Phylogeny, Age, and Evolution of Tribe Lilieae (Liliaceae) Based on Whole Plastid Genomes

Abstract

Tribe Lilieae, encompassing Lilium, Notholirion, Cardiocrinum, and Fritillaria, includes economically important crops with a horticultural and medicinal value. It is considered to be a core lineage of Liliaceae, but phylogenetic relationships within it, and the timing of the origin of individual clades, remain incompletely resolved. To address these issues, we reconstructed the evolutionary history of the tribe. We sequenced 45 Liliaceae plastomes and combined them with publicly available data (for a total of 139 plastomes) to explore the systematics, origin, divergence, and evolution of Lilieae. Our taxon sampling covers all ten sections of Lilium, all Cardiocrinum species, three Notholirion species, and major phylogenetic clades of Fritillaria. Our phylogenetic analysis confirms the monophyly of major sections/subgenera of Lilium and Fritillaria with strong support. We dated the origin of Lilieae to the Eocene, with genera and species radiations inferred to have occurred in the Miocene. The reconstruction of the ancestral area implies that Lilieae may have originated from the Qinghai-Tibet Plateau (QTP): the Himalayas and Hengduan Mountains and uplifting of the QTP likely promoted divergence within the tribe. Ancestral-state reconstructions of the bulb component number (including bulblets and scales) show a strong correlation with the genus-level phylogenetic diversity in Lilieae. They also predict that the most recent common ancestor of Lilieae had bulbs with numerous bulblets. Based on these observations, we predicted that climatic oscillations associated with the QTP uplift played an important role in the evolution of the Lilieae bulb. Our findings provide a well-supported picture of evolutionary relationships and a useful framework for understanding the pathway of bulb evolution within Lilieae, contributing to a better understanding of the evolutionary history of lilies.

Keywords: Fritillaria; Liliales; Lilium; QTP; divergence time estimate; trait evolution.

FIGURE 1

Phylogenetic relationships of Lilieae species inferred using whole plastomes (WP) and nuclear ribosomal internal transcribed spacer (ITS) sequence data. Maximum-likelihood bootstrap support/Bayesian posterior probability values are shown near corresponding nodes (“-” indicates support values less than 50%; “*” represents 100%/1 support). The genus, subgenus, and sectional classifications of Lilieae are indicated to the middle of trees and colored within trees. (A) Phylogenetic relationships inferred from WP data and (B) Phylogenetic relationships inferred from ITS data.

FIGURE 2

The estimation of divergence time based on 139 plastomes of Liliales and outgroups. The 95% highest posterior density (HPD) estimates for each well-supported clade are represented by bars. The APG (2016) classification is indicated to the right of the tree and colored within the tree. Yellow pentagons indicate six calibration points (see text).

FIGURE 3

Reconstructions of the ancestral area based on plastome-based phylogeny of Lilieae (see Figure 1A). Pie charts show proportions of inferred ancestral ranges, pie slice colors to regions defined in the caption and inset world map. Mean divergence ages are given on nodes (see Figure 2). Bars on nodes indicate the 95% HPD of divergence ages.

FIGURE 4

Reconstruction of the ancestral trait of Liliaea bulbs. (A) Reconstruction of the ancestral trait; (B–O) Bulb types of selected Lilieae species: (B) L. taliense, (C) L. pardanthinum, (D) L. sulphureum, (E) L. lophophorum, (F) L. duchartrei, (G) L. pensylvanicum, (H) L. distichum, (I) L. davidii, (J) L. brownii, (K) F. delavayi, (L) F. davidii, (M) F. maximowiczii, (N) C. giganteum, and (O) N. bulbuliferum.