Structural polymorphisms and distinct genomic composition suggest recurrent origin and ongoing evolution of B chromosomes in the Prospero autumnale complex (Hyacinthaceae)

Abstract

Summary Supernumerary B chromosomes (Bs) are genomic parasitic components, originating from the A complement via chromosomal rearrangements, which follow their own evolutionary trajectories. They often contain repetitive DNAs, some shared with regular chromosomes and some newly evolved. Genomic composition, origin and evolution of Bs have been analysed in the chromosomally variable Prospero autumnale complex.Two rDNAs and a satellite DNA (PaB6) from regular chromosomes were mapped to Bs of 26 plants from three diploid cytotypes, their hybrids and polyploid derivatives. In homoploid diploid hybrids, genomic in situ hybridization (GISH) allowed B painting with the parental DNAs.Bs were structurally variable and highly enriched in 5S rDNA and satDNA PaB6, and rarely in 35S rDNA. Eleven combinations of rDNA and PaB6 localization were observed. The quantities of PaB6 in Bs and regular chromosomes were not correlated, suggesting amplification mechanisms other than recombination. PaB6 and 5S rDNA amounts increased with increasing ploidy level. GISH revealed two independent origins of Bs.The structural variation, repeat content, repeat‐type fluctuations and differing genomic affinities of Bs in different cytotypes suggest that they represent young proto‐B chromosomes. Bs in P. autumnale probably form recurrently as by‐products of the extensive genome restructuring within this chromosomally variable species complex.

Multiple Origins and Nested Cycles of Hybridization Result in High Tetraploid Diversity in the Monocot Prospero

“…An excellent system to elucidate genome dynamics and polyploid evolutionary trajectories is provided by the monocot Prospero autumnale (Hyacinthaceae, autumn squill), distributed across the Mediterranean Basin, Europe, and western Asia (Parker et al, 1991 ; Speta, 1993 ). The P. autumnale complex is remarkably variable in chromosome number (dysploidy on diploid level, polyploidy, B-chromosomes: Ainsworth et al, 1983 ; Vaughan et al, 1997 ; Jang et al, 2013 , 2016 ), chromosome structure (fusions, inversions, translocations, centric shifts, supernumerary chromosomal segments: Taylor, 1997 ; Jang et al, 2013 ), genome size (Ebert et al, 1996 ; Vaughan et al, 1997 ; Jang et al, 2013 ) and repetitive DNA distribution and copy number (Emadzade et al, 2014 ). The P. autumnale complex encompasses four diploid cytotypes with unique combinations of basic chromosome number ( x = 7, 6, 5), genome size, locations of pericentric satellite DNA PaB6 and of 5S and 35S rDNA loci (Jang et al, 2013 ; Emadzade et al, 2014 ).…”

Euchromatic Supernumerary Chromosomal Segments—Remnants of Ongoing Karyotype Restructuring in the Prospero autumnale Complex?

“…At least some of these SCSs might be quite old, their origin preceding the diversification of the extant diploid cytotypes. Extensive chromosomal rearrangements in P. autumnale have also been proposed to be the most likely reason for its extraordinary variability (both structural and genomic) and the ongoing origin of B chromosomes [ 24 ]. It is possible that the putative ancestral SCS of chromosome 1 has originated from a B chromosome that translocated to chromosome 1 early in the diversification of the P. autumnale complex.…”

“…GISH has been performed in one diploid hybrid individual B 6 B 7 (H258) and four allopolyploid individuals, two of AAB 7 B 7 (H110–1 & 2) and two of B 6 B 6 B 7 B 7 (H574–1 & 2) composition, using labelled parental diploid genomic DNA as probes [ 24 , 29 ]. Total genomic DNA from diploid cytotypes AA, B 6 B 6 , and B 7 B 7 was isolated using the CTAB (Cetyltrimethylammonium Bromide) method [ 29 ] and sheared at 98 °C for 5 min.…”

“…Hybridisation and polyploidisation of three of these diploid cytotypes (AA, B 6 B 6 , and B 7 B 7 ) have given rise to further polyploid cytotypes, including autopolyploids of genome B 7 ( x = 7) [ 16 , 17 , 18 , 19 , 20 ] and two classes of allopolyploids, of A/B 7 (both x = 7) and of B 6 /B 7 genome composition [ 20 , 21 , 22 , 23 ]. Both B chromosomes (Bs) and SCSs have been reported in the three diploid cytotypes AA, B 6 B 6 , and B 7 B 7 [ 15 ], and in various polyploids [ 6 , 17 , 21 , 24 ]. SCSs in P. autumnale are preferentially located terminally on the short arms of chromosomes 1 and 4 in the A and B 7 genomes and are frequently quite large.…”

Chromosome numbers and polyploidy events in Korean non-commelinids monocots: A contribution to plant systematics

“…The rDNA loci number variation within species or among closely related taxa have often been shown to be correlated with geographic and/or populational factors (e.g., Jang et al, 2016a). Thus, the localization of rDNA loci analyzed in comparative context aids not only the analyses of chromosomal structural changes, but when interpreted in phylogenetic context (e.g., Jang et al, 2013Jang et al, , 2016b, it also allows broader conclusions with implications for taxonomy. Monocot genomes are often more dynamically evolving than those of the dicots.…”