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

Abstract

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.

Practical considerations for plant phylogenomics

“…Recently developed tools such as OrthoFinder (Emms and Kelly, ), in our experience, perform better than OrthoMCL in retaining gene family structure instead of breaking gene families apart. Approaches such as constructing phylomes (the collection of gene phylogenies for a taxon; Huerta‐Cepas et al., ) followed by tree‐based orthology pruning (Yang et al., ) or all‐by‐all BLAST followed by Markov clustering and tree‐based orthology pruning (Yang and Smith, ) are more appropriate for the challenges of plant orthology inference, especially with complex gene and genome duplication scenarios. Optimal homology and orthology inference in plants is still an active research area, with novel tools being developed by multiple research groups including the Joint Genome Institute (https://phytozome.jgi.doe.gov).…”

“…With proper orthology inference and filtering, phylotranscriptomic data sets using housekeeping genes can achieve matrix occupancy similar to Sanger-based methods (Yang and Smith, 2014;Yang et al, 2015Yang et al, , 2018. Methods developed without explicit consideration for gene and genome duplication events, such as HaMStR (Ebersberger et al, 2009) and OrthoMCL (Li et al, 2003), are potentially problematic in plants, especially when non-single-copy gene families are of interest.…”

Recurrent genome duplication events likely contributed to both the ancient and recent rise of ferns

“…Gene trees for each of the 4,067(MCL-BLAST) or 52,043 (Pure-MCL) OGs were reconstructed by using FastTree v2.1.4 (Price et al 2009(Price et al , 2010 under -nt model with default settings, and then gene duplications in all the gene trees were mapped onto a species tree (as in Figure 1A) (Qi et al 2018) with the same rationales as several previous studies (Cannon et al 2015;Li et al 2015;Yang et al 2015Yang et al , 2018 as well as ours using the script developed by one of us (J.Q.) (script available upon request).…”

The Origin and Early Evolution of the Legumes are a Complex Paleopolyploid Phylogenomic Tangle closely associated with the Cretaceous-Paleogene (K-Pg) Boundary

“…The recent proliferation of genomic data is revealing just how prevalent repeated WGDs have been in the history of the angiosperms (e.g. Wendel, 2015;Soltis et al, 2016;Yang et al, 2018) and how many large angiosperm clades are characterized by genome triplications (e.g. Pentapetalae, Brassicaceae, Asteraceae, Solanaceae).…”

“…On the other hand, many paleopolyploidy events that significantly pre-and post-date the KPB are known (e.g. Angiospermae (Jiao et al, 2011), Pentapetalae (Jiao et al, 2012), Salicaceae (Tuskan et al, 2006), Caryophyllales (Yang et al, 2018), Gossypium (Wendel, 2015)), including in legumes (e.g. Glycine, Genisteae, the Leucaena group, Vachellia), and more extensive sampling of recently diversified groups may well reveal a weaker pattern of clustering around the KPB.…”