Abstract

Ancient whole-genome duplications (WGDs)- paleopolyploidy events-are key to solving Darwin's 'abominable mystery' of how flowering plants evolved and radiated into a rich variety of species. The vertebrates also emerged from their invertebrate ancestors via two WGDs, and genomes of diverse gymnosperm trees, unicellular eukaryotes, invertebrates, fishes, amphibians and even a rodent carry evidence of lineage-specific WGDs. Modern polyploidy is common in eukaryotes, and it can be induced, enabling mechanisms and short-term cost-benefit assessments of polyploidy to be studied experimentally. However, the ancient WGDs can be reconstructed only by comparative genomics: these studies are difficult because the DNA duplicates have been through tens or hundreds of millions of years of gene losses, mutations, and chromosomal rearrangements that culminate in resolution of the polyploid genomes back into diploid ones (rediploidisation). Intriguing asymmetries in patterns of post-WGD gene loss and retention between duplicated sets of chromosomes have been discovered recently, and elaborations of signal transduction systems are lasting legacies from several WGDs. The data imply that simpler signalling pathways in the pre-WGD ancestors were converted via WGDs into multi-stranded parallelised networks. Genetic and biochemical studies in plants, yeasts and vertebrates suggest a paradigm in which different combinations of sister paralogues in the post-WGD regulatory networks are co-regulated under different conditions. In principle, such networks can respond to a wide array of environmental, sensory and hormonal stimuli and integrate them to generate phenotypic variety in cell types and behaviours. Patterns are also being discerned in how the post-WGD signalling networks are reconfigured in human cancers and neurological conditions. It is fascinating to unpick how ancient genomic events impact on complexity, variety and disease in modern life.

Highlights

  • Ancient whole-genome duplications (WGDs)—paleopolyploidy events—are key to solving Darwin’s ‘abominable mystery’ of how flowering plants evolved and radiated into a rich variety of species

  • Fast-forward to today’s exciting era of high-throughput genome sequencing, and phylogenomic maps assembled from multiple whole-genome sequences tell the evolutionary story with revised timelines: From the Carboniferous to early Cretaceous periods, the land was dominated by gymnosperms including the cycads, Ginkgo, and conifers that still flourish in subarctic forests[2]

  • The nuclear genomes of several gymnosperms have been sequenced recently, a heroic undertaking, given their exceptional size (10 to 40 gigabases) and high density of long terminal repeat (LTR)-retrotransposon repeats[3,4,5]. Within these genomes many non-overlapping duplicated chromosomal regions were identified that display gene synteny, meaning that their gene contents are similar to those of other chromosomal blocks within the same genome and across gymnosperm genomes. These gene synteny patterns and complementary transcriptome data support the hypothesis that the gymnosperms emerged from their common ancestor via a WGD named ζ that occurred an estimated 390 million years ago (Mya) during the Devonian period[6,7,8,9]

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Summary

Darwin CR

Murat F, Armero A, Pont C, et al.: Reconstructing the genome of the most recent common ancestor of flowering plants. Li Z, Baniaga AE, Sessa EB, et al.: Early genome duplications in conifers and other seed plants. Jiao Y, Wickett NJ, Ayyampalayam S, et al.: Ancestral polyploidy in seed plants and angiosperms. 9. Clark JW, Donoghue PC: Constraining the timing of whole genome duplication in plant evolutionary history. Amborella Genome Project: The Amborellagenome and the evolution of flowering plants. Philos Trans R Soc Lond B Biol Sci. 2010; 365(1539): 369–382.

15. Wolfe K
37. Otto SP
40. Comai L
45. Ploetz RC
48. Tsukaya H
67. Wolfe KH
Findings
99. Grant SG
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