Monophyletic Origin and Evolution of the Largest Crucifer Genomes

Abstract

Clade E, or the Hesperis clade, is one of the major Brassicaceae (Crucifereae) clades, comprising some 48 genera and 351 species classified into seven tribes and is distributed predominantly across arid and montane regions of Asia. Several taxa have socioeconomic significance, being important ornamental but also weedy and invasive species. From the comparative genomic perspective, the clade is noteworthy as it harbors species with the largest crucifer genomes but low numbers of chromosomes (n = 5-7). By applying comparative cytogenetic analysis and whole-chloroplast phylogenetics, we constructed, to our knowledge, the first partial and complete cytogenetic maps for selected representatives of clade E tribes and investigated their relationships in a family-wide context. The Hesperis clade is a well-supported monophyletic lineage comprising seven tribes: Anchonieae, Buniadeae, Chorisporeae, Dontostemoneae, Euclidieae, Hesperideae, and Shehbazieae. The clade diverged from other Brassicaceae crown-group clades during the Oligocene, followed by subsequent Miocene tribal diversifications in central/southwestern Asia. The inferred ancestral karyotype of clade E (CEK; n = 7) originated from an older n = 8 genome, which also was the purported progenitor of tribe Arabideae (KAA genome). In most taxa of clade E, the seven linkage groups of CEK either remained conserved (Chorisporeae) or were reshuffled by chromosomal translocations (Euclidieae). In 50% of Anchonieae and Hesperideae species, the CEK genome has undergone descending dysploidy toward n = 6 (-5). These genomic data elucidate early genome evolution in Brassicaceae and pave the way for future whole-genome sequencing and assembly efforts in this as yet genomically neglected group of crucifer plants.

Figure 1.

Representatives of the seven tribes of clade E. A, A bouquet of Matthiola incana (ANCH). B, Bunias orientalis (BUNI). C, Euclidium syriacum (EUCL). D, Leiospora exscapa (EUCL). E, Tetracme quadricornis (EUCL). F, Strigosella africana (EUCL). G, Hesperis tristis (HESP). H, Tchihatchewia isatidea (HESP). I, Chorispora bungeana (CHOR). J, Parrya olgae (CHOR). K, Dontostemon elegans (DONT). L, Shehbazia tibetica (SHEH). Photographs are by T. Mandáková (A), K. Schneider (B), P.E. Yevseyenkov (C), I.E. Smelyansky (D), A.L. Ebel (E), S.V. Smirnov (F), L. Hoskovec (G), E. Rencová (H), P.A. Kosachev (I and K), N. Yu Beshko (J), and Q. Lin (L). All photographs are reproduced with the permission of their authors.

Figure 2.

Ideograms of the extant and ancestral genomes of clade E tribes and examples of cytogenetic analyses. A, Genome structure of C. tenella (CHOR). B, Genome structures of E. syriacum and the neotetraploid S. africana (both EUCL). Black arrows refer to the inverted collinearity of block E in relation to the ancestral crucifer karyotype (ACK); red arrows show a EUCL-specific paracentric inversion on chromosome 1; the blue arrow indicates a paracentric inversion differentiating chromosome 3 in E. syriacum and S. africana. C, Identification of genomic blocks A and B (linkage group 1) by comparative chromosome painting analysis on pachytene chromosomes (top three species) and mitotic chromosomes of seven clade E species. D, Ancestral karyotype of clade E (CEK). The color code and capital letters correspond to the eight chromosomes and 22 genomic blocks of ACK, respectively. The black circle marks the position of the 35S rDNA locus. Colors in C correspond to epifluorescence of biotin-, digoxigenin- and Cy3-labeled painting contigs. Chromosomes were counterstained by 4′,6-diamidino-2-phenylindole (DAPI).

Figure 3.

Parsimonious evolutionary scenario of the origin of the CEK (n = 7) and KAA (n = 8) genomes from evolutionarily older n = 8 genome(s). The presumed relationships of these genomes to other inferred ancestral Brassicaceae genomes are outlined.

Figure 4.

Brassicaceae family tree/chronogram showing the phylogenetic positions and divergence times of clade E tribes. A maximum clade credibility tree was produced by BEAST analysis based on whole-chloroplast sequence data of Brassicaceae taxa. Divergence times based on a relaxed clock log normal model are shown, with blue lines representing 95% high posterior density intervals. Classification to lineages and clades follows Franzke et al. (2011) and Huang et al. (2016), respectively.