Dated molecular phylogenies indicate a Miocene origin for Arabidopsis thaliana

Abstract

Dated molecular phylogenies are the basis for understanding species diversity and for linking changes in rates of diversification with historical events such as restructuring in developmental pathways, genome doubling, or dispersal onto a new continent. Valid fossil calibration points are essential to the accurate estimation of divergence dates, but for many groups of flowering plants fossil evidence is unavailable or limited. Arabidopsis thaliana, the primary genetic model in plant biology and the first plant to have its entire genome sequenced, belongs to one such group, the plant family Brassicaceae. Thus, the timing of A. thaliana evolution and the history of its genome have been controversial. We bring previously overlooked fossil evidence to bear on these questions and find the split between A. thaliana and Arabidopsis lyrata occurred about 13 Mya, and that the split between Arabidopsis and the Brassica complex (broccoli, cabbage, canola) occurred about 43 Mya. These estimates, which are two-to threefold older than previous estimates, indicate that gene, genomic, and developmental evolution occurred much more slowly than previously hypothesized and that Arabidopsis evolved during a period of warming rather than of cooling. We detected a 2-to 10-fold shift in species diversification rates on the branch uniting Brassicaceae with its sister families. The timing of this shift suggests a possible impact of the Cretaceous-Paleogene mass extinction on their radiation and that Brassicales codiversified with pierid butterflies that specialize on mustard-oil-producing plants.he most important genetic model in plant biology is Arabidopsis thaliana. It is the first plant to have its entire genome sequenced, and it serves as a key comparison point with other eukaryotic genomes. A. thaliana is diploid and has a small genome distributed on just five chromosomes, considerations in its choice as a model (1). The age of the Arabidopsis crown group (CG), previously estimated at 5.8-3 Mya (2, 3), and of splits within Brassicaceae have been used to understand the pace of evolution in genes affecting self-incompatibility (4, 5), the rate of change in signal transduction and gene expression (6, 7), the persistence of shared chromosomal rearrangements in A. thaliana and Brassica oleracea (8), the tempo of evolution of miRNA sequences (9), the evolution of pierid butterflies specializing in plants that produce mustard oils (10), and the ages of wholegenome duplication (WGD) events giving rise to gene pairs in Arabidopsis (11). As genomes of additional Brassicaceae (e.g., Capsella rubella) and other Brassicales (e.g., Carica papaya) (12) are sequenced, the importance of robust estimates of divergence dates relating these genomes to one another and to the geological record increases substantially.The accuracy of divergence times inferred from sequence data depends on valid, verifiable fossils to calibrate phylogenetic trees. Previous dates for the origin of Arabidopsis relied on the report of fossil pollen assigned to the genus Rori...

Polyploid Evolution of the Brassicaceae during the Cenozoic Era

“…Furthermore, it was previously shown that the Ks branch lengths of Cleome and Arabidopsis from Gossypium (outgroup) are also nearly identical ). Collectively, these results suggest that both Brassicaceae and Cleomaceae species are evolving with a similar molecular evolutionary rate and, thus, a single synonymous substitution rate of 8.22 3 10 2 9 substitutions/ synonymous site/year for Brassicaceae species, extrapolated using an established age of 22.5 million years ago (Mya) for the whole-genome triplication event in diploid brassicas (Beilstein et al, 2010), is applicable to both Brassicaceae and Cleomaceae-specific polyploidization events.…”

“…Additionally, early comparative genetic mapping (Parkin et al, 2005) and cytogenetic studies (Lysak et al, 2005;Ziolkowski et al, 2006), as well as the recent whole-genome sequencing of Brassica rapa (Wang et al, 2011) have identified an additional later mesopolyploidy (wholegenome triplication) event in diploid Brassicas. Using Bayesian approaches and fossil information as age constraints, the age of the triplication event has now been estimated to be 22.5 million years (Beilstein et al, 2010). Similarly, recent genome sequencing of Leavenworthia alabamica (Haudry et al, 2013), Camelina sativa (Kagale et al, 2014), and Brassica oleracea (Liu et al, 2014;Parkin et al, 2014) have uncovered more recent neo/mesopolyploidy events that formed the basis for the evolution of their hexaploid genomes.…”

Molecular phylogeny and systematics of the tribe Chorisporeae (Brassicaceae)

“…Recent family-wide studies (e.g., Beilstein et al 2006Beilstein et al , 2008Beilstein et al , 2010Warwick et al 2007Warwick et al , 2010; Koch et al 2007;Koch and Al-Shehbaz 2009;Franzke et al 2009;German et al 2009;Couvreur et al 2010;Zhao et al 2010) were congruent and showed that the vast majority of tribes can be assigned to three phylogenetic lineages (designated I, II, and III in Beilstein et al 2006). These studies are further congruent in the placement in lineage III of Chorisporeae C.A.…”

The genome of the mesopolyploid crop species Brassica rapa

“…With more than 300 additional genera, Brassica species alone includes many important vegetables that are widely used in the cuisine of many cultures (B. rapa: Chinese cabbage, Pak-choi and turnip; B. oleracea: broccoli, cabbage and cauliflower) as well as oilseed crops (B. napus, B. rapa, B. juncea and B. carinata) which provide collectively 12% of world edible vegetable oil production 5 . The six widely cultivated Brassica species are also a classical example of the importance of polyploidy in botanical evolution, described by the "U's triangle" 6 , with the three diploid oleracea 7 and B. rapa 8 since its divergence from the A. thaliana lineage 13-17 MYA 9,10 or more 11 .…”