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Prickly waterlily and rigid hornwort genomes shed light on early angiosperm evolution.

ABSTRACT: Angiosperms represent one of the most spectacular terrestrial radiations on the planet¹, but their early diversification and phylogenetic relationships remain uncertain^2-5. A key reason for this impasse is the paucity of complete genomes representing early-diverging angiosperms. Here, we present high-quality, chromosomal-level genome assemblies of two aquatic species-prickly waterlily (Euryale ferox; Nymphaeales) and the rigid hornwort (Ceratophyllum demersum; Ceratophyllales)-and expand the genomic representation for key sectors of the angiosperm tree of life. We identify multiple independent polyploidization events in each of the five major clades (that is, Nymphaeales, magnoliids, monocots, Ceratophyllales and eudicots). Furthermore, our phylogenomic analyses, which spanned multiple datasets and diverse methods, confirm that Amborella and Nymphaeales are successively sister to all other angiosperms. Furthermore, these genomes help to elucidate relationships among the major subclades within Mesangiospermae, which contain about 350,000 species. In particular, the species-poor lineage Ceratophyllales is supported as sister to eudicots, and monocots and magnoliids are placed as successively sister to Ceratophyllales and eudicots. Finally, our analyses indicate that incomplete lineage sorting may account for the incongruent phylogenetic placement of magnoliids between nuclear and plastid genomes.

SUBMITTER: Yang Y

PROVIDER: S-EPMC8075997 | biostudies-literature | 2020 Mar

REPOSITORIES: biostudies-literature

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Prickly waterlily and rigid hornwort genomes shed light on early angiosperm evolution.

Yang Yongzhi Y Sun Pengchuan P Lv Leke L Wang Donglei D Ru Dafu D Li Ying Y Ma Tao T Zhang Lei L Shen Xingxing X Meng Fanbo F Jiao Beibei B Shan Lanxing L Liu Man M Wang Qingfeng Q Qin Zhiji Z Xi Zhenxiang Z Wang Xiyin X Davis Charles C CC Liu Jianquan J

Nature plants 20200224 3

Angiosperms represent one of the most spectacular terrestrial radiations on the planet<sup>1</sup>, but their early diversification and phylogenetic relationships remain uncertain<sup>2-5</sup>. A key reason for this impasse is the paucity of complete genomes representing early-diverging angiosperms. Here, we present high-quality, chromosomal-level genome assemblies of two aquatic species-prickly waterlily (Euryale ferox; Nymphaeales) and the rigid hornwort (Ceratophyllum demersum; Ceratophyllal ...[more]

PMID: 32094642

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Project description:BackgroundChlamydiae are obligate intracellular bacteria of protists, invertebrates and vertebrates, but have not been found to date in photosynthetic eukaryotes (algae and embryophytes). Genes of putative chlamydial origin, however, are present in significant numbers in sequenced genomes of photosynthetic eukaryotes. It has been suggested that such genes were acquired by an ancient horizontal gene transfer from Chlamydiae to the ancestor of photosynthetic eukaryotes. To further test this hypothesis, an extensive search for proteins of chlamydial origin was performed using several recently sequenced algal genomes and EST databases, and the proteins subjected to phylogenetic analyses.ResultsA total of 39 proteins of chlamydial origin were retrieved from the photosynthetic eukaryotes analyzed and their identity verified through phylogenetic analyses. The distribution of the chlamydial proteins among four groups of photosynthetic eukaryotes (Viridiplantae, Rhodoplantae, Glaucoplantae, Bacillariophyta) was complex suggesting multiple acquisitions and losses. Evidence is presented that all except one of the chlamydial genes originated from an ancient endosymbiosis of a chlamydial bacterium into the ancestor of the Plantae before their divergence into Viridiplantae, Rhodoplantae and Glaucoplantae, i.e. more than 1.1 BYA. The chlamydial proteins subsequently spread through secondary plastid endosymbioses to other eukaryotes. Of 20 chlamydial proteins recovered from the genomes of two Bacillariophyta, 10 were of rhodoplant, and 10 of viridiplant origin suggesting that they were acquired by two different secondary endosymbioses. Phylogenetic analyses of concatenated sequences demonstrated that the viridiplant secondary endosymbiosis likely occurred before the divergence of Chlorophyta and Streptophyta.ConclusionWe identified 39 proteins of chlamydial origin in photosynthetic eukaryotes signaling an ancient invasion of the ancestor of the Plantae by a chlamydial bacterium accompanied by horizontal gene transfer. Subsequently, chlamydial proteins spread through secondary endosymbioses to other eukaryotes. We conclude that intracellular chlamydiae likely persisted throughout the early history of the Plantae donating genes to their hosts that replaced their cyanobacterial/plastid homologs thus shaping early algal/plant evolution before they eventually vanished.

Dataset Information

Prickly waterlily and rigid hornwort genomes shed light on early angiosperm evolution.

Publications

Prickly waterlily and rigid hornwort genomes shed light on early angiosperm evolution.

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