ERSPECtIVes Box 1 Whole-genome duplications across the phylogeny of eukaryotes Angiosperms Animals Fungi 铺 Cenozoic Cretaceous Monocots ore)Eudicots 145 mya Ascomycetes Devonian 409 mya vertebrates Angiosperms-moss split ebrates split Cambrian Precambrian Whole-genome duplications (WGDs)seem to have been followed by a Similarly, early polyploidization events in one or more angiosperm plant lbstantial increase in morphological complexity (see the figure, lineages might explain the rapid rise and diversification of angiosperms paleopolyploidy events are indicated as red bars and are based on studies in the Early Cretaceous period 240. Fundamental innovations that published previously for plants 6, 24, fish2,5556, vertebrates, fungi and occurred early in angiosperm evolution are the invention of the closed ciliates"). The two rounds of genome duplication(1R and 2R)in the carpel, and the emergence of flowers and of double fertilization.These vertebrate stem were followed by a period of rapid morphological early innovations were elaborated specialized pollination n, which led to: enhanced nervous, endocrine and circulatory strategies and fruits. The evolution of xylem vessels is also believed stems; enhanced sensory organs; more complex brains; and the skull, have been important in early erm diversification, but their origin vertebrae, the endoskeleton and teeth. These were followed in the is less clear. Some basal angiosperms, such as Amborella spp, lack vessels, jawed vertebrate lineage by innovations such as paired appendages, hinged whereas vessel structures have been discovered in members of the 0o2-l0s. Many of these innovations are Gnetales order and in ferns. 0. However, the diversity of vasculature related to the emergence in vertebrates of the neural cresto. Since Ohno in at rms is unparallelled. The timing of the early angiosperm first suggested that these innovations are facilitated by genome polyploidizations is unclear. It is possible that they contributed to the duplications", a causal link between the 2R duplication and the emergence elaboration and diversification of the afe of vertebrates has been suggested (see, for example, REFS 78, 107) than to their establishment 22009 Macmillan Publishers Limited All rights reservedNature Reviews | Genetics Land vertebrates Angiosperms–moss split Fish–land vertebrates split Teleosts Ascomycetes 3R 2R 1R Fish Angiosperms Moss Animals Fungi Ciliates Cenozoic Cretaceous Jurassic Triassic Permian Carboniferous Devonian Silurian Ordovician Cambrian Precambrian Physcomitrella patens Kluyveromyces lactis Paramecium spp. Tetrahymena spp. Lampreys Hagfish Neurospora crassa Aspergillus fumigatus Acorus americanus Sor Zea mays ghum bicolor Oryza sativa Hordeum vulgare Triticum aestivum Musa spp. Eschscholzia californica Arabidopsis thaliana Carica papaya Gossypium hirsutum Populus trichocarpa Medic Glycine max ago truncatula Vitis vinif Lotus japonicus era Lactuca sativa Centaurea solstitialis Solanum lycopersicum Solanum tuberosum Bichir (Polypteriformes) T Medaka akifugu rubripes Zebrafish Bony tongues (Osteoglossiformes) Gar (Semionotiformes) Sturgeon (Acipenseriformes) Mammals Amphibi Lobe-finned fish a Birds Saccharomyces cerevisiae Saccharomyces spp. Candida glabrata Monocots (Core) Eudicots 65 mya 145 mya 208 mya 245 mya 290 mya 363 mya 409 mya 439 mya 510 mya 542 mya >542 mya Box 1 | Whole-genome duplications across the phylogeny of eukaryotes Whole-genome duplications (WGDs) seem to have been followed by a substantial increase in morphological complexity (see the figure, paleopolyploidy events are indicated as red bars and are based on studies published previously for plants3,16,24, fish20,55,56, vertebrates101, fungi17 and ciliates9 ). The two rounds of genome duplication (1R and 2R) in the vertebrate stem were followed by a period of rapid morphological innovation, which led to: enhanced nervous, endocrine and circulatory systems; enhanced sensory organs; more complex brains; and the skull, vertebrae, the endoskeleton and teeth. These were followed in the jawed vertebrate lineage by innovations such as paired appendages, hinged jaws and an adaptive immune system40,102–105. Many of these innovations are related to the emergence in vertebrates of the neural crest40,102. Since Ohno first suggested that these innovations are facilitated by genome duplications106, a causal link between the 2R duplication and the emergence of vertebrates has been suggested (see, for example, REFS 78,107). Similarly, early polyploidization events in one or more angiosperm plant lineages might explain the rapid rise and diversification of angiosperms in the Early Cretaceous period6,11,13,14,52,108. Fundamental innovations that occurred early in angiosperm evolution are the invention of the closed carpel, and the emergence of flowers and of double fertilization109. These early innovations were elaborated on to create specialized pollination strategies and fruits. The evolution of xylem vessels is also believed to have been important in early angiosperm diversification85, but their origin is less clear. Some basal angiosperms, such as Amborella spp., lack vessels, whereas vessel structures have been discovered in members of the Gnetales order and in ferns85,110,111. However, the diversity of vasculature in angiosperms is unparallelled. The timing of the early angiosperm polyploidizations is unclear. It is possible that they contributed to the elaboration and diversification of the aforementioned inventions rather than to their establishment. Pers P ectives 726 | oCToBEr 2009 | voluME 10 www.nature.com/reviews/genetics © 2009 Macmillan Publishers Limited. All rights reserved