Dosage-sensitive genes suggest no whole-genome duplications in ancestral angiosperm

(Press-News.org) 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 widely recognized as a key driver of the origin and trait evolution of both seed plants and angiosperms. Detecting these ancient WGD events, however, is technically challenging, as their genomic signatures are often obscured by subsequent gene loss, chromosomal rearrangements, and synonymous substitution saturation during rediploidization.

In 2011, based on a bimodal age distribution of gene duplications that predate the monocot–eudicot divergence, researchers proposed two independent ancestral WGD events—the ζ event in seed plants and the ε event in angiosperms. However, a 2017 study challenged this conclusion, positing that the observed bimodal signal might be a product of methodological artifacts rather than a reflection of genuine evolutionary processes. Specifically, the inconsistency in calibrating phylogenetic nodes for molecular dating was identified as a key confounding factor. This discrepancy has thus far kept the issue unresolved.

To clarify the ancient WGD history of seed plants and angiosperms, researchers from the Wuhan Botanical Garden of the Chinese Academy of Sciences and Ghent University introduced dosage-sensitive genes as evolutionary markers for detecting ancient WGDs. These genes typically 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.

Their findings were published in Science Advances on January 2.

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), ranging from highest sensitivity (Group A) to lowest (Group D).

The study confirmed that highly dosage-sensitive OGs (Group A) exhibit stronger purifying selection, more protein–protein interactions, broader tissue expression profiles, 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 for the analysis.

Results revealed only one prominent ancient duplication peak, corresponding to the ancestral seed plant WGD (ζ event). In contrast, the signal for the 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 of the ε event among dosage-sensitive OGs, failing to support its status as an independent WGD. Thus, the evolutionary patterns of dosage-sensitive genes support the existence of a single ancestral WGD in seed plants, with no additional WGD occurring during the evolution of ancestral angiosperms.

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