Liriodendron genome sheds light on angiosperm phylogeny and species-pair differentiation

Abstract

The genus Liriodendron belongs to the family Magnoliaceae, which resides within the magnoliids, an early diverging lineage of the Mesangiospermae. However, the phylogenetic relationship of magnoliids with eudicots and monocots has not been conclusively resolved and thus remains to be determined^1-6. Liriodendron is a relict lineage from the Tertiary with two distinct species-one East Asian (L. chinense (Hemsley) Sargent) and one eastern North American (L. tulipifera Linn)-identified as a vicariad species pair. However, the genetic divergence and evolutionary trajectories of these species remain to be elucidated at the whole-genome level⁷. Here, we report the first de novo genome assembly of a plant in the Magnoliaceae, L. chinense. Phylogenetic analyses suggest that magnoliids are sister to the clade consisting of eudicots and monocots, with rapid diversification occurring in the common ancestor of these three lineages. Analyses of population genetic structure indicate that L. chinense has diverged into two lineages-the eastern and western groups-in China. While L. tulipifera in North America is genetically positioned between the two L. chinense groups, it is closer to the eastern group. This result is consistent with phenotypic observations that suggest that the eastern and western groups of China may have diverged long ago, possibly before the intercontinental differentiation between L. chinense and L. tulipifera. Genetic diversity analyses show that L. chinense has tenfold higher genetic diversity than L. tulipifera, suggesting that the complicated regions comprising east-west-orientated mountains and the Yangtze river basin (especially near 30° N latitude) in East Asia offered more successful refugia than the south-north-orientated mountain valleys in eastern North America during the Quaternary glacial period.

Fig. 1. Liriodendron lineage-specific WGD.

a, K_s distributions for the whole paranome identified from the whole genome of Liriodendron (green), grape (blue) and Amborella (orange). WGT, whole-genome triplication. b, K_s distribution for the whole paranome identified from the whole transcriptome of L. chinense. c, Comparison of Liriodendron and grape genomes. Dot plots of orthologues show a 2–3 chromosomal relationship between the Liriodendron genome and grape genome. d, Macrosynteny patterns show that a typical ancestral region in the basal angiosperm Amborella can be tracked to up to two regions in Liriodendron and to up to three regions in the grape. Grey wedges in the background highlight major syntenic blocks spanning more than 30 genes between the genomes (highlighted by one syntenic set shown in colour). e, Microcollinearity patterns between genomic regions from Amborella, Liriodendron and the grape. Rectangles represent predicted gene models, with purple and brown showing relative gene orientations. Grey wedges connect matching gene pairs, with two sets highlighted in red.

Fig. 2. Phylogenetic relationships among magnoliids, eudicots and monocots.

a, Liriodendron shows typical features of monocots in its reproductive organs (flower parts in multiples of three and monosulcate pollen grains) and of eudicots in its vegetative organs (two cotyledons, a taproot system, a eudicot-like stem cross-section and netted venation). These experiments were repeated independently at least ten times with similar results. Scale bar, 200 µm. b, Three topologies that coincided with three alternative phylogenetic hypotheses are plotted, and the results of a chi-squared test of the orthogroup numbers supporting each topology are shown below, revealing no statistically significant difference in topology preference. c, The eudicot- and monocot-specific gene families present in Liriodendron are statistically similar to those present in Amborella, whereas Spirodela polyrhiza has a bias towards monocot-specific gene families, and Macleaya cordata has a bias towards eudicot-specific gene families when compared with Amborella. d, Dated phylogeny for 11 plant species with Picea abies as an outgroup. A time scale is shown at the bottom, and red points in some nodes indicate fossil calibration points.

Fig. 3. Geographic distribution and population diversity of Liriodendron accessions.

a, Geographic distribution of Liriodendron accessions. Brown triangles represent the fossil distribution of Liriodendron plants in high-latitude regions of the Northern Hemisphere. Fringe patterns show two principal refugia where Tertiary relict floras occurred: southern East Asia and eastern North America. The natural distributions of L. chinense and L. tulipifera are plotted, with coloured dots representing individual Liriodendron accessions. b, Neighbour-joining tree of all accessions constructed from whole-genome SNPs. Accessions coming from the same geographic areas are grouped together and coloured corresponding to the colours used in a. LY, Liu Yang; SZ, Sang Zhi; EX, E Xi; ST, Song Tao; LP, Li Ping; ML, Meng La; XY, Xu Yong; SN, Sui Ning; DBS, DaBie Shan; HS, Huang Shan; LS1, Lushan_1; SY, Song Yang; LS2, Lushan_2; WYS, WuYi Shan; ON, Ontario; LA, Louisiana; GA, Georgia; TN, Tennessee; NC, North Carolina; MO, Missouri. c, Principal component analysis plots of the first two components for all 20 accessions, with dots coloured corresponding to their provenances. d, Nucleotide diversity (π) and population divergence (F_ST) across the three groups. The value in each circle represents a measure of nucleotide diversity for this group, and the value on each line indicates the population divergence between the two groups.

Fig. 4. Historical fluctuations in effective population size.

a–c, Plots of PSMC results for 20 individuals (7 from western China (a); 7 from eastern China (b); and 6 from North America (c)), as indicated in each legend. The grey lines represent the mass accumulation rate (MAR) of the Chinese Loess Plateau in a and b, and the atmospheric surface air temperature relative to the present in c.