The Amborella Genome and the Evolution of Flowering Plants

Introduction Darwin famously characterized the rapid rise and early diversification of flowering plants (angiosperms) in the fossil record as an “abominable mystery. ” Identifying genomic changes that accompanied the origin of angiosperms is key to unraveling the molecular basis of biological innovations that contributed to their geologically near-instantaneous rise to ecological dominance. Amborella trichopoda, an understory shrub endemic to New Caledonia, is the sole surviving sister species of all other living flowering plants (angiosperms). The Amborella genome provides an exceptional reference for inferring features of the first flowering plants and identifies an ancient angiosperm-wide whole-genome duplication (red star). Amborella flowers have spirally arranged tepals, unfused carpels (female; shown), and laminar stamens. Amborella trichopoda, an understory shrub endemic to New Caledonia, is the sole surviving sister species of all other living flowering plants (angiosperms). The Amborella genome provides an exceptional reference for inferring features of the first flowering plants and identifies an ancient angiosperm-wide whole-genome duplication (red star). Amborella flowers have spirally arranged tepals, unfused carpels (female; shown), and laminar stamens. Methods We provide a draft genome for Amborella trichopoda, the single living representative of the sister lineage to all other extant flowering plants and use phylogenomic and comparative genomic analyses to elucidate ancestral gene content and genome structure in the most recent common ancestor of all living angiosperms. Results We reveal that an ancient genome duplication predated angiosperm diversification. However, unlike all other sequenced angiosperm genomes, the Amborella genome shows no evidence of more recent, lineage-specific genome duplications, making Amborella particularly well suited to help interpret genomic changes after polyploidy in other angiosperms. The remarkable conservation of gene order (synteny) among the genomes of Amborella and other angiosperms has enabled reconstruction of the ancestral gene arrangement in eudicots (~75% of all angiosperms). An ancestral angiosperm gene set was inferred to contain at least 14,000 protein-coding genes; subsequent changes in gene content and genome structure across disparate flowering plant lineages are associated with the evolution of important crops and model species. Relative to nonangiosperm seed plants, 1179 gene lineages first appeared in association with the origin of the angiosperms. These include genes important in flowering, wood formation, and responses to environmental stress. Unlike other angiosperms, the Amborella genome lacks evidence for recent transposon insertions while retaining ancient and divergent transposons. The genome harbors an abundance of atypical lineage-specific 24-nucleotide microRNAs, with at least 27 regulatory microRNA families inferred to have been present in the ancestral angiosperm. Population genomic analysis of 12 individuals from across the small native range of Amborella in New Caledonia reveals geographic structure with conservation implications, as well as both a recent genetic bottleneck and high levels of genome diversity. Discussion The Amborella genome is a pivotal reference for understanding genome and gene family evolution throughout angiosperm history. Genome structure and phylogenomic analyses indicate that the ancestral angiosperm was a polyploid with a large constellation of both novel and ancient genes that survived to play key roles in angiosperm biology. Shaping Plant Evolution Amborella trichopoda is understood to be the most basal extant flowering plant and its genome is anticipated to provide insights into the evolution of plant life on Earth (see the Perspective by Adams). To validate and assemble the sequence, Chamala et al. (p. 1516) combined fluorescent in situ hybridization (FISH), genomic mapping, and next-generation sequencing. The Amborella Genome Project (p. 10.1126/science.1241089) was able to infer that a whole-genome duplication event preceded the evolution of this ancestral angiosperm, and Rice et al. (p. 1468) found that numerous genes in the mitochondrion were acquired by horizontal gene transfer from other plants, including almost four entire mitochondrial genomes from mosses and algae. The Amborella genome retains features of the ancestral angiosperm and illuminates flowering plant genomic evolution. Amborella trichopoda is strongly supported as the single living species of the sister lineage to all other extant flowering plants, providing a unique reference for inferring the genome content and structure of the most recent common ancestor (MRCA) of living angiosperms. Sequencing the Amborella genome, we identified an ancient genome duplication predating angiosperm diversification, without evidence of subsequent, lineage-specific genome duplications. Comparisons between Amborella and other angiosperms facilitated reconstruction of the ancestral angiosperm gene content and gene order in the MRCA of core eudicots. We identify new gene families, gene duplications, and floral protein-protein interactions that first appeared in the ancestral angiosperm. Transposable elements in Amborella are ancient and highly divergent, with no recent transposon radiations. Population genomic analysis across Amborella’s native range in New Caledonia reveals a recent genetic bottleneck and geographic structure with conservation implications.