Each of these was used again as the query of a BLAST search against the genomes of the 26 other angiosperms with an e-value threshold that was raised to 10 to increase the length of the compared region. Only the best matching region returned by the BLAST search was considered, which removed segments of the predicted cDNA that were highly divergent between distantly related taxa and would be poorly aligned.
At this stage, matrices were discarded if the total alignment was smaller than bp or the smallest sequence was smaller than bp. A phylogenetic tree was inferred for each of the remaining single-gene matrices using PhyML Guindon and Gascuel under the substitution model deemed adequately parameter-rich for each data set using likelihood ratio tests done with PhyML while fixing the topology to that inferred under a HKY model.
Orthology was assessed by comparing the inferred topology with the expected species tree based on Soltis et al.
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An accurate estimation of the P -value by the S-H test theoretically requires that a large pool of plausible trees be sampled Goldman et al. The selected data sets might consequently include some false negatives, especially in the case of closely related paralogs. The test however represents a rapid way to compare topologies for a large number of data sets and to identify most cases of paralogy problems. Differences between nuclear and plastid phylogenies can also be caused by incomplete lineage sorting or hybridization, but with 27 species spread so broadly across angiosperms, the resulting topological differences would be small if existent at all Maddison and Knowles , and topology tests would likely not be significant.
On the other hand, significant topological differences due to lateral gene transfer between distantly related species cannot be differentiated from paralogy problems without a careful evaluation of the gene diversity present in diverse genomes Christin et al. Our approach removes such sequences and is consequently conservative. The remaining alignments were assumed to be composed of only co-orthologs sensu Sonnhammer and Koonin and were used for dating analyses. The topology corresponding to the expected species tree based on Soltis et al. Of the 27, coding sequences predicted from the Sorghum bicolor genome, had a homolog in all of the 27 other plant genomes.
After removing all the alignments that were too short data sets or that produced phylogenies incompatible with the species tree data sets , a total of data sets were retained. Of these, 5 were further removed because they represented duplicates that arose in the ancestor of Sorghum after the diversification of Poaceae they matched the same loci as other Sorghum markers in at least some other grasses.
The final data set included loci for a total of 83, aligned bp. Each data set was analysed with two sets of calibration points see below and with four different methods. These methods all use a Bayesian procedure and allow for rate variation among branches of the phylogenetic tree, but they differ in their assumptions.
For analyses using BEAST, two independent MCMC tree searches were run for 20,, generations, with a sampling frequency of generations after a burn-in period of 5,, The adequacy of the length of the analysis and burn-in period was confirmed using Tracer Rambaut and Drummond through a visual inspection of the traces for the tree likelihood and the substitution model parameters and checking that their ESS was larger than The prior on the distribution of node ages was approximated by a Yule speciation process and evolutionary rates among branches followed a log-normal distribution.
The topology was kept constant throughout the analyses, which was necessary to directly compare results across multiple software programs, models, and priors. The different markers were concatenated into a single plastid and a single nuclear data set, which were first used without data partitioning. Additional BEAST analyses of the plastid and genome data sets allowed different substitution model parameters for 1st, 2nd and 3rd positions of codons, which did not significantly alter the results Supplementary Fig.
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S1; available on http: For all analyses, ages and rates were computed as the median across the set of sampled trees. In addition, standard deviations were calculated to obtain estimates comparable across software packages. The analyses were also done with the correlated CIR model Lepage et al. Ages were retrieved from the sampled trees, with a burn-in period of cycles and a sampling frequency of 10 cycles. The MCMC procedure was run for 1,, generations, with a sampling frequency of generations after a burn-in period of , The effect of the prior was evaluated by rerunning the analysis under external calibration only see below with different values for four priors.
With the scale in twenties of million years ago, the mean and standard deviation of the rate at the root were set successively to 0. For each of these combinations, the mean and standard deviation of the Brownian motion constant were independently changed to the following values; 0. For these additional analyses, the burn-in period was decreased to 10, generations and the sampling frequency and number of samples to , to allow additional comparisons. To evaluate the effect of sampling density, the plastid data set was reanalysed with a species sampling similar to that of the nuclear genomes.
Plastid sequences for 28 species that were identical or closely related to those in the nuclear data set Fig. In addition, to evaluate the effect of sequence length, dating analyses were repeated with a number of nucleotides corresponding to the plastid data set sampled without replacement from the nuclear data set.
Dating analyses were run without taking into account Poaceae fossils, which were compared a posteriori to the ages inferred for various nodes within grasses Table 1. The exclusion of Poaceae fossils as calibration points in the initial analysis allowed their later use to validate or invalidate the results of alternative dating hypotheses. Fossils with reliable dates and taxonomic placement for eudicots and non-grass monocots were used to set minimal ages on stem nodes of clades to which they have been previously assigned.
