Diversification times among <i>Brassica</i> (Brassicaceae) crops suggest hybrid formation after 20 million years of divergence

Arias, Tatiana; Beilstein, Mark A.; Tang, Michelle; McKain, Michael R.; Pires, J. Chris

doi:10.3732/ajb.1300312

Cited by 95 publications

(80 citation statements)

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“…Furthermore, the desiccation of the Mediterranean Sea took place around the Miocene-Pliocene boundary, leading into the geologically catastrophic Messinian salinity crisis (Hsu et al, 1977) when further major climatic changes were experienced. The emergence of the core Oleracea lineage (that includes B. rapa and B. oleracea; 4.2 to 9.3 Mya), and diversification of Crambe and Vella (;7 Mya) also coincided with the Messinian salinity crisis (Arias et al, 2014). The dramatically increased aridity and salinity during this period had considerable impact on land vegetation, triggering forest cover decline and radiation of the seasonally adapted taxa (Janis, 1993;Cerling et al, 1997;Fortelius et al, 2006).…”

Section: Discussionmentioning

confidence: 97%

Polyploid Evolution of the Brassicaceae during the Cenozoic Era

et al. 2014

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The Brassicaceae (Cruciferae) family, owing to its remarkable species, genetic, and physiological diversity as well as its significant economic potential, has become a model for polyploidy and evolutionary studies. Utilizing extensive transcriptome pyrosequencing of diverse taxa, we established a resolved phylogeny of a subset of crucifer species. We elucidated the frequency, age, and phylogenetic position of polyploidy and lineage separation events that have marked the evolutionary history of the Brassicaceae. Besides the well-known ancient a (47 million years ago [Mya]) and b (124 Mya) paleopolyploidy events, several species were shown to have undergone a further more recent (;7 to 12 Mya) round of genome multiplication. We identified eight whole-genome duplications corresponding to at least five independent neo/mesopolyploidy events. Although the Brassicaceae family evolved from other eudicots at the beginning of the Cenozoic era of the Earth (60 Mya), major diversification occurred only during the Neogene period (0 to 23 Mya). Remarkably, the widespread species divergence, major polyploidy, and lineage separation events during Brassicaceae evolution are clustered in time around epoch transitions characterized by prolonged unstable climatic conditions. The synchronized diversification of Brassicaceae species suggests that polyploid events may have conferred higher adaptability and increased tolerance toward the drastically changing global environment, thus facilitating species radiation.

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Section: Discussionmentioning

confidence: 97%

Polyploid Evolution of the Brassicaceae during the Cenozoic Era

et al. 2014

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“…Brassica species share an additional common feature in that they all experienced an extra whole genome triplication (WGT) event, which occurred approximately 9-15 million years ago 3,4 or even approximately 28 million years ago. [5][6][7] THE U'S TRIANGLE MODEL DESCRIBES THE RELATIONSHIP AMONG BRASSICA CROPS Six species of the genus Brassica are used widely throughout the world as oilseed, condiments, fodder or vegetable crops. Three of these species are diploid (Brassica rapa, n510; B. nigra, n58; and B. oleracea, n59), whereas the other three are allotetraploids (B. juncea, n518; B. napus, n519; B. carinata, n517) derived from each pair of the three diploid species.…”

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Genome Triplication Drove the Diversification of Brassica Plants

Cheng¹,

Wu²,

Liang³

et al. 2015

Compendium of Plant Genomes

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The genus Brassica belongs to the plant family Brassicaceae, which includes many important crop species that are used as oilseed, condiments, or vegetables throughout the world. Brassica plants comprise many diverse species, and each species contains rich morphotypes showing extreme traits. Brassica species experienced an extra whole genome triplication (WGT) event compared with the model plant Arabidopsis thaliana. Whole genome sequencing of the Brassica species Brassica rapa, Brassica oleracea and others demonstrated that WGT plays an important role in the speciation and morphotype diversification of Brassica plants. Comparative genomic analysis based on the genome sequences of B. rapa and A. thaliana clearly identified the WGT event and further demonstrated that the translocated Proto-Calepine Karyotype (tPCK, n57) was the diploid ancestor of the three subgenomes in B. rapa. Following WGT, subsequent extensive genome fractionation, block reshuffling and chromosome reduction accompanied by paleocentromere descent from the three tPCK subgenomes during the rediploidization process produced stable diploid species. Genomic rearrangement of the diploid species and their hybridization then contributed to Brassica speciation. The subgenome dominance effect and biased gene retention, such as the over-retention of auxin-related genes after WGT, promoted functional gene evolution and thus propelled the expansion of rich morphotypes in the Brassica species. In conclusion, the WGT event initiated subsequent genomic and gene-level evolution, which further drove Brassica speciation and created rich morphotypes in each species. GENUS BRASSICA IN BRASSICACEAE Plants of the genus Brassica are grouped into the tribe Brassiceae, which belongs to the plant family Brassicaceae. Brassicaceae comprises a large family of plants that exhibit common and distinct features in their flowers. The flowers have cruciform petals and six stamens, two of which are short outer stamens. In total, Brassicaceae is composed of 3709 species and 338 genera, 1 with 308 of the 338 genera further assigned to 44 tribes.2 Among the abundant Brassicaceae species, the genus Brassica is important because it contains many economically valuable crops that are used as oilseeds, condiments, and culinary vegetables. Brassica species share an additional common feature in that they all experienced an extra whole genome triplication (WGT) event, which occurred approximately 9-15 million years ago 3,4 or even approximately 28 million years ago. 5-7THE U'S TRIANGLE MODEL DESCRIBES THE RELATIONSHIP AMONG BRASSICA CROPS Six species of the genus Brassica are used widely throughout the world as oilseed, condiments, fodder or vegetable crops. Three of these species are diploid (Brassica rapa, n510; B. nigra, n58; and B. oleracea, n59), whereas the other three are allotetraploids (B. juncea, n518; B. napus, n519; B. carinata, n517) derived from each pair of the three diploid species. The genetic relationships of these species were identified and confirmed by extensive experi...

