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Reticulate evolution in eukaryotes: Origin and evolution of the nitrate assimilation pathway.

ABSTRACT: Genes and genomes can evolve through interchanging genetic material, this leading to reticular evolutionary patterns. However, the importance of reticulate evolution in eukaryotes, and in particular of horizontal gene transfer (HGT), remains controversial. Given that metabolic pathways with taxonomically-patchy distributions can be indicative of HGT events, the eukaryotic nitrate assimilation pathway is an ideal object of investigation, as previous results revealed a patchy distribution and suggested that the nitrate assimilation cluster of dikaryotic fungi (Opisthokonta) could have been originated and transferred from a lineage leading to Oomycota (Stramenopiles). We studied the origin and evolution of this pathway through both multi-scale bioinformatic and experimental approaches. Our taxon-rich genomic screening shows that nitrate assimilation is present in more lineages than previously reported, although being restricted to autotrophs and osmotrophs. The phylogenies indicate a pervasive role of HGT, with three bacterial transfers contributing to the pathway origin, and at least seven well-supported transfers between eukaryotes. In particular, we propose a distinct and more complex HGT path between Opisthokonta and Stramenopiles than the one previously suggested, involving at least two transfers of a nitrate assimilation gene cluster. We also found that gene fusion played an essential role in this evolutionary history, underlying the origin of the canonical eukaryotic nitrate reductase, and of a chimeric nitrate reductase in Ichthyosporea (Opisthokonta). We show that the ichthyosporean pathway, including this novel nitrate reductase, is physiologically active and transcriptionally co-regulated, responding to different nitrogen sources; similarly to distant eukaryotes with independent HGT-acquisitions of the pathway. This indicates that this pattern of transcriptional control evolved convergently in eukaryotes, favoring the proper integration of the pathway in the metabolic landscape. Our results highlight the importance of reticulate evolution in eukaryotes, by showing the crucial contribution of HGT and gene fusion in the evolutionary history of the nitrate assimilation pathway.

SUBMITTER: Ocana-Pallares E

PROVIDER: S-EPMC6400420 | biostudies-literature | 2019 Feb

REPOSITORIES: biostudies-literature

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Reticulate evolution in eukaryotes: Origin and evolution of the nitrate assimilation pathway.

Ocaña-Pallarès Eduard E Najle Sebastián R SR Scazzocchio Claudio C Ruiz-Trillo Iñaki I

PLoS genetics 20190221 2

Genes and genomes can evolve through interchanging genetic material, this leading to reticular evolutionary patterns. However, the importance of reticulate evolution in eukaryotes, and in particular of horizontal gene transfer (HGT), remains controversial. Given that metabolic pathways with taxonomically-patchy distributions can be indicative of HGT events, the eukaryotic nitrate assimilation pathway is an ideal object of investigation, as previous results revealed a patchy distribution and sugg ...[more]

PMID: 30789903

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Project description:BackgroundThe thirteen species of Dryopteris in North America have long been suspected of having undergone a complicated history of reticulate evolution via allopolyploid hybridization. Various explanations for the origins of the allopolyploid taxa have been suggested, and though most lines of evidence have supported the so-called "semicristata" hypothesis, contention over the group's history has continued in several recent, conflicting studies.ResultsSequence data from nine plastid and two nuclear markers were collected from 73 accessions representing 35 species of Dryopteris. Sequences from each of the allopolyploids are most closely related to their progenitor species as predicted by the "semicristata" hypothesis. Allotetraploid D. campyloptera appears to be derived from a hybrid between diploid D. expansa and D. intermedia; D. celsa, from diploid D. ludoviciana x D. goldiana; and D. carthusiana and D. cristata, from diploid "D. semicristata" x D. intermedia and D. ludoviciana, respectively. Allohexaploid D. clintoniana appears to be derived from D. cristata x D.goldiana. The earliest estimated dates of formation of the allopolyploids, based on divergence time analyses, were within the last 6 Ma. We found no evidence for recurrent formation of any of the allopolyploids. The sexual allopolyploid taxa are derived from crosses between parents that show intermediate levels of genetic divergence relative to all pairs of potential progenitors. In addition, the four allotetraploids are transgressive with respect to geographic range relative to one or both of their parents (their ranges extend beyond those of the parents), suggesting that ecological advantages in novel habitats or