Genomic evidence for rediploidization and adaptive evolution following the whole-genome triplication

Abstract

Whole-genome duplication (WGD), or polyploidy, events are widespread and significant in the evolutionary history of angiosperms. However, empirical evidence for rediploidization, the major process where polyploids give rise to diploid descendants, is still lacking at the genomic level. Here we present chromosome-scale genomes of the mangrove tree Sonneratia alba and the related inland plant Lagerstroemia speciosa. Their common ancestor has experienced a whole-genome triplication (WGT) approximately 64 million years ago coinciding with a period of dramatic global climate change. Sonneratia, adapting mangrove habitats, experienced extensive chromosome rearrangements post-WGT. We observe the WGT retentions display sequence and expression divergence, suggesting potential neo- and sub-functionalization. Strong selection acting on three-copy retentions indicates adaptive value in response to new environments. To elucidate the role of ploidy changes in genome evolution, we improve a model of the polyploidization-rediploidization process based on genomic evidence, contributing to the understanding of adaptive evolution during climate change.

Fig. 1. Genomic architecture of Sonneratia alba and relatives.

a Hi-C interactive heatmap of the genome-wide organization of S. alba. The deeper red means the stronger interaction between the DNA regions. Chr: chromosome. b Circos plot of the S. alba and L. speciosa genomes. Concentric circles, from outer to inner, show (1) pseudo-chromosome (Mb), (2) gene density, (3) GC content (34.01–57.76% per 200 Kb), and (4) syntenic block. Source data are provided as a Source Data file.

Fig. 2. The whole-genome triplication (WGT) event is shared in S. alba and L. speciosa.

a Phylogenetic tree of seven eudicots, including S. alba and relatives. Blue node bars are 95% confidence intervals. Red nodes indicate two fossil calibration nodes. The star represents the WGT event. The occurrences of the K-Pg boundary and PETM are indicated by the arrows on the timeline. b Ks distribution between paralogous genes within the same species and orthologous genes from pairs of species. c Synteny between the homologous regions of S. alba (red), L. speciosa (pink), and P. granatum (green). It reflects the overall synteny relationship with a 3:1 ratio between S. alba vs. P. granatum, L. speciosa vs. P. granatum, respectively. The representation showcases partial regions of the genomes. d Numbers of homologous gene groups supporting different scenarios on the order of speciation and WGT events in Sonneratia and Lagerstroemia. e Chromosome evolution following WGT from the ALK (the ancestral Lythraceae karyotype). The star represents the WGT event. f Macrosynteny patterns among the three Lythraceae plants. “sal” represents S. alba, “pgr” represents P. granatum, and “lsp” represents L. speciosa.

Fig. 3. A model of the polyploidization–rediploidization process in plants during global climate change.

a Whole-genome triplication (γ-WGT and α^S-WGT) events coincide with dramatic global climate changes. The sea level rise, massive extinction, and WGT event might provide the opportunity for the offshore woody plants to survive, leading to the emergence of the mangrove. The images portray the prevalent environments during various periods. In the Early Cretaceous (around 120 Mya), an arid climate prevailed. At the K-Pg boundary (around 66 Mya), the dramatic global climate change following a significant asteroid collision with Earth. During the PETM (around 55 Mya), there was a notable global temperature increase and a rise in eustatic sea levels. Finally, the image depicts the current environment. The cartoon elements have been sourced and modified from materials contributed by Christine Thurber, Dieter Tracey, Jane Hawkey, Jane Thomas, and Tracey Saxby (available in the IAN Image Library at https://ian.umces.edu/media-library/) under a CC BY-SA 4.0 License. Detailed credits for these cartoon materials can be found in Supplementary Data 2. b A hypothetical model of polyploidization–rediploidization process. The initial diploid genome experiences whole-genome triplication around the period of dramatic global environment and climate change. Polyploidy may persist during this period. Rediploidization post polyploidization is a major process for polyploids, driving the genome toward a diploid state through divergence of homologous genes in terms of sequence and expression, redundancy reductions, and large chromosome rearrangements such as fusion and fission events. The round of polyploidization and rediploidization process is widespread in angiosperms. The brown chromosomes represent homologous chromosomes, while the red and blue chromosomes represent significantly diverged chromosomes. The yellow bands indicate regions derived from other ancestral chromosomes through chromosomal rearrangements.

Fig. 4. Natural selection patterns among different-copy retention groups.

a The inferred distribution of fitness effects (N_es), proportion of adaptive divergence (α), and rate of adaptive substitution relative to neutral divergence (ω_a) for different-copy retention groups generated by the WGT event. Each distribution was estimated based on 200 bootstrap replicates. Traditional MK test with fixation index (b), constraint effect (c), and selection effect (d) for these different-copy retention groups. The two-tailed t test was applied to test for all pairwise differences. P-values are indicated by single asterisks (P-value < 0.05) or triple asterisks (P-value < 0.001). I* (P-value = 3.9 × 10⁻²), II*** (P-value = 4.5 × 10⁻⁴), III* (P-value = 1.6 × 10⁻²), VI*** (P-value = 8.3 × 10⁻⁴), IV***, V***, VII***, VIII***, and IX*** (P-value < 1 × 10⁻¹⁵) represent the significantly different values for pairwise comparisons between groups. Box edges indicate upper and lower quartiles, centerlines indicate median values, and whiskers extend to 1.5 times the interquartile range. The number of genes in each retention group (one-copy, two-copy, and three-copy) was 3439, 4832, and 1171, respectively. Source data are provided as a Source Data file.

Fig. 5. The pathway of root development and salt tolerance in S. alba.

Salt modulates root growth direction by causing asymmetric auxin distribution and reducing the gravity response. Several genes may together facilitate the erect lateral branches of the horizontal roots and shape the pneumatophores. The duplicates with at least one copy up-regulated under high salt conditions, related to salt tolerance, are shown on the right. These genes are WGT retained duplicates and detailed three-copy retention groups are listed in Supplementary Data 4.