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. 2017 Feb 1;34(2):262-281.
doi: 10.1093/molbev/msw242.

Evolution of Rosaceae Fruit Types Based on Nuclear Phylogeny in the Context of Geological Times and Genome Duplication

Yezi Xiang  1 , Chien-Hsun Huang  1 , Yi Hu  2 , Jun Wen  3 , Shisheng Li  4 , Tingshuang Yi  5 , Hongyi Chen  4 , Jun Xiang  4 , Hong Ma  1
Affiliations

Evolution of Rosaceae Fruit Types Based on Nuclear Phylogeny in the Context of Geological Times and Genome Duplication

Yezi Xiang et al. Mol Biol Evol. .

Erratum in

Abstract

Fruits are the defining feature of angiosperms, likely have contributed to angiosperm successes by protecting and dispersing seeds, and provide foods to humans and other animals, with many morphological types and important ecological and agricultural implications. Rosaceae is a family with ∼3000 species and an extraordinary spectrum of distinct fruits, including fleshy peach, apple, and strawberry prized by their consumers, as well as dry achenetum and follicetum with features facilitating seed dispersal, excellent for studying fruit evolution. To address Rosaceae fruit evolution and other questions, we generated 125 new transcriptomic and genomic datasets and identified hundreds of nuclear genes to reconstruct a well-resolved Rosaceae phylogeny with highly supported monophyly of all subfamilies and tribes. Molecular clock analysis revealed an estimated age of ∼101.6 Ma for crown Rosaceae and divergence times of tribes and genera, providing a geological and climate context for fruit evolution. Phylogenomic analysis yielded strong evidence for numerous whole genome duplications (WGDs), supporting the hypothesis that the apple tribe had a WGD and revealing another one shared by fleshy fruit-bearing members of this tribe, with moderate support for WGDs in the peach tribe and other groups. Ancestral character reconstruction for fruit types supports independent origins of fleshy fruits from dry-fruit ancestors, including the evolution of drupes (e.g., peach) and pomes (e.g., apple) from follicetum, and drupetum (raspberry and blackberry) from achenetum. We propose that WGDs and environmental factors, including animals, contributed to the evolution of the many fruits in Rosaceae, which provide a foundation for understanding fruit evolution.

Keywords: Rosaceae; coalescence; fruit evolution; genome duplication; molecular clock; nuclear phylogeny.

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Figures

<sc>Fig</sc>. 1
Fig. 1
A summary of Rosaceae phylogeny and Rosaceae fruit morphologies. On the left is a summary tree with results from five coalescence analyses of 882, 571, 444, 256, and 113 gene sets, respectively, and a concatenation analysis using the 113-gene supermatrix. Topologies consistent in all six trees are drawn in black lines. Grey lines show uncertain relationships, with some trees support the topology. For further information see figure 3 and supplementary figure S14, Supplementary Material online. Asterisks (*) indicate 100% supports in all six trees. Diamonds indicate more than 90% supports in at least five trees and more than 85% supports in all six trees. Squares indicate more than 80% supports in at least three trees and more than 40% supports in all six trees. Plant photographs on the right show the diversity of Rosaceae fruits. The left row (from the top) includes Malus pumila (apple), Eriobotrya japonica (loquat), Kerria japonica, Prunus armeniaca (almond), Prunus sp. (cherry), Spiraea thunbergii, Duchesnea indica, Potentilla supina, Rosa laevigata, Rubus sp. (raspberry), and Dryas octopetala. The right row (from the top) includes Pyrus bretschneideri (pear), Crataegus pinnatifida, Exochorda racemosa, Prunus salicina (plum), Prunus persica (peach), Agrimonia pilosa, Fragaria × ananassa (strawberry), Geum aleppicum, Rosa sp., and Rubus fruticosus (blackberry).
<sc>Fig.</sc> 2
Fig. 2
A phylogeny from ML analysis using a dataset of concatenated 113 gene sequences. Numbers associated with nodes indicate bootstrap values obtained by Maximum Likelihood (ML) analyses. Asterisks (*) indicate 100% support.
<sc>Fig.</sc> 3
Fig. 3
A summary of alternative topologies in results from 12 coalescence analyses and one concatenation analysis. At the top are phylogenetic methods and numbers of genes in various sets and relationships between gene sets (see “Results” and “Materials and Methods” sections, and supplementary fig. S24, Supplementary Material online for additional information). The column on the left indicates possible topologies. Designations: Dryadoideae basal: Dryadoideae at the basal position, as sister to the combined clade of Amygdaloideae and Rosoideae, others similarly. K: Kerrieae. Ex: Exochordeae. So: Sorbarieae. G: Gillenieae. A: Agrimonieae. Po: Potentilleae. Ro: Roseae. Rh: Rhaphiolepis. Er: Eriobotrya. S: a combined clade of Sorbus alnifolia, Sorbus aria, Sorbus torminalis, Sorbus commixta, and Sorbus aucuparia. M: a clade including Malus baccata and its three nearest relatives (as shown in fig. 1). Py: Pyrus. C: Cydonia and its five nearest relatives (as in fig. 1). Number in each square refers to values in support of a particular topology indicated in the left column. Strong support refers to support values of at least 70%. Weak support refers to values less than 70%. If there is a strong support for a topology in a particular node, other topologies at this node are strongly rejected. If there is a weak support for a topology in a particular node, other topologies at this node are weakly rejected.
<sc>Fig.</sc> 4
Fig. 4
Chronogram of Rosaceae using 148 species phylogeny with 19 fossil constraints. Positions of the fossil calibrations are depicted with numbered circles. Crown nodes of Rosids, Rosales and Rosaceae are indicated with arrows. The red dashed line and blue strip highlight the Cretaceous-Paleogene and Eocene-Oligocene boundaries, respectively. Ages are presented as millions of years (Myr). There are two possible topologies within Dryadoideae (relationships among Purshia, Cercocarpus and Chamaebatia) having similar support from our analyses of various gene sets (see supplementary fig. S14, Supplementary Material online); here we only present the result from the analysis with the 113-gene concatenation. Jur: Jurassic. E- and L-Cretaceous mean Early and Late Cretaceous. Pal: Paleocene. Oli: Oligocene. P: Pliocene. Q: Quaternary.
<sc>Fig</sc>. 5
Fig. 5
Detecting and positioning large-scale gene duplications by comparing gene family trees to the species tree. Percentage of duplicated gene families (among those containing genes from both species lineages from the node of interest) are presented adjacent to each node when there were higher than 4% gene families duplicated at the corresponding node. Numbers higher than 10% and 50% are highlighted with blue and red, respectively. Distributions of three possible topologies for each of the duplicated gene trees are shown in the upper left table, with both the percentage and the actual numbers of gene families recorded. By the diagnosis of tree topologies, nodes with strong evidence for WGD are marked with yellow. Colored boxes indicate species potentially having gene duplications within a genus (dark blue) or shared across genera (light blue); genera having euploid variations summarized by Dickinson et al. (2007) (orange) or polyploid species observed by Vamosi and Dickinson (2006) (pink) or both (red) are also highlighted.
<sc>Fig.</sc> 6
Fig. 6
Evolutionary histories of fruit types in Rosaceae. (A) The evolutionary history of different fruit types in Rosaceae in the context of an abbreviated phylogeny from than shown in figure 1. Grey line represents ancestral fruit type of Rosaceae. Other line colors represent different fruit types of extant taxa. The positions of nodes and branches correspond with geological time scale on the right redrawn from the molecular clock analysis shown in figure 4. The positions of fruit drawings do not represent the history or age of the fruit types. (B) Proposed histories of three fruit types in Rosoideae. a: a hypothetical ancestral fruit of Rosoideae (achenetum); b: a hypothetical ancestral fruit of Rubus (drupetum, with less flesh); c: Rubus (drupetum, with more flesh); d: a hypothetical ancestral fruit of Fragaria (achenetum, without enlargement of receptacle); e: Fragaria (achenetum, with fleshy enlargement of receptacle); f: a hypothetical ancestral fruit of Rosa (achenetum, with partial enclosure of fruits by the hypanthium); g: Rosa (achenetum, with full enclosure by the hypanthium, and increased fruit size). (C) Proposed histories of several fruit types in Amygdaloideae. h, i: Hypothetical ancestral fruits of Amygdaloideae, evolving from a follicetum with many (indefinite) carpels (h) to that with five or fewer carpels (i). j: A hypothetical ancestor of Amygdaleae (nuculanium, with a few carpels). k: Prunus (drupe, with a single carpel). l, m: hypothetical ancestral fruits of Pyrinae. l evolved into m via the partial “sinking” of the ovary into the hypanthium and fusing with it. n: Crataegus (with the endocarp still near the top). o: Eriobotrya (with relatively thin flesh). p: Pseudocydonia (with many ovules for a carpel, a likely ancestral character). q: Malus (with centrally located endocarp along the vertical axis, thick flesh, and one or two seeds per carpel, all likely derived features).
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