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Resolution of Deep Angiosperm Phylogeny Using Conserved Nuclear Genes and Estimates of Early Divergence Times

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Resolution of Deep Angiosperm Phylogeny Using Conserved Nuclear Genes and Estimates of Early Divergence Times

Liping Zeng et al. Nat Commun.

Abstract

Angiosperms are the most successful plants and support human livelihood and ecosystems. Angiosperm phylogeny is the foundation of studies of gene function and phenotypic evolution, divergence time estimation and biogeography. The relationship of the five divergent groups of the Mesangiospermae (~99.95% of extant angiosperms) remains uncertain, with multiple hypotheses reported in the literature. Here transcriptome data sets are obtained from 26 species lacking sequenced genomes, representing each of the five groups: eudicots, monocots, magnoliids, Chloranthaceae and Ceratophyllaceae. Phylogenetic analyses using 59 carefully selected low-copy nuclear genes resulted in highly supported relationships: sisterhood of eudicots and a clade containing Chloranthaceae and Ceratophyllaceae, with magnoliids being the next sister group, followed by monocots. Our topology allows a re-examination of the evolutionary patterns of 110 morphological characters. The molecular clock estimates of Mesangiospermae diversification during the late to middle Jurassic correspond well to the origins of some insects, which may have been a factor facilitating early angiosperm radiation.

Figures

Figure 1
Figure 1. Five recently published representative topologies among eudicots (Eud), monocots (Mon), magnoliids (Mag), Ceratophyllaceae (Cer) and Chloranthaceae (Chl).
Shown are topologies derived from: (a) refs , and ; (b) ref. ; (c) ref. ; (d) ref. ; and (e) ref. . Out stands for the outgroup, an asterisk indicates a BS value of 100%.
Figure 2
Figure 2. A cladogram depicting established relationships of 20 representative species.
This tree was used as the reference for selecting suitable nuclear gene markers, with uncertain relationships collapsed.
Figure 3
Figure 3. A highly supported hypothesis for relationships among the five major groups of Mesangiospermae.
(a) A phylogeny of 61 taxa using 59 genes. Numbers associated with nodes are the bootstrap value (BS, on the left) obtained by RAxML and the posterior probability (PP, on the right) obtained by MrBayes based on concatenated 59 genes. Asterisks indicate either BS of 100% or PP of 1.0. Diamonds indicate both BS of 100% and PP of 1.0. Taxa with transcriptome data specifically generated for this study are shown in bold. (b) An abbreviated tree showing the relationship of the five lineages of Mesangiospermae, with associated support values (BS/PP).
Figure 4
Figure 4. The effect of the number of genes on the phylogenetic topology.
(a) percentages (y axis) of trees with the same topology as that in Fig. 3, when 20 trees were generated using the number (x axis) of randomly selected genes. The minimal number of genes required for 100% recovery of the (Chlor, Cerato), ((Chlor, Cerato), Eud) and (((Chlor, Cerato), Eud), Magnoliids) clades was 34, 40 and 48, respectively, as indicated by arrows. (b) A cladogram inferred by different numbers of ranked genes. Numbers associated with nodes are the bootstrap value (BS, above the line) obtained by RAxML and the posterior probability (PP, below the line) obtained by MrBayes with 55, 50, 46, 41, 33, 25 and 16 genes (right to left), respectively. BS of 100% or PP of 1.0 is indicated by asterisk. Chlor, Cerato, Eud, Magno, Mon and Out represent Chloranthaceae, Ceratophyllaceae, eudicots, magnoliids, monocots and outgroup, respectively.
Figure 5
Figure 5. Estimated divergence times of Mesangiospermae and shared morphological characters.
(a) The estimated divergence time for each node is shown relative to the geological time scale below the cladogram. Numbers in the rectangles on some branches indicate the numbers of morphological characters shared by the corresponding lineages. (by) Plant photographs show the diversities of angiosperms; (Rosids: A. thaliana (b), Chaenomeles cathayensis (c), Wisteria sinensis (d), Juglans regia (e); Asterids: Coreopsis basalis (f), Solanum wrightii (g), Scutellaria baicalensis (h), Pharbitis purpurea (i); Chloranthaceae: Chloranthus japonicus (j), Hedyosmum orientale (k), Sarcandra glabra (l); Ceratophyllaceae: Ceratophyllum demersum (m); Magnoliids: Magnolia denudata (n), Aristolochiae heterophyllae (o), Houttuynia cordata (p), Chimonanthus praecox (q); Monocots: Paphiopedilum henryanum (r), Cocos nucifera (s), Hippeastrum rutilum (t), Setaira viridis (u); Basal angiosperms: A. trichopoda (v), Nuphar advena (w), Cabomba caroliniana (x), Schisandra sphenanthera (y).
Figure 6
Figure 6. A chronogram showing the angiosperm divergence times as estimated by the BEAST using 59 genes.
Two fossil calibration points: (1) the earliest gymnosperm fossils (ca. 290–310 Myr) and (2) the earliest fossil tricolpate pollen (~125 Myr) were marked with two solid circles.

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