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“…The only exception was Eutrema salsugineum (accession Shandong), a member of the Brassicaceae family that shares a common ancestor with A. thaliana and Brassica spp. ∼47 and 40 million y ago, respectively (20). Comparisons between the E. salsugineum methylome and those of other plants revealed two major differences.…”

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On the origin and evolutionary consequences of gene body DNA methylation

Bewick

Niederhuth

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

285

418

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In plants, CG DNA methylation is prevalent in the transcribed regions of many constitutively expressed genes (gene body methylation; gbM), but the origin and function of gbM remain unknown. Here we report the discovery that Eutrema salsugineum has lost gbM from its genome, to our knowledge the first instance for an angiosperm. Of all known DNA methyltransferases, only CHROMOMETHYLASE 3 (CMT3) is missing from E. salsugineum. Identification of an additional angiosperm, Conringia planisiliqua, which independently lost CMT3 and gbM, supports that CMT3 is required for the establishment of gbM. Detailed analyses of gene expression, the histone variant H2A.Z, and various histone modifications in E. salsugineum and in Arabidopsis thaliana epigenetic recombinant inbred lines found no evidence in support of any role for gbM in regulating transcription or affecting the composition and modification of chromatin over evolutionary timescales.DNA methylation | gene body methylation | epigenetics | histone modifications | CHROMOMETHYLASE 3 I n angiosperms, cytosine DNA methylation occurs in three sequence contexts: Methylated CG (mCG) is catalyzed by METHYLTRANSFERASE 1 (MET1), mCHG (where H is A/C/T) by CHROMOMETHYLASE 3 (CMT3), and mCHH by DOMAINS REARRANGED METHYLTRANSFERASE 2 (DRM2) or CHROMOMETHYLASE 2 (CMT2) (1). MET1 performs a maintenance function and is targeted by VARIANT IN METHYLATION 1 (VIM1), which binds preexisting hemimethylated CG sites. In contrast, DRM2 is targeted by RNA-directed DNA methylation (RdDM) for the de novo establishment of mCHH. CMT3 forms a self-reinforcing loop with the H3K9me2 pathway to maintain mCHG; however, considering that transformation of CMT3 into the cmt3 background can rescue DNA methylation defects, it is reasonable to also consider CMT3 a de novo methyltransferase (2). Two main lines of evidence suggest that DNA methylation plays an important role in the transcriptional silencing of transposable elements (TEs): that TEs are usually methylated, and that the loss of DNA methylation (e.g., in methyltransferase mutants) is often accompanied by TE reactivation.A large number of plant genes (e.g., ∼13.5% of all Arabidopsis thaliana genes) also contain exclusively mCG in the transcribed region and a depletion of mCG from both the transcriptional start and stop sites (referred to as "gene body DNA methylation"; gbM) ( Fig. 1A) (3)(4)(5). A survey of plant methylome data showed that the emergence of gbM in the plant kingdom is specific to angiosperms (6), whereas nonflowering plants (such as mosses and green algae) have much more diverse genic methylation patterns (7,8). Similar to mCG at TEs, the maintenance of gbM requires MET1. In contrast to DNA methylation at TEs, however, gbM does not appear to be associated with transcriptional repression. Rather, genes containing gbM are ubiquitously expressed at moderate to high levels compared with non-gbM genes (4, 5, 9), and within gbM genes there is a correlation between transcript abundance and methylation levels (10, 11).It has been proposed ...

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Diversification times among Brassica (Brassicaceae) crops suggest hybrid formation after 20 million years of divergence

Abstract: These results challenge previous hypotheses about the biogeographic origins of the tribe Brassiceae and the crop Brassica species and appear to be correlated with major geological and climatic events in the Mediterranean basin.

Cited by 95 publications

References 58 publications

Polyploid Evolution of the Brassicaceae during the Cenozoic Era

Polyploid Evolution of the Brassicaceae during the Cenozoic Era

Genome Triplication Drove the Diversification of Brassica Plants

On the origin and evolutionary consequences of gene body DNA methylation

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