected in Carica papaya and Rumex acetosa (Gschwend et al, 2012 ; Jesionek et al, 2020 ; Wang, Na, et al, 2012 ). The accumulation of repeats reduces gene densities, compared with autosomal or pseudoautosomal regions (PARs), and this has been observed in Silene latifolia , again affecting both sex chromosomes (Blavet et al, 2015 ).…”

The contributions of Dr. Nettie Stevens to the field of sex chromosome biology

“…Although, plant sex chromosomes are not without consequences from suppressed recombination. A consistent pattern found is an enrichment of transposable elements (TEs) and other repeats [65,[76][77][78], which often accumulate in regions of low recombination [79]. In fact, in several species TE expansions have instead driven the Y chromosome to be larger than the X, such as in Coccinia grandis [80] and S. latifolia [81].…”

The Czech Plant Nucleus Workshop 2021

“…In many species, dioecy has evolved recently, so these plants provide an excellent model for studying the early stages of sex chromosome divergence, which later in evolution leads to gradual sex chromosome degeneration (Hobza et al 2018). Z. Kubát (IBP) showed that some TEs proliferate preferentially either in the male or in the female germline which can be connected with specific circumstances affecting TE management and activity in male and female plants and during gametophyte formation (Jesionek et al 2021). The process of evolutionary diversification of sex chromosomes is also connected with specific chromatin modifications of both histones and cytosines in Silene latifolia as demonstrated by M. Hubinský (IBP) (Rodríguez Lorenzo et al 2020).…”