These calibration densities are not equal to the marginal prior distributions, which are also influenced by the topological constraints and tree prior Heled and Drummond BEAST analyses were first run without molecular data, which showed that the marginal prior distributions take non-uniform distributions when the topology is fixed Supplementary Figs. S2—S5, available at http: Based on the review by Magallon and Sanderson , minimal bounds were set at In addition, a minimal age of Ma was set on the stem node of core eudicots, based on the appearance of tricolpate pollen in the fossil record Friis et al.
The appearance of tricolpate pollen was also used to set a maximal age for the crown of core eudicots at Ma. The rationale behind this constraint is that, given the rich fossil record of pollen and the distinctive morphology of tricolpate pollen, it is unlikely that tricolpate pollen grains would be undetected for a long period of time after their evolution Anderson et al.
The use of maximal age constraints is controversial, but its absence can lead to unacceptably ancient divergence time estimates Hug and Roger ; Ho and Phillips Compatibility of dating analyses with fossil evidence a. Ages not compatible with fossil evidence are indicated by an asterisk; b Elias ; c Crepet and Feldman ; d Herendeen and Crane , compared with age of the crown Poaceae; e Fox and Koch , compared with stem of core Chloridoideae; f , g Prasad et al. These nine constraints are congruent with each other Christin et al. Not all of the calibration points listed above could be placed in the phylogeny based on markers from whole genomes or the reduced phylogeny based on plastid markers.
Because of the reduced species sampling, the corresponding node was not present in these smaller phylogenies. Consequently, constraints on Buxales, Typhales, Liliales and Zingiberales were not used for these analyses. Phytoliths are microscopic silica bodies precipitated in and around plant cells in many land plants that remain in the soil when plants die and decay Piperno The morphology of grass phytoliths varies among extant taxa, suggesting that fossil phytoliths might be assigned to specific taxonomic groups and be informative regarding the timing of speciation events Prasad et al.
Fossilized phytoliths, and especially the associated cuticles, are relatively rare in ancient soils and the described fossils are unlikely to represent the earliest appearance of the group. The 67 Ma phytoliths fossils were consequently included as a minimal age on the stem of Oryzeae last common ancestor of Oryza sativa and Microlaena stipoides. In the nuclear genomes data set, O. Strong variation in branch lengths was present in the plastid phylogeny Fig.
In particular, the average length from the root of the tree to the tips of the BEP-PACMAD clade greatly exceeded that of branches leading to most other monocots, including the other graminid lineages sensu Givnish et al. Comparison of the fit of different molecular clock models a. The ages estimated by BEAST are compatible with the known macrofossils, but not with phytoliths attributed to Oryzeae, even if these are attributed to more ancient ancestors of Oryzeae Table 1.
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S6, available at http: Effect of different calibrations on inferred evolutionary rates. The distribution of rates in expected mutations per site per billion years inferred by BEAST for different taxonomic groups is indicated by boxplots for external calibration only black and external calibration plus phytoliths gray , for a plastid markers and b nuclear markers. Ages estimated under external calibration only a.
In contrast, the correlated log-normal model implemented in the same software led to younger estimates for nodes within graminids, as well as older estimates for multiple nodes outsides graminids Fig. If the prior for the standard deviation of the Brownian motion constant is very small 0. S7, available at http: We interpreted age estimates to be incompatible with the fossil record if the maximum credible age for a given node was younger than a known fossil belonging to that clade. Comparison of age estimates produced by different methods on plastid markers.
For external calibration only, ages estimated by BEAST in million years ago are compared with those produced by other methods. Black lines indicate 1: Using phytolith fossils as a calibration point external calibration plus phytoliths strongly affected estimated ages with all methods Table 4. As illustrated with BEAST results, this extra calibration point leads to older estimates for all nodes within graminids, but has little effect on nodes within eudicots Fig.
Ages estimated by BEAST in million years ago under external calibration plus phytoliths are plotted against those obtained under external calibration only. The black line indicates 1: Ages estimated from plastid markers under external calibration plus phytoliths a. Differences in root-to-tip length between BEP-PACMAD and other taxa was smaller in the trees inferred with nuclear genomes than in those from plastid markers, with the exception of the Brassicaceae which had longer root-to-tip distances than other taxa Fig. In the absence of constraints within grasses, the ages estimated from the transcripts were very similar among the different methods, with an age for the crown of BEP-PACMAD at With the exception of one node within eudicots at the base of Brassicaceae , these ages were, moreover, very similar to those inferred from plastid markers with BEAST Fig.
However, they were not compatible with putative Oryzeae phytoliths at 67 Ma, as the crown of the BEP clade the group containing Oryzeae was estimated at Differences between plastid and nuclear markers were not due to different species numbers or sequence length, as the data sets sampled to the same size produced similar results Supplementary Fig. S8, available at http: Feb 02, marine biologist.
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