Angiosperms, also known as flowering plants, represent the most diverse group of seed plants, and their origin and evolution have long been a central question in plant evolutionary biology. Whole-genome duplication (WGD, or polyploidization) is considered to have played a key role in the origin and trait evolution of both seed plants and angiosperms. However, detecting these ancient WGD events is technically challenging, as their genomic signatures are often obscured by subsequent gene loss, chromosomal rearrangements, and synonymous substitution saturation during rediploidization. 

In 2011, Jiao et al. proposed two independent ancestral WGD events-denoted as the ζ event in seed plants and the ε event in angiosperms-based on a bimodal age distribution of gene duplications predating the monocot-eudicot divergence. However, in 2017, Ruprecht et al. suggested that this bimodal signal might result from methodological artifacts, specifically inconsistent calibration of phylogenetic nodes used in molecular dating, rather than reflecting true evolutionary events, leaving the issue unresolved.

To clarify the ancient WGD history of seed plants and angiosperms, researchers from the Wuhan Botanical Garden (Chinese Academy of Sciences) and Ghent University introduced dosage-sensitive genes as evolutionary markers for detecting ancient WGDs. These genes often encode core components of protein complexes, signaling pathways, or regulatory networks. Changes in their expression dosage can disrupt cellular stoichiometric balance, making them preferentially retained after WGDs. 

The researchers analyzed orthologous gene groups (OGs) from angiosperms with different WGD histories and quantified their relative dosage sensitivity using correlation coefficients between observed OG copy numbers and expected post-WGD copy numbers. Based on these correlations, OGs were classified into four groups (A to D), from highest (A) to lowest (D) sensitivity. 

The study confirmed that highly dosage-sensitive OGs (Group A) exhibit stronger purifying selection, more protein-protein interactions, broader tissue expression, and clearer Ks peaks corresponding to known WGDs, validating their utility as reliable WGD markers.

Using these dosage-sensitive OGs, the researchers integrated gene tree-species tree reconciliation, gene copy number correlation analysis, and probabilistic retention modeling to test competing WGD scenarios. Two early-diverging angiosperms, Amborella trichopoda and Aristolochia fimbriata, which lack post-angiosperm WGDs, were selected as key lineages. 

Results revealed only one prominent ancient duplication peak, corresponding to the ancestral seed plant WGD (ζ event). In contrast, the signal for a putative angiosperm-specific WGD (ε event) was extremely weak, with duplication node ratios significantly lower than theoretical expectations. 

Both correlation analysis and probabilistic modeling further indicated very low retention rates for the ε event among dosage-sensitive OGs, failing to support its status as an independent WGD. Thus, evolutionary patterns of dosage-sensitive genes support a single ancestral WGD in seed plants, with no additional WGD occurring during ancestral angiosperm evolution.

This study, titled“Revisiting ancient whole-genome duplications in the seed and flowering plants through the lens of dosage-sensitive genes,” was published in Science Advances by corresponding authors SHI Tao (Wuhan Botanical Garden, CAS) and Yves Van de Peer (Ghent University).