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

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.

Assembly and origin of the flora of the Chihuahuan Desert: The case of sclerophyllous Rosaceae

“…angustifolia 30.5 Mya, V. australis 9.59 Mya, Amelanchier‐Malacomeles 34.08 Mya, Xerospiraea 44.07 Mya, Cercocarpus 35.49 Mya, Purshia 33.02 Mya, C. fothergilloides 21.7 Mya , C. pringlei ‐ C . rzedowskii 12.37 Mya) coincide with those of previous studies (Lo & Donoghue, ; Xiang et al, ; Zhang et al, ). Furthermore, divergence time in hard‐leaved shrubby Rosaceae occurred mostly in the Mid‐Eocene, however, divergence among current lineages began in the Oligocene (e.g., Lindleya , Vauquelinia and Amelanchier ) with most of the species studied not diverging until the Late Miocene, (e.g., A. paniculata , C. rzedowskii , C. pringlei , Kageneckia , L. mespiloides , M. denticulata , V. corymbosa and V. australis ).…”

“…The fossil of Vauquelinia comptonifolia was identified in the Green River Formation in Wyoming, and dated at 46.2–40.4 Mya in the Mid‐Eocene (MacGinitie, ). Stem and crown ages of Rosaceae were according to previous studies (Xiang et al, ; Zhang et al, ). Three independent MCMC runs were performed with 40 million generations and sampling every 40,000 generations.…”

“…Amelanchier , Cercocarpus , Malacomeles and Purshia have representatives distributed in this arid land. The time of divergence for Rosaceae has been estimated at 95.09 Mya including its three subfamilies (Amygdaloidae: 90.18 Mya; Rosoideae: 75.78 Mya; Dryadoideae: 40.67 Mya; Lo & Donoghue, ; Xiang et al, ; Zhang et al, ). Furthermore, for the tribe Maleae to which most of the species in the Chihuahuan Desert belong, the time of divergence was established in the Eocene‐Oligocene (56–43 Mya), suggesting that the current diversity of this group did not originate until the Miocene (23–5.3 Mya), coinciding with the onset of aridity in North America (Lo & Donoghue, ; Xiang et al, ).…”

“…The time of divergence for Rosaceae has been estimated at 95.09 Mya including its three subfamilies (Amygdaloidae: 90.18 Mya; Rosoideae: 75.78 Mya; Dryadoideae: 40.67 Mya; Lo & Donoghue, ; Xiang et al, ; Zhang et al, ). Furthermore, for the tribe Maleae to which most of the species in the Chihuahuan Desert belong, the time of divergence was established in the Eocene‐Oligocene (56–43 Mya), suggesting that the current diversity of this group did not originate until the Miocene (23–5.3 Mya), coinciding with the onset of aridity in North America (Lo & Donoghue, ; Xiang et al, ). With regard to macrofossils, the fossil Madro‐Tertiary Flora included Amelanchier (Middle Eocene 45 Mya, and Oligocene 30–33 Mya), Cercocarpus (Late Eocene 34.1 Mya, Oligocene 30.7 Mya, and Late Miocene 12 Mya), and Vauquelinia (Late Eocene 34.1 Mya, and Oligocene 30.7 Mya; Axelrod, ).…”

Genetic mapping in polyploids

“…It also yielded a detailed picture of the high level of genomic conservation between these species (Figure 4a,b). Both Rosa and Fragaria belong to the Rosoideae clade (in the Potentilleae and Roseae tribes, respectively), whose divergence is estimated to have occurred approximately 60 mya (million years ago) (Xiang et al, 2016). High levels of gene conservation have also been reported in the grass family, for example (Bennetzen, 2007).…”