The evolution of multi-gene families and metabolic pathways in the evening primroses (Oenothera: Onagraceae): A comparative transcriptomics approach

• Published in: PloS one Vol. 17; no. 6; p. e0269307
• Main Authors: Kariñho-Betancourt, Eunice, Carlson, David, Hollister, Jessie, Fischer, Axel, Greiner, Stephan, Johnson, Marc T J
• Format: Journal Article
• Language: English
• Published: United States Public Library of Science 24.06.2022; Public Library of Science (PLoS)
• Subjects: Ammonia; Analysis; Biology and Life Sciences; Cell metabolism; Chloroplasts; Chromosomes; Comparative studies; Computer and Information Sciences; Datasets; Enzymes; Evolution; Evolution & development; Evolution, Molecular; Evolutionary genetics; Flavonoids; Gene expression; Gene families; Genes; Genetic aspects; Genetics; Genomes; Genomics; Heterogeneity; Metabolic Networks and Pathways; Metabolic pathways; Metabolism; Metabolites; Molecular evolution; Multigene Family; Mutation; Oenothera; Oenothera - genetics; Oenothera biennis - genetics; Onagraceae; Phenolic compounds; Phenols; Phenylalanine; Phenylalanine ammonia-lyase; Phylogeny; Physical Sciences; Plant biology; Plant genetics; Plastids; Primroses; Seeds; Taxonomy; Transcriptome; Transcriptomes; Transcriptomics; United States
• ISSN: 1932-6203; 1932-6203
• DOI: 10.1371/journal.pone.0269307

The plant genus Oenothera has played an important role in the study of plant evolution of genomes and plant defense and reproduction. Here, we build on the 1kp transcriptomic dataset by creating 44 new transcriptomes and analyzing a total of 63 transcriptomes to present a large-scale comparative study across 29 Oenothera species. Our dataset included 30.4 million reads per individual and 2.3 million transcripts on average. We used this transcriptome resource to examine genome-wide evolutionary patterns and functional diversification by searching for orthologous genes and performed gene family evolution analysis. We found wide heterogeneity in gene family evolution across the genus, with section Oenothera exhibiting the most pronounced evolutionary changes. Overall, more significant gene family expansions occurred than contractions. We also analyzed the molecular evolution of phenolic metabolism by retrieving proteins annotated for phenolic enzymatic complexes. We identified 1,568 phenolic genes arranged into 83 multigene families that varied widely across the genus. All taxa experienced rapid phenolic evolution (fast rate of genomic turnover) involving 33 gene families, which exhibited large expansions, gaining about 2-fold more genes than they lost. Upstream enzymes phenylalanine ammonia-lyase (PAL) and 4-coumaroyl: CoA ligase (4CL) accounted for most of the significant expansions and contractions. Our results suggest that adaptive and neutral evolutionary processes have contributed to Oenothera diversification and rapid gene family evolution.