Abstract
Key message
Karyotypes evolve through numerical and structural chromosome rearrangements. We show that Phaseolus leptostachyus, a wild bean, underwent a rapid genome reshuffling associated with the reduction from 11 to 10 chromosome pairs, but without whole genome duplication, the highest chromosome evolution rate known for plants.
Abstract
Plant karyotypes evolve through structural rearrangements often associated with polyploidy or dysploidy. The genus Phaseolus comprises ~ 90 species, five of them domesticated due to their nutritional relevance. Most of the species have 2n = 22 karyotypes and are highly syntenic, except for three dysploid karyotypes of species from the Leptostachyus group (2n = 20) that have accumulated several rearrangements. Here, we investigated the degrees of structural rearrangements among Leptostachyus and other Phaseolus groups by estimating their chromosomal evolution rates (CER). For this, we combined our oligo-FISH barcode system for beans and chromosome-specific painting probes for chromosomes 2 and 3, with rDNA and a centromeric probe to establish chromosome orthologies and identify structural rearrangements across nine Phaseolus species. We also integrated the detected rearrangements with a phylogenomic approach to estimate the CERs for each Phaseolus lineage. Our data allowed us to identify translocations, inversions, duplications and deletions, mostly in species belonging to the Leptostachyus group. Phaseolus leptostachyus showed the highest CER (12.31 rearrangements/My), a tenfold increase in contrast to the 2n = 22 species analysed. This is the highest rate known yet for plants, making it a model species for investigating the mechanisms behind rapid genome reshuffling in early species diversification.
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Acknowledgements
We would like to kindly thank the CIAT, EMBRAPA Cenargen and IPK for providing the seeds, as well as Fernanda de Oliveira Bustamante, Lívia do Vale Martins, Guilherme Tomaz Braz, Jiming Jiang, and Ana Christina Brasileiro-Vidal for the development of oligo-FISH probes.
Funding
This study was supported by CNPq (National Council for Scientific and Technological Development, acronym in Portuguese, Grant no. 310804/2017–5) and CAPES (Coordination of Improvement of Higher Education Personnel, acronym in Portuguese, Financial Code 001).
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T.N. conducted experiments, analyzsd the data, constructed the figures, and wrote the paper. A.P.H. conceived this research, provided the resources, discussed the results, and helped writing the paper. Both authors read and approved the final version of this text.
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122_2023_4462_MOESM1_ESM.pdf
Supplementary figure S1 Distribution of structural rearrangements among Phaseolus species over evolutionary time. (PDF 882 kb)
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Supplementary figure S4 Phylogenetic tree based on concatenated ITS loci and chloroplast genomes; the negative numbers on the nodes correspond to the ages of each clade in millions of years ago. (PDF 80 kb)
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Supplementary Table S1 Accession codes for the sequencing data deposited in the GenBank used for phylogenetic analyses. (PDF 4 kb)
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Nascimento, T., Pedrosa-Harand, A. High rates of structural rearrangements have shaped the chromosome evolution in dysploid Phaseolus beans. Theor Appl Genet 136, 215 (2023). https://doi.org/10.1007/s00122-023-04462-3
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DOI: https://doi.org/10.1007/s00122-023-04462-3