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The story of promiscuous crucifers: origin and genome evolution of an invasive species, Cardamine occulta (Brassicaceae), and its relatives.

ABSTRACT: BACKGROUND AND AIMS:Cardamine occulta (Brassicaceae) is an octoploid weedy species (2n = 8x = 64) originated in Eastern Asia. It has been introduced to other continents including Europe and considered to be an invasive species. Despite its wide distribution, the polyploid origin of C. occulta remained unexplored. The feasibility of comparative chromosome painting (CCP) in crucifers allowed us to elucidate the origin and genome evolution in Cardamine species. We aimed to investigate the genome structure of C. occulta in comparison with its tetraploid (2n = 4x = 32, C. kokaiensis and C. scutata) and octoploid (2n = 8x = 64, C. dentipetala) relatives. METHODS:Genomic in situ hybridization (GISH) and large-scale CCP were applied to uncover the parental genomes and chromosome composition of the investigated Cardamine species. KEY RESULTS:All investigated species descended from a common ancestral Cardamine genome (n = 8), structurally resembling the Ancestral Crucifer Karyotype (n = 8), but differentiated by a translocation between chromosomes AK6 and AK8. Allotetraploid C. scutata originated by hybridization between two diploid species, C. parviflora and C. amara (2n = 2x = 16). By contrast, C. kokaiensis has an autotetraploid origin from a parental genome related to C. parviflora. Interestingly, octoploid C. occulta probably originated through hybridization between the tetraploids C. scutata and C. kokaiensis. The octoploid genome of C. dentipetala probably originated from C. scutata via autopolyploidization. Except for five species-specific centromere repositionings and one pericentric inversion post-dating the polyploidization events, the parental subgenomes remained stable in the tetra- and octoploids. CONCLUSIONS:Comparative genome structure, origin and evolutionary history was reconstructed in C. occulta and related species. For the first time, whole-genome cytogenomic maps were established for octoploid plants. Post-polyploid evolution in Asian Cardamine polyploids has not been associated with descending dysploidy and intergenomic rearrangements. The combination of different parental (sub)genomes adapted to distinct habitats provides an evolutionary advantage to newly formed polyploids by occupying new ecological niches.

SUBMITTER: Mandakova T

PROVIDER: S-EPMC6758578 | biostudies-literature | 2019 Sep

REPOSITORIES: biostudies-literature

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The story of promiscuous crucifers: origin and genome evolution of an invasive species, Cardamine occulta (Brassicaceae), and its relatives.

Mandáková Terezie T Zozomová-Lihová Judita J Kudoh Hiroshi H Zhao Yunpeng Y Lysak Martin A MA Marhold Karol K

Annals of botany 20190901 2

<h4>Background and aims</h4>Cardamine occulta (Brassicaceae) is an octoploid weedy species (2n = 8x = 64) originated in Eastern Asia. It has been introduced to other continents including Europe and considered to be an invasive species. Despite its wide distribution, the polyploid origin of C. occulta remained unexplored. The feasibility of comparative chromosome painting (CCP) in crucifers allowed us to elucidate the origin and genome evolution in Cardamine species. We aimed to investigate the g ...[more]

PMID: 30868165

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Project description:Background and aimsRecently formed allopolyploid species represent excellent subjects for exploring early stages of polyploid evolution. The hexaploid Cardamine schulzii was regarded as one of the few nascent allopolyploid species formed within the past ?150 years that presumably arose by autopolyploidization of a triploid hybrid, C. × insueta; however, the most recent investigations have shown that it is a trigenomic hybrid. The aims of this study were to explore the efficiency of progenitor-specific microsatellite markers in detecting the hybrid origins and genome composition of these two allopolyploids, to estimate the frequency of polyploid formation events, and to outline their evolutionary potential for long-term persistence and speciation.MethodsFlow-cytometric ploidy-level screening and genotyping by progenitor-specific microsatellite markers (20 microsatellite loci) were carried out on samples focused on hybridizing populations at Urnerboden, Switzerland, but also including comparative material of the parental species from other sites in the Alps and more distant areas.Key resultsIt was confirmed that hybridization between the diploids C. amara and C. rivularis auct. gave rise to triploid C. × insueta, and it is inferred that this has occurred repeatedly. Evidence is provided that C. schulzii comprises three parental genomes and supports its origin from hybridization events between C. × insueta and the locally co-occurring hypotetraploid C. pratensis, leading to two cytotypes of C. schulzii: hypopentaploid and hypohexaploid. Each cytotype of C. schulzii is genetically uniform, suggesting their single origins.ConclusionsPersistence of C. schulzii has presumably been achieved only by perennial growth and clonal reproduction. This contrasts with C. × insueta, in which multiple origins and occasional sexual reproduction have generated sufficient genetic variation for long-term survival and evolutionary success. This study illustrates a complex case of recurrent hybridization and polyploidization events, and highlights the role of triploids that promoted the origin of trigenomic hybrids.

Project description:BackgroundIn plants, expression of ARGONAUTE1 (AGO1), the catalytic subunit of the RNA-Induced Silencing Complex responsible for post-transcriptional gene silencing, is controlled through a feedback loop involving the miR168 microRNA. This complex auto-regulatory loop, composed of miR168-guided AGO1-catalyzed cleavage of AGO1 mRNA and AGO1-mediated stabilization of miR168, was shown to ensure the maintenance of AGO1 homeostasis that is pivotal for the correct functioning of the miRNA pathway.ResultsWe applied different approaches to studying the genomic organization and the structural and functional evolution of MIR168 homologs in Brassicaeae. A whole genome comparison of Arabidopsis and poplar, phylogenetic footprinting and phylogenetic reconstruction were used to date the duplication events originating MIR168 homologs in these genomes. While orthology was lacking between Arabidopsis and poplar MIR168 genes, we successfully isolated orthologs of both loci present in Arabidopsis (MIR168a and MIR168b) from all the Brassicaceae species analyzed, including the basal species Aethionema grandiflora, thus indicating that (1) independent duplication events took place in Arabidopsis and poplar lineages and (2) the origin of MIR168 paralogs predates both the Brassicaceae radiation and the Arabidopsis alpha polyploidization. Different phylogenetic footprints, corresponding to known functionally relevant regions (transcription starting site and double-stranded structures responsible for microRNA biogenesis and function) or for which functions could be proposed, were found to be highly conserved among MIR168 homologs. Comparative predictions of the identified microRNAs also indicate extreme conservation of secondary structure and thermodynamic stability.ConclusionWe used a comparative phylogenetic footprinting approach to identify the structural and functional constraints that shaped MIR168 evolution in Brassicaceae. Although their duplication happened at least 40 million years ago, we found evidence that both MIR168 paralogs have been maintained throughout the evolution of Brassicaceae, most likely functionally as indicated by the extremely high conservation of functionally relevant regions, predicted secondary structure and thermodynamic profile. Interestingly, the expression patterns observed in Arabidopsis indicate that MIR168b underwent partial subfunctionalization as determined by the experimental characterization of its expression pattern provided in this study. We found further evolutionary evidence that pre-miR168 lower stem (the RNA-duplex structure adjacent to the miR-miR* stem) is significantly longer than animal lower stems and probably plays a relevant role in multi-step miR168 biogenesis.

Dataset Information

The story of promiscuous crucifers: origin and genome evolution of an invasive species, Cardamine occulta (Brassicaceae), and its relatives.

Publications

The story of promiscuous crucifers: origin and genome evolution of an invasive species, Cardamine occulta (Brassicaceae), and its relatives.

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