New estimates and synthesis of chromosome numbers, ploidy levels and genome size variation in Allium sect. Codonoprasum: advancing our understanding of the unresolved diversification and evolution of this section

Abstract

Background: The genus Allium is known for its high chromosomal variability, but most chromosome counts are based on a few individuals and genome size (GS) reports are limited in certain taxonomic groups. This is evident in the Allium sect. Codonoprasum, a species-rich (> 150 species) and taxonomically complex section with weak morphological differences between taxa, the presence of polyploidy and frequent misidentification of taxa. Consequently, a significant proportion of older karyological reports may be unreliable and GS data are lacking for the majority of species within the section. This study, using chromosome counting and flow cytometry (FCM), provides the first comprehensive and detailed insight into variation in chromosome number, polyploid frequency and distribution, and GS in section members, marking a step towards understanding the unresolved diversification and evolution of this group.

Results: We analysed 1578 individuals from 316 populations of 25 taxa and reported DNA ploidy levels and their GS, with calibration from chromosome counts in 22 taxa. Five taxa had multiple ploidy levels. First estimates of GS were obtained for 16 taxa. A comprehensive review of chromosome number and DNA-ploidy levels in 129 taxa of the section revealed that all taxa have x = 8, except A. rupestre with two polyploid series (x = 8, descending dysploidy x = 7), unique for this section. Diploid taxa dominated (72.1%), while di- & polyploid (12.4%) and exclusively polyploid (15.5%) taxa were less common. Ploidy diversity showed that diploid taxa dominated in the eastern Mediterranean and decreased towards the west and north, whereas only polyploid cytotypes of di- & polyploid taxa or exclusively polyploid taxa dominated in northern and northwestern Europe. A 4.1-fold variation in GS was observed across 33 taxa analysed so far (2C = 22.3-92.1 pg), mainly due to polyploidy, with GS downsizing observed in taxa with multiple ploidy levels. Intra-sectional GS variation suggests evolutionary relationships, and intraspecific GS variation within some taxa may indicate taxonomic heterogeneity and/or historical migration patterns.

Conclusions: Our study showed advantages of FCM as an effective tool for detecting ploidy levels and determining GS within the section. GS could be an additional character in understanding evolution and phylogenetic relationships within the section.

Keywords: Chromosome number; Cytogeography; DNA ploidy level; Flow cytometry; Genome size; Polyploidy.

Fig. 1

Distribution of ploidy levels of some taxa of Allium sect. Codonoprasum, based on new and published records [publ. CHN]. A A. carinatum subsp. carinatum, B A. carinatum subsp. pulchellum, C A. dentiferum [DEN] and A. longispathum sensu Jauzein and Tison (2001) [LON], D A. pallens [PAL] and group of populations assigned to the informal group “A. dentiferum-pallens” [DEN-PAL], E A. flavum subsp. flavum, F A. flavum subsp. tauricum. Circles represent new records based on either chromosome number counts or FCM (Table S1), diamonds represent previously published records [publ. CHN]. Mixed-ploidy populations are indicated by ‘+’ between co-occurring ploidies. The approximate range of each taxon (except A. longispathum and “A. dentiferum-pallens”), based on various sources, is shown in light yellow within the respective map

Fig. 2

Relationships between relative genome size (RGS) and geography (longitude, latitude) for measured accessions of A A. carinatum subsp. carinatum, B A. carinatum subsp. pulchellum, C A. dentiferum, D A. pallens, E A. flavum subsp. flavum, F A. flavum subsp. tauricum. Each ploidy level is shown separately within the plots. Each point represents the mean RGS of the respective population (see Table S1)

Fig. 3

Ploidy level composition of taxa of Allium sect. Codonoprasum. Frequency (both absolute and relative) of ploidy categories (di-; di- & polyploid; polyploid) with A all revised taxa with at least one chromosome count and B with 13 taxa excluded based on Özhatay and Koçyiğit (2019). C Ploidy level composition of the respective di-&polyploid and polyploid taxa, both with (all, n = 37 taxa) and without accounting for some taxa excluded (ex, n = 36 taxa) based on Özhatay and Koçyiğit (2019). D Frequency distribution of diploid, di- & polyploid, and exclusively polyploid taxa (for colours see (A)) in the respective regions (from east to west: Caucasus without RUS; Near East without TUR; TUR; CYP; UKR + RUS + BLR; BGR + ROU; GRC incl. Aegean islands; Former YUG; ITA; Central Europe; Northern Europe; North Africa; FRA; GBR + IRL; ESP + PRT). For details see Tables S1, S2, S4, S5

Fig. 4

Genome size of taxa in the Allium sect. Codonoprasum. All available data on GS (population means) meeting the strict criteria (see M&M) were used for the analyses. A Absolute genome size (AGS, 2C values, pg). In the inset, variation in AGS (2C values) within the whole genus Allium (data from Leitch et al. 2019) and A. sect. Codonoprasum (Tables S1, S3) are compared. B Monoploid genome size (1Cx values, pg). Taxa are ordered along the x-axis from left to the right according to an increasing median of 2C values of the lowermost ploidy. Where multiple population measurements are available for a given taxon, a boxplot of GS is presented, separately for each ploidy level. The median AGS is represented by a coloured circle. In the case of only one measurement per taxon/ploidy, only the coloured circle representing the measured value is shown