Elucidation of the phylogeny of Cucurbitaceae, particularly Trichosanthes, based on plastome data and nuclear single-copy genes.

BACKGROUND

Cucurbitaceae is an economically important family with a wide geographical distribution range. The phylogenetic backbone of Cucurbitaceae has not been well resolved, and conflicting results have been reported in previous phylogenetic studies. Trichosanthes is the largest genus in Cucurbitaceae; however, its infrageneric classification remains controversial. Here, we used both plastome and nuclear datasets to reconstruct the phylogeny of Cucurbitaceae with emphasis on Trichosanthes. The plastome dataset includes 137 taxa, representing 15 tribes and 35 genera. The 1,244 single-copy nuclear genes (SCNs) dataset includes 143 samples from all 15 tribes and 68 genera of Cucurbitaceae.

RESULTS

Phylograms of plastome dataset and 1,244 SCNs essentially agreed with each other with the exception of first branching tribes and Tr. Bryonieae. The phylogram of the plastome dataset was used to illustrate phylogeny and molecular dating. Cucurbitaceae was subdivided into nine clades along the phylogram backbone. The first branching clade of Cucurbitaceae included four tribes: Actionstemmateae, Fevilleeae, Gomphogyneae, and Zanonieae. Actionstemmateae was sister to the remaining three tribes, with Gomphogyneae and Fevilleeae being successive sister to Zanonieae. Six tribes, including Indofevilleeae, Thladiantheae, Momordiceae, Siraitieae, Joliffieae, and Bryonieae, formed successive and well-supported clades along the backbone of Cucurbitaceae. Cucurbitaceae originated in the Late Cretaceous (ca. 94.186 million years ago [MYA]), and diversified during the Late Cretaceous to the Eocene. Diversification of all tribes occurred during the later Cretaceous to Eocene. Trichosanthes originated ca. 30.089 MYA, and the section diversification occurred in middle Miocene approximately 6 million years (20.839 - 14.804 MYA). Climate optimum in the Mid-Eocene and Mid-Miocene was probably among the important drivers of the diversification of Trichosanthes complex.

CONCLUSIONS

Our results provide new insights into the phylogeny of Cucurbitaceae, including members of the first branching clade and the relative phylogenetic positions of Indofevilleeae, Thladiantheae, and Momordiceae, and show that Trichosanthes is paraphyletic with three genera nested within it. Our results suggest that the previously proposed infrageneric classification systems for Trichosanthes need to be revised. Section Involucraria was subdivided into two distantly related groups. Trichosanthes originated in the Oligocene and experienced rapid diversification in the Middle Miocene and throughout the Pliocene. Long-fringed petals might have arisen once in a clade formed by Trichosanthes and Hodgsonia.