Evolution of Portulacineae Marked by Gene Tree Conflict and Gene Family Expansion Associated with Adaptation to Harsh Environments.

Several plant lineages have evolved adaptations that allow survival in extreme and harsh environments including many families within the plant clade Portulacineae (Caryophyllales) such as the Cactaceae, Didiereaceae, and Montiaceae. Here, using newly generated transcriptomic data, we reconstructed the phylogeny of Portulacineae and examined potential correlates between molecular evolution and adaptation to harsh environments. Our phylogenetic results were largely congruent with previous analyses, but we identified several early diverging nodes characterized by extensive gene tree conflict. For particularly contentious nodes, we present detailed information about the phylogenetic signal for alternative relationships. We also analyzed the frequency of gene duplications, confirmed previously identified whole genome duplications (WGD), and proposed a previously unidentified WGD event within the Didiereaceae. We found that the WGD events were typically associated with shifts in climatic niche but did not find a direct association with WGDs and diversification rate shifts. Diversification shifts occurred within the Portulacaceae, Cactaceae, and Anacampserotaceae, and whereas these did not experience WGDs, the Cactaceae experienced extensive gene duplications. We examined gene family expansion and molecular evolutionary patterns with a focus on genes associated with environmental stress responses and found evidence for significant gene family expansion in genes with stress adaptation and clades found in extreme environments. These results provide important directions for further and deeper examination of the potential links between molecular evolutionary patterns and adaptation to harsh environments.

Improved transcriptome sampling pinpoints 26 ancient and more recent polyploidy events in Caryophyllales, including two allopolyploidy events.

Studies of the macroevolutionary legacy of polyploidy are limited by an incomplete sampling of these events across the tree of life. To better locate and understand these events, we need comprehensive taxonomic sampling as well as homology inference methods that accurately reconstruct the frequency and location of gene duplications. We assembled a data set of transcriptomes and genomes from 168 species in Caryophyllales, of which 43 transcriptomes were newly generated for this study, representing one of the most densely sampled genomic-scale data sets available. We carried out phylogenomic analyses using a modified phylome strategy to reconstruct the species tree. We mapped the phylogenetic distribution of polyploidy events by both tree-based and distance-based methods, and explicitly tested scenarios for allopolyploidy. We identified 26 ancient and more recent polyploidy events distributed throughout Caryophyllales. Two of these events were inferred to be allopolyploidy. Through dense phylogenomic sampling, we show the propensity of polyploidy throughout the evolutionary history of Caryophyllales. We also provide a framework for utilizing transcriptome data to detect allopolyploidy, which is important as it may have different macroevolutionary implications compared with autopolyploidy.

From cacti to carnivores: Improved phylotranscriptomic sampling and hierarchical homology inference provide further insight into the evolution of Caryophyllales.

PREMISE OF THE STUDY: The Caryophyllales contain ~12,500 species and are known for their cosmopolitan distribution, convergence of trait evolution, and extreme adaptations. Some relationships within the Caryophyllales, like those of many large plant clades, remain unclear, and phylogenetic studies often recover alternative hypotheses. We explore the utility of broad and dense transcriptome sampling across the order for resolving evolutionary relationships in Caryophyllales. METHODS: We generated 84 transcriptomes and combined these with 224 publicly available transcriptomes to perform a phylogenomic analysis of Caryophyllales. To overcome the computational challenge of ortholog detection in such a large data set, we developed an approach for clustering gene families that allowed us to analyze >300 transcriptomes and genomes. We then inferred the species relationships using multiple methods and performed gene-tree conflict analyses. KEY RESULTS: Our phylogenetic analyses resolved many clades with strong support, but also showed significant gene-tree discordance. This discordance is not only a common feature of phylogenomic studies, but also represents an opportunity to understand processes that have structured phylogenies. We also found taxon sampling influences species-tree inference, highlighting the importance of more focused studies with additional taxon sampling. CONCLUSIONS: Transcriptomes are useful both for species-tree inference and for uncovering evolutionary complexity within lineages. Through analyses of gene-tree conflict and multiple methods of species-tree inference, we demonstrate that phylogenomic data can provide unparalleled insight into the evolutionary history of Caryophyllales. We also discuss a method for overcoming computational challenges associated with homolog clustering in large data sets.

Widespread paleopolyploidy, gene tree conflict, and recalcitrant relationships among the carnivorous Caryophyllales.

PREMISE OF STUDY: The carnivorous members of the large, hyperdiverse Caryophyllales (e.g., Venus flytrap, sundews, and Nepenthes pitcher plants) represent perhaps the oldest and most diverse lineage of carnivorous plants. However, despite numerous studies seeking to elucidate their evolutionary relationships, the early-diverging relationships remain unresolved. METHODS: To explore the utility of phylogenomic data sets for resolving relationships among the carnivorous Caryophyllales, we sequenced 10 transcriptomes, including all the carnivorous genera except those in the rare West African liana family Dioncophyllaceae. We used a variety of methods to infer the species tree, examine gene tree conflict, and infer paleopolyploidy events. KEY RESULTS: Phylogenomic analyses supported the monophyly of the carnivorous Caryophyllales, with a crown age of 68-83 million years. In contrast to previous analyses, we recovered the remaining noncore Caryophyllales as nonmonophyletic, although the node supporting this relationship contained a significant amount of gene tree discordance. We present evidence that the clade contains at least seven independent paleopolyploidy events, previously unresolved nodes from the literature have high levels of gene tree conflict, and taxon sampling influences topology even in a phylogenomic data set, regardless of the use of coalescent or supermatrix methods. CONCLUSIONS: Our data demonstrate the importance of carefully considering gene tree conflict and taxon sampling in phylogenomic analyses. Moreover, they provide a remarkable example of the propensity for paleopolyploidy in angiosperms, with at least seven such events in a clade of less than 2500 species.