Comparative cytogenomics reveals genome reshuffling and centromere repositioning in the legume tribe Phaseoleae

Abstract

The tribe Phaseoleae (Leguminosae; Papilionoideae) includes several legume crops with assembled genomes. Comparative genomic studies indicate the preservation of large genomic blocks among legumes, however, the chromosome dynamics during Phaseoleae evolution has not been investigated yet. We conducted a comparative genomic analysis to define an informative genomic block (GB) system and to reconstruct the ancestral Phaseoleae karyotype (APK). We defined the GBs based on the orthologous genes between Phaseolus vulgaris and Vigna unguiculata genomes. We searched for these GBs in different genome species belonging to the Phaseolinae (P. lunatus) and Glycininae subtribes (Amphicarpaea edgeworthii and Spatholobus suberectus), and in the Medicago truncaluta outgroup. To support our in silico analysis, we used oligo-FISH probes of P. vulgaris chromosomes 2 and 3 to paint the orthologous chromosomes of two non-sequenced Phaseolinae species (Macroptilium atropurpureum and Lablab purpureus). We inferred the APK with n = 11 and 19 GBs (A to S). We hypothesized five chromosome fusions that reduced the ancestral legume karyotype with n = 16 to n = 11 in APK. Furthermore, we identified the main rearrangements within Phaseolinae and observed an extensive centromere repositioning resulting from evolutionary new centromeres (ENC) in the Phaseolus lineage. Additionally, we demonstrated that the A. edgeworthii genome is more reshuffled than the dysploid S. suberectus genome, in which we could reconstruct the main events that lead the chromosome number reduction. The development of the GB system and the proposed APK provide useful approaches for future comparative genomic analyses of legume species.

Assembly of the 81.6 Mb centromere of pea chromosome 6 elucidates the structure and evolution of metapolycentric chromosomes

“…Insights into the possible mechanisms involved in metapolycentromere formation could be obtained from centromere shifts reported in monocentric chromosomes (see [30] and references therein). These centromere shifts are explained either by chromosomal rearrangements…”

“…Insights into the possible mechanisms involved in metapolycentromere formation could be obtained from centromere shifts reported in monocentric chromosomes (see [ 30 ] and references therein). These centromere shifts are explained either by chromosomal rearrangements such as translocations or inversions or by the repositioning of centromeric chromatin to a new location without disrupting the linear order of chromosomes [ 31 ].…”

Phaseolus vulgaris mutants reveal variation in the nuclear genome

“…Most of the cytogenetic analyses in common bean concern determining chromosome numbers and karyotypic features using fluorescence in situ hybridization (FISH) with repetitive DNA sequences, i.e., 5S and 35S rDNA as probes ( Mercado-Ruaro and Delgado-Salina, 1998 ; Mercado-Ruaro and Delgado-Salina, 2000 ). To date, the development of cytogenetic maps, including the mapping of BAC clones, has been undertaken to investigate the chromosomal structure of common bean and other Phaseolus species with diverse geographical distribution ( Fonseca et al., 2010 ; Iwata-Otsubo et al., 2016 ; Montenegro et al., 2022 ). They allowed for surveying evolutionary and geographical aspects within the genus Phaseolus.…”

Cytogenomic and phylogenomic evidence for new infrageneric relationships in Macroptilium (Benth.) beans

“…Recently, a GB system using comparative genomics was used for reconstructing the ancestral karyotype for Phaseoleae (APK), indicating n = 11 as the ancestral karyotype of the tribe. The main chromosomal rearrangements that shaped the evolution of this tribe involved APK1, 6 and 9, followed by extensive centromere repositioning within the group (Montenegro et al 2022). Additionally, chromosome painting probes for P. vulgaris chromosomes 2 and 3 were hybridized in situ to M. atropurpureum chromosomes, revealing a similar painting pattern to V. unguiculata and the APK orthologous chromosomes (Montenegro et al 2022).…”

“…The main chromosomal rearrangements that shaped the evolution of this tribe involved APK1, 6 and 9, followed by extensive centromere repositioning within the group (Montenegro et al 2022). Additionally, chromosome painting probes for P. vulgaris chromosomes 2 and 3 were hybridized in situ to M. atropurpureum chromosomes, revealing a similar painting pattern to V. unguiculata and the APK orthologous chromosomes (Montenegro et al 2022). Despite the phylogenetic proximity to Phaseolus and Vigna, all belonging to the subtribe Phaseolinae, complete assembled genomes are still lacking in Macroptilium.…”