Plants with double genomes might have had a better chance to survive the Cretaceous-Tertiary extinction event

Abstract

Most flowering plants have been shown to be ancient polyploids that have undergone one or more whole genome duplications early in their evolution. Furthermore, many different plant lineages seem to have experienced an additional, more recent genome duplication. Starting from paralogous genes lying in duplicated segments or identified in large expressed sequence tag collections, we dated these youngest duplication events through penalized likelihood phylogenetic tree inference. We show that a majority of these independent genome duplications are clustered in time and seem to coincide with the Cretaceous-Tertiary (KT) boundary. The KT extinction event is the most recent mass extinction caused by one or more catastrophic events such as a massive asteroid impact and/or increased volcanic activity. These events are believed to have generated global wildfires and dust clouds that cut off sunlight during long periods of time resulting in the extinction of approximately 60% of plant species, as well as a majority of animals, including dinosaurs. Recent studies suggest that polyploid species can have a higher adaptability and increased tolerance to different environmental conditions. We propose that polyploidization may have contributed to the survival and propagation of several plant lineages during or following the KT extinction event. Due to advantages such as altered gene expression leading to hybrid vigor and an increased set of genes and alleles available for selection, polyploid plants might have been better able to adapt to the drastically changed environment 65 million years ago.

Fig. 1.

Age distribution of the Arabidopsis paralogs based on K_S values. Age distributions for other plants can be found in SI Text (see Fig. S1). K_S represents the number of synonymous substitutions per site. The conspicuous peak around K_S = 0.6 originates from the youngest genome duplication in the Arabidopsis lineage.

Fig. 2.

ML fits of the duplicate age distributions of S. lycopersicum (calibration point AS120, with constraints, normal fit) (see Table S1 for an explanation of the terminology for the calibration points), M. truncatula (AV115, with constraints, gamma fit), O. sativa (AO145, with constraints, gamma fit), and G. hirsutum (AV115, with constraints, normal fit). The dashed line indicates the ML estimate of the distribution mode. The dotted lines delimit the corresponding 95% confidence intervals. Distributions for other plant species and constraints can be found in SI Text.

Fig. 3.

Phylogenetic tree of flowering plants (eudicots and monocots) for which the genome sequence has been determined or for which large EST collections are available. WGDs are indicated by green bars depicting the union of their 95% age confidence intervals calculated with various constraints (see Table S1). The dark green portions of the bars are centered on the best age estimates (see Table 1). Orange bars are WGD age estimates from literature. The WGD in poplar [here estimated by including Manihot (see Table S1)] has most probably occurred before its divergence of Salix, although dating by K_S values and phylogenetic means suggest a younger date, probably due to the slower evolutionary rate in trees (see text and SI Text for details). Blue bars denote the hexaploid nature of the ancestral eudicot genome (5, 26). The black dots indicate very recent polyploidy events, ≈1–2 mya in G. hirsutum, <10 mya in Solanum tuberosum, and 10–15 mya in Glycine max. The resulting tetraploids have not or only partially diploidized so far.