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Admixture of divergent genomes facilitates hybridization across species in the family Brassicaceae.

ABSTRACT: Hybridization and polyploidization are pivotal to plant evolution. Genetic crosses between distantly related species are rare in nature due to reproductive barriers but how such hurdles can be overcome is largely unknown. Here we report the hybrid genome structure of xBrassicoraphanus, a synthetic allotetraploid of Brassica rapa and Raphanus sativus. We performed cytogenetic analysis and de novo genome assembly to examine chromosome behaviors and genome integrity in the hybrid. Transcriptome analysis was conducted to investigate expression of duplicated genes in conjunction with epigenome analysis to address whether genome admixture entails epigenetic reconfiguration. Allotetraploid xBrassicoraphanus retains both parental chromosomes without genome rearrangement. Meiotic synapsis formation and chromosome exchange are avoided between nonhomologous progenitor chromosomes. Reconfiguration of transcription network occurs, and less divergent cis-elements of duplicated genes are associated with convergent expression. Genome-wide DNA methylation asymmetry between progenitors is largely maintained but, notably, B. rapa-originated transposable elements are transcriptionally silenced in xBrassicoraphanus through gain of DNA methylation. Our results demonstrate that hybrid genome stabilization and transcription compatibility necessitate epigenome landscape adjustment and rewiring of cis-trans interactions. Overall, this study suggests that a certain extent of genome divergence facilitates hybridization across species, which may explain the great diversification and expansion of angiosperms during evolution.

SUBMITTER: Shin H

PROVIDER: S-EPMC9320894 | biostudies-literature | 2022 Jul

REPOSITORIES: biostudies-literature

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Admixture of divergent genomes facilitates hybridization across species in the family Brassicaceae.

Shin Hosub H Park Jeong Eun JE Park Hye Rang HR Choi Woo Lee WL Yu Seung Hwa SH Koh Wonjun W Kim Seungill S Soh Hye Yeon HY Waminal Nomar Espinosa NE Belandres Hadassah Roa HR Lim Joo Young JY Yi Gibum G Ahn Jong Hwa JH Kim June-Sik JS Kim Yong-Min YM Koo Namjin N Kim Kyunghee K Perumal Sampath S Kang Taegu T Kim Junghyo J Jang Hosung H Kang Dong Hyun DH Kim Ye Seul YS Jeong Hyeon-Min HM Yang Junwoo J Song Somin S Park Suhyoung S Kim Jin A JA Lim Yong Pyo YP Park Beom-Seok BS Hsieh Tzung-Fu TF Yang Tae-Jin TJ Choi Doil D Kim Hyun Hee HH Lee Soo-Seong SS Huh Jin Hoe JH

The New phytologist 20220428 2

Hybridization and polyploidization are pivotal to plant evolution. Genetic crosses between distantly related species are rare in nature due to reproductive barriers but how such hurdles can be overcome is largely unknown. Here we report the hybrid genome structure of xBrassicoraphanus, a synthetic allotetraploid of Brassica rapa and Raphanus sativus. We performed cytogenetic analysis and de novo genome assembly to examine chromosome behaviors and genome integrity in the hybrid. Transcriptome ana ...[more]

PMID: 35403705

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Project description:Background and aimsHybridization is a common and important force in plant evolution. One of its outcomes is introgression - the transfer of small genomic regions from one taxon to another by hybridization and repeated backcrossing. This process is believed to be common in glacial refugia, where range expansions and contractions can lead to cycles of sympatry and isolation, creating conditions for extensive hybridization and introgression. Polyploidization is another genome-wide process with a major influence on plant evolution. Both hybridization and polyploidization can have complex effects on plant evolution. However, these effects are often difficult to understand in recently evolved species complexes.MethodsWe combined flow cytometry, analyses of transcriptomic sequences and pollen tube growth assays to investigate the consequences of polyploidization, hybridization and introgression on the recent evolution of several Erysimum (Brassicaceae) species from the South of the Iberian Peninsula, a well-known glacial refugium. This species complex differentiated in the last 2 million years, and its evolution has been hypothesized to be determined mainly by polyploidization, interspecific hybridization and introgression.Key resultsOur results support a scenario of widespread hybridization involving both extant and 'ghost' taxa. Several taxa studied here, most notably those with purple corollas, are polyploids, probably of allopolyploid origin. Moreover, hybridization in this group might be an ongoing phenomenon, as pre-zygotic barriers appeared weak in many cases.ConclusionsThe evolution of Erysimum spp. has been determined by hybridization to a large extent. Species with purple (polyploids) and yellow flowers (mostly diploid) exhibit a strong signature of introgression in their genomes, indicating that hybridization occurred regardless of colour and across ploidy levels. Although the adaptive value of such genomic exchanges remains unclear, our results demonstrate the significance of hybridization for plant diversification, which should be taken into account when studying plant evolution.

Dataset Information

Admixture of divergent genomes facilitates hybridization across species in the family Brassicaceae.

Publications

Admixture of divergent genomes facilitates hybridization across species in the family Brassicaceae.

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