Repeated Whole-Genome Duplication, Karyotype Reshuffling, and Biased Retention of Stress-Responding Genes in Buckler Mustard

Abstract

Whole-genome duplication (WGD) is usually followed by gene loss and karyotype repatterning. Despite evidence of new adaptive traits associated with WGD, the underpinnings and evolutionary significance of such genome fractionation remain elusive. Here, we use Buckler mustard (Biscutella laevigata) to infer processes that have driven the retention of duplicated genes after recurrent WGDs. In addition to the b-and a-WGD events shared by all Brassicaceae, cytogenetic and transcriptome analyses revealed two younger WGD events that occurred at times of environmental changes in the clade of Buckler mustard (Biscutelleae): a mesopolyploidy event from the late Miocene that was followed by considerable karyotype reshuffling and chromosome number reduction and a neopolyploidy event during the Pleistocene. Although a considerable number of the older duplicates presented signatures of retention under positive selection, the majority of retained duplicates arising from the younger mesopolyploidy WGD event matched predictions of the gene balance hypothesis and showed evidence of strong purifying selection as well as enrichment in gene categories responding to abiotic stressors. Retention of large stretches of chromosomes for both genomic copies supported the hypothesis that cycles of WGD and biased fractionation shaped the genome of this stress-tolerant polypolyloid, promoting the adaptive recruitment of stress-responding genes in the face of environmental challenges.

Hybridization‐facilitated genome merger and repeated chromosome fusion after 8 million years

“…2.6 million years). Whereas the ancPCK genome was identified as an ancestral genome of Biscutella (Geiser et al ., ), Ricotia (this study) and most likely the other three Biscutelleae genera, the PCK genome is specific for the bona fide monophyletic (expanded) lineage II/clade B (Mandáková and Lysak, ). Historically, the co‐occurrence and hybridization between ancPCK‐ and PCK‐like genomes is fully compatible with the past as well as extant presence of four ( Biscutella , Heldreichia , Lunaria and Ricotia ) of the five Biscutelleae genera (Özüdoğru et al ., ) in the Western Irano‐Turanian region and eastern Mediterranean, together with numerous (expanded) lineage‐II tribes.…”

“…This points to a tetraploid origin of Ricotia . In all species analyzed, homeologous GBs slightly differed in physical length (Figure S3); however, the differences were subtle as compared with other mesopolyploid Brassicaceae species with a higher degree of diploidization (Mandáková et al ., 2010a, ,b; Geiser et al ., ). This is most likely reflecting a slow rate of post‐polyploid diploidization, including biased subgenome fractionation.…”

“…In R. aucheri ( n = 14; Figure ), eight chromosomes structurally resembled the ancestral chromosomes of ACK (two homeologs of AK1, AK2 and AK4, and one homeolog of AK3 and AK7), two chromosomes had the structure of the AK6/8 chromosome with GB association O + P + Wb + R, as in the ancPCK and PCK genomes (Mandáková and Lysak, ; Geiser et al ., ), and the remaining four chromosomes originated by R. aucheri ‐specific CRs among five ancestral chromosomes: AK3, AK5, AK7, AK8/6 and AK5/8/6.…”

“…Karyotypes of two species from the Tenuifolia clade ( R. isatoides and R. tenuifolia , both n = 14; Figure ) shared nine chromosomes with the ACK genome (two homeologs of AK1, AK3 and AK4, and one homeolog of AK2, AK5 and AK7), two homeologs of ancPCK and PCK‐like chromosome AK6/8, one ancPCK‐specific chromosome AK8/6 (with GB association V + Wa + Q + X; Geiser et al ., ), and one PCK‐specific chromosome AK5/8/6 (with GB association M – N + V + K – L + Wa + Q + X; Mandáková and Lysak, ). One Tenuifolia‐specific chromosome (AK2/7) was formed by a nested chromosome insertion (NCI) involving ‘insertion’ AK2 and ‘recipient’ AK7 chromosomes, respectively.…”

“…Comparison of Ricotia and Biscutella genomes (Geiser et al ., ) offers some parallels, but at the same time tells different stories. Both Biscutelleae genera have evolved from different tetraploid progenitor genomes, with n = 15 ( Ricotia ) and n = 16 ( Biscutella ).…”