The Amborella Genome and the Evolution of Flowering Plants
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.
Structured Abstract
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.
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.
Abstract
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.
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Supplementary Material
Summary
Text
Figs. S1 to S42
Tables S1 to S46
Additional Acknowledgment
References
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References and Notes
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Science
Volume 342 | Issue 6165
20 December 2013
20 December 2013
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Copyright © 2013, American Association for the Advancement of Science.
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Published in print: 20 December 2013
Acknowledgments
Sequencing reads, reference genome assembly, and gene annotations of Amborella trichopoda are available from NCBI (BioProject PRJNA212863). The Amborella genome is also available in CoGe (http://genomevolution.org/CoGe/) and at the Amborella Genome Database (http://www.amborella.org), where additional tools for comparative genomic analysis are available. This work was funded by the NSF Plant Genome Research Program (grant 0922742) to C.W.D., H.M., W.B.B., P.S.S., D.E.S., V.A.A., J.L.-M., S.R.W., J.D.P., and S.R., with additional funding from NSF’s iPlant Collaborative to P.S.S. and D.E.S. Author contributions are included in the Supplementary Materials.
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