Phylotranscriptomic analyses reveal multiple whole-genome duplication events, the history of diversification and adaptations in the Araceae

Abstract

Background and aims: The Araceae are one of the most diverse monocot families with numerous morphological and ecological novelties. Plastid and mitochondrial genes have been used to investigate the phylogeny and to interpret shifts in the pollination biology and biogeography of the Araceae. In contrast, the role of whole-genome duplication (WGD) in the evolution of eight subfamilies remains unclear.

Methods: New transcriptomes or low-depth whole-genome sequences of 65 species were generated through Illumina sequencing. We reconstructed the phylogenetic relationships of Araceae using concatenated and species tree methods, and then estimated the age of major clades using TreePL. We inferred the WGD events by Ks and gene tree methods. We investigated the diversification patterns applying time-dependent and trait-dependent models. The expansions of gene families and functional enrichments were analysed using CAFE and InterProScan.

Key results: Gymnostachydoideae was the earliest diverging lineage followed successively by Orontioideae, Lemnoideae and Lasioideae. In turn, they were followed by the clade of 'bisexual climbers' comprised of Pothoideae and Monsteroideae, which was resolved as the sister to the unisexual flowers clade of Zamioculcadoideae and Aroideae. A special WGD event ψ (psi) shared by the True-Araceae clade occurred in the Early Cretaceous. Net diversification rates first declined and then increased through time in the Araceae. The best diversification rate shift along the stem lineage of the True-Araceae clade was detected, and net diversification rates were enhanced following the ψ-WGD. Functional enrichment analyses revealed that some genes, such as those encoding heat shock proteins, glycosyl hydrolase and cytochrome P450, expanded within the True-Araceae clade.

Conclusions: Our results improve our understanding of aroid phylogeny using the large number of single-/low-copy nuclear genes. In contrast to the Proto-Araceae group and the lemnoid clade adaption to aquatic environments, our analyses of WGD, diversification and functional enrichment indicated that WGD may play a more important role in the evolution of adaptations to tropical, terrestrial environments in the True-Araceae clade. These insights provide us with new resources to interpret the evolution of the Araceae.

Keywords: Araceae; WGDs; adaptation; diversification; phylogenomics.

Fig. 1.

Phylogenetic tree of the Araceae using RAxML and ASTRAL methods based on 1081 orthologous groups from 60 representative species. Nodes with no values have 100 % bootstrap support. ‘-’ indicates that the two placements reconstructed by ASTRAL are inconsistent with the results inferred by RAxML.

Fig. 2.

The time-calibrated phylogenetic tree and evidence for WGD events in the Araceae. (A) Histograms of Ks distribution in the Proto-Araceae group and the lemnoid clade. (B) Histograms of Ks distribution of the True-Araceae clade. (C) The τ-WGD event was shared by the Araceae and other monocot families. The ψ-WGD event was shared by the True-Araceae clade. Fifty-two per cent of gene sub-trees were consistent with the species tree, and possibly supported a shared WGD by the True-Araceae clade using MAPS analyses. The three dotted lines indicate the OAE 1b, OAE 1d and K–Pg event from left to right.

Fig. 3.

Macroevolutionary dynamics of Araceae estimated by BAMM. (A) The pattern of net diversification rate across time. The rate-through-time plot indicates an increase in the diversification rate after the ψ-WGD event. (B) The placement of the best shift for the diversification of the Araceae. Branch colours represent the relative net diversification rates on the left side of the tree. Number 1 indicates the placement of the ψ-WGD event.

Fig. 4.

Differences in net diversification rates for the Proto-Araceae group, the lemnoid clade and the True-Araceae clade using three methods. Number 0 indicates the Proto-Araceae group and the lemnoid clade. Number 1 indicates the True-Araceae clade. (A) Diversification rate-through-time plots estimated by BAMM across time. (B) Results of BiSSE analyses; net diversification rates under the best-fit model are shown. (C) Results of HiSSE analyses with net diversification rates under the best-fit model. Net diversification rates are indicated as colour shadings along branch edges (from blue to red).