Multiple Paleopolyploidizations during the Evolution of the Compositae Reveal Parallel Patterns of Duplicate Gene Retention after Millions of Years

Abstract

Of the approximately 250,000 species of flowering plants, nearly one in ten are members of the Compositae (Asteraceae), a diverse family found in almost every habitat on all continents except Antarctica. With an origin in the mid Eocene, the Compositae is also a relatively young family with remarkable diversifications during the last 40 My. Previous cytologic and systematic investigations suggested that paleopolyploidy may have occurred in at least one Compositae lineage, but a recent analysis of genomic data was equivocal. We tested for evidence of paleopolyploidy in the evolutionary history of the family using recently available expressed sequence tag (EST) data from the Compositae Genome Project. Combined with data available on GenBank, we analyzed nearly 1 million ESTs from 18 species representing seven genera and four tribes. Our analyses revealed at least three ancient whole-genome duplications in the Compositae-a paleopolyploidization shared by all analyzed taxa and placed near the origin of the family just prior to the rapid radiation of its tribes and independent genome duplications near the base of the tribes Mutisieae and Heliantheae. These results are consistent with previous research implicating paleopolyploidy in the evolution and diversification of the Heliantheae. Further, we observed parallel retention of duplicate genes from the basal Compositae genome duplication across all tribes, despite divergence times of 33-38 My among these lineages. This pattern of retention was also repeated for the paleologs from the Heliantheae duplication. Intriguingly, the categories of genes retained in duplicate were substantially different from those in Arabidopsis. In particular, we found that genes annotated to structural components or cellular organization Gene Ontology categories were significantly enriched among paleologs, whereas genes associated with transcription and other regulatory functions were significantly underrepresented. Our results suggest that paleopolyploidy can yield strikingly consistent signatures of gene retention in plant genomes despite extensive lineage radiations and recurrent genome duplications but that these patterns vary substantially among higher taxonomic categories.

Prevalent Role of Gene Features in Determining Evolutionary Fates of Whole-Genome Duplication Duplicated Genes in Flowering Plants

“…However, studies on the Compositae (Asteraceae) lineage showed that duplicated genes generated by WGD were significantly enriched for genes associated with structural components or cellular organization, and regulatory and developmental genes such as transcription factors were significantly underrepresented. This pattern was almost consistent in all Compositae species investigated (Barker et al, 2008). Together, these observations suggest that some underlying mechanisms might have contributed to the evolutionary fates of duplicated genes derived from WGD events across divergent taxa, although selection forces might be varied substantially among higher taxonomic categories.…”

Contributions of Flowering Time Genes to Sunflower Domestication and Improvement

“…Recent gene family expansion has also been described for the FT/TFL1 family (Blackman et al 2010). Some of these expansions likely result from persistence of duplications that arose during polyploidy events at the base of the Compositae or, more recently, within the Heliantheae (Barker et al 2008). For example, values of K s , the synonymous substitution rate between two sequences, for sunflower duplicate pairs of ZTL and FKF1 were 0.71 and 0.66, respectively, consistent with the former event; K s was 0.45 for one of the duplication events in the sunflower FT clade, consistent with the latter event.…”

Fast Diploidization in Close Mesopolyploid Relatives ofArabidopsis

“…Several lineagespecific WGD events thus far documented across the angiosperms (Tang et al, 2008;Jaillon et al, 2009;Soltis et al, 2009) represent only the tip of the iceberg, as potential other WGD events remain uncovered. We envisage that more mesopolyploid WGDs will be revealed in Brassicaceae and other families, such as Asteraceae, where differently aged polyploidization events (Barker et al, 2008) and descending dysploidy have a prominent role in the genome evolution.…”

“…Multiple and often lineage-specific WGD events uncovered in Asteraceae (Barker et al, 2008), Cleomaceae Barker et al, 2009), Solanaceae (Schlueter et al, 2004), and other taxa (Soltis et al, 2009) imply a key role of WGDs in the evolution of land plants. The steadily improving knowledge of crucifer genome evolution suggests that the duplication-diploidization process is ongoing and occurred several times across the family.…”