Chromosome fusions shaped karyotype evolution and evolutionary relationships in the model family Brassicaceae

. 2025 May 19 ; 16 (1) : 4631. [epub] 20250519

Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid40389407
Odkazy

PubMed 40389407
PubMed Central PMC12089291
DOI 10.1038/s41467-025-59640-2
PII: 10.1038/s41467-025-59640-2
Knihovny.cz E-zdroje

The ancestral crucifer karyotype and 22 conserved genomic blocks (CGBs) facilitate phylogenomic analyses in the Brassicaceae. Chromosomal rearrangements reshuffled CGBs of ancestral chromosomes during karyotype evolution. Here, we identify eight protochromosomes representing the common ancestral karyotype (ACBK) of the two Brassicoideae supertribes: Camelinodae (Lineage I) and Brassicodae (Lineage II). The characterization of multiple cascading fusion events allows us to infer evolutionary relationships based on these events. In the Camelinodae, the ACBK first evolved into the AKI genome, which remained conserved in the Cardamineae, whereas it was altered to tAKI by a reciprocal translocation that preceded the diversification of most Camelinodae tribes. The identified fusion breakpoints largely overlap with CGB boundaries, suggesting that CGBs are mainly disrupted by chromosome fusions. Our results demonstrate the stable inheritance of chromosome fusions and their importance for reconstructing evolutionary relationships. The chromosomal breakpoint approach provides a basis for ancestral state reconstruction based on chromosome-level genome assemblies.

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Al-Shehbaz, I. A. A. generic and tribal synopsis of the Brassicaceae (Cruciferae). Taxon61, 931–954 (2012).

Walden, N., Nguyen, T. P., Mandáková, T., Lysak, M. A. & Schranz, M. E. Genomic blocks in Aethionema arabicum support arabideae as next diverging clade in Brassicaceae. Front. Plant Sci.11, 719 (2020). PubMed PMC

Hendriks, K. P. et al. Global Brassicaceae phylogeny based on filtering of 1,000-gene dataset. Curr. Biol.33, 4052–4068 (2023). PubMed

Schranz, M. E., Lysak, M. A. & Mitchell-Olds, T. The ABC’s of comparative genomics in the Brassicaceae: building blocks of crucifer genomes. Trends Plant Sci.11, 535–542 (2006). PubMed

Lysak, M. A., Mandáková, T. & Schranz, M. E. Comparative paleogenomics of crucifers: ancestral genomic blocks revisited. Curr. Opin. Plant Biol.30, 108–115 (2016). PubMed

German, D. A. et al. An updated classification of the Brassicaceae (Cruciferae). PhytoKeys220, 127–144 (2023). PubMed PMC

Mandáková, T. & Lysak, M. A. Chromosomal phylogeny and karyotype evolution in x=7 crucifer species (Brassicaceae). Plant Cell20, 2559–2570 (2008). PubMed PMC

Peruzzi, L. x” is not a bias, but a number with real biological significance. Plant Biosyst.147, 1238–1241 (2013).

Schranz, M. E., Windsor, A. J., Song, B. H., Lawton-Rauh, A. & Mitchell-Olds, T. Comparative genetic mapping in Boechera stricta, a close relative of Arabidopsis. Plant Physiol.144, 286–298 (2007). PubMed PMC

Mandáková, T. et al. Fast diploidization in close mesopolyploid relatives of Arabidopsis. Plant Cell22, 2277–2290 (2010). PubMed PMC

Burrell, A. M. et al. A comparative genomic map for Caulanthus amplexicaulis and related species (Brassicaceae). Mol. Ecol.20, 784–798 (2011). PubMed

Wu, H. et al. Insights into salt tolerance from the genome of Thellungiella salsuginea. Proc. Natl. Acad. Sci. USA109, 12219–12224 (2012). PubMed PMC

Slotte, T. et al. The Capsella rubella genome and the genomic consequences of rapid mating system evolution. Nat. Genet.45, 831–835 (2013). PubMed

Mandáková, T. et al. The more the merrier: recent hybridization and polyploidy in Cardamine. Plant Cell25, 3280–3295 (2013). PubMed PMC

Hay, A. et al. Cardamine hirsuta: a versatile genetic system for comparative studies. Plant J.78, 1–15 (2014). PubMed

Kagale, S. et al. The emerging biofuel crop Camelina sativa retains a highly undifferentiated hexaploid genome structure. Nat. Commun.5, 3706 (2014). PubMed PMC

Parkin, I. A. et al. Transcriptome and methylome profiling reveals relics of genome dominance in the mesopolyploid Brassica oleracea. Genome Biol.15, R77 (2014). PubMed PMC

Mandáková, T., Singh, V., Krämer, U. & Lysak, M. A. Genome structure of the heavy metal hyperaccumulator Noccaea caerulescens and its stability on metalliferous and nonmetalliferous soils. Plant Physiol.169, 674–689 (2015). PubMed PMC

Guo, X. et al. Linked by ancestral bonds: multiple whole-genome duplications and reticulate evolution in a Brassicaceae tribe. Mol. Biol. Evol.38, 1695–1714 (2021). PubMed PMC

Yang, W. et al. The chromosome-level genome sequence and karyotypic evolution of Megadenia pygmaea (Brassicaceae). Mol. Ecol. Resour.21, 871–879 (2021). PubMed

Huang, Y. et al. The meso-octoploid Heliophila variabilis genome sheds a new light on the impact of polyploidization and diploidization on the diversity of the Cape flora. Plant J.116, 446–466 (2023). PubMed

Liu, J. et al. Genomes of Meniocus linifolius and Tetracme quadricornis unveil the ancestral karyotype and genomic features of core Brassicaceae. Plant Commun.5, 100878 (2024). PubMed PMC

Schubert, I. & Lysak, M. A. Interpretation of karyotype evolution should consider chromosome structural constraints. Trends Genet.27, 207–216 (2011). PubMed

Mayrose, I. & Lysak, M. A. The evolution of chromosome numbers: mechanistic models and experimental approaches. Genome Biol. Evol.13, evaa220 (2021). PubMed PMC

Sun, P. et al. WGDI: a user-friendly toolkit for evolutionary analyses of whole-genome duplications and ancestral karyotypes. Mol. Plant15, 1841–1851 (2022). PubMed

Sun, P. et al. Subgenome-aware analyses reveal the genomic consequences of ancient allopolyploid hybridizations throughout the cotton family. Proc. Natl. Acad. Sci. USA121, e2313921121 (2024). PubMed PMC

Lysak, M. A. Celebrating Mendel, McClintock, and Darlington: on end-to-end chromosome fusions and nested chromosome fusions. Plant Cell34, 2475–2491 (2022). PubMed PMC

Lysak, M. A. et al. Mechanisms of chromosome number reduction in Arabidopsis thaliana and related Brassicaceae species. Proc. Natl. Acad. Sci. USA103, 5224–5229 (2006). PubMed PMC

Mandáková, T., Marhold, K. & Lysak, M. A. The widespread crucifer species Cardamine flexuosa is an allotetraploid with a conserved subgenomic structure. New Phytol.201, 982–992 (2014). PubMed

Kamm, A., Galasso, I., Schmidt, T. & Heslop-Harrison, J. S. Analysis of a repetitive DNA family from Arabidopsis arenosa and relationships between Arabidopsis species. Plant Mol. Biol.27, 853–862 (1995). PubMed

Comai, L., Tyagi, A. P. & Lysak, M. A. FISH analysis of meiosis in Arabidopsis allopolyploids. Chromosome Res.11, 217–226 (2003). PubMed

Jakobsson, M. et al. A unique recent origin of the allotetraploid species Arabidopsis suecica: evidence from nuclear DNA markers. Mol. Biol. Evol.23, 1217–1231 (2006). PubMed

Novikova, P. Y. et al. Genome sequencing reveals the origin of the allotetraploid Arabidopsis suecica. Mol. Biol. Evol.34, 957–968 (2017). PubMed PMC

Mandáková, T., Pouch, M., Brock, J. R., Al-Shehbaz, I. A. & Lysak, M. A. Origin and evolution of diploid and allopolyploid Camelina genomes were accompanied by chromosome shattering. Plant Cell31, 2596–2612 (2019). PubMed PMC

Zhang, Z. et al. An updated explanation of ancestral karyotype changes and reconstruction of evolutionary trajectories to form Camelina sativa chromosomes. BMC Genom.21, 705 (2020). PubMed PMC

Burns, R. et al. Gradual evolution of allopolyploidy in Arabidopsis suecica. Nat. Ecol. Evol.5, 1367–1381 (2021). PubMed PMC

Mandáková, T. & Lysak, M. A. The identification of the missing maternal genome of the allohexaploid camelina (Camelina sativa). Plant J.112, 622–629 (2022). PubMed

Martin, S. L., Toro, B. L., James, T., Sauder, C. A. & Laforest, M. Insights from the genomes of 4 diploid Camelina spp.G3-Genes Genom. Genet.12, jkac182 (2022). PubMed PMC

Chaudhary, R. et al. Sequencing of Camelina neglecta, a diploid progenitor of the hexaploid oilseed Camelina sativa. Plant Biotechnol. J.21, 521–535 (2023). PubMed PMC

Murat, F. et al. Reconstructing the genome of the most recent common ancestor of flowering plants. Nat. Genet.49, 490–496 (2017). PubMed

Aköz, G. & Nordborg, M. The Aquilegia genome reveals a hybrid origin of core eudicots. Genome Biol.20, 1–12 (2019). PubMed PMC

Shi, T. et al. The slow-evolving Acorus tatarinowii genome sheds light on ancestral monocot evolution. Nat. Plants8, 764–777 (2022). PubMed PMC

Ma, L. et al. Diploid and tetraploid genomes of Acorus and the evolution of monocots. Nat. Commun.14, 3661 (2023). PubMed PMC

Wang, Z. et al. A high-quality Buxus austro-yunnanensis (Buxales) genome provides new insights into karyotype evolution in early eudicots. BMC Biol.20, 216–232 (2022). PubMed PMC

Xu, X., Sun, P., Gao, C., Zheng, W. & Chen, S. Assembly of the poorly differentiated Verasper variegatus W chromosome by different sequencing technologies. Sci. Data10, 893 (2023). PubMed PMC

Carta, A., Bedini, G. & Peruzzi, L. A deep dive into the ancestral chromosome number and genome size of flowering plants. New Phytol.228, 1097–1106 (2020). PubMed

Yin, Y. et al. Molecular mechanisms and topological consequences of drastic chromosomal rearrangements of muntjac deer. Nat. Commun.12, 6858 (2021). PubMed PMC

Shao, Y. et al. Phylogenomic analyses provide insights into primate evolution. Science380, 913–924 (2023). PubMed

Zhang, C. & Mirarab, S. ASTRAL-Pro 2: ultrafast species tree reconstruction from multi-copy gene family trees. Bioinformatics38, 4949–4950 (2022). PubMed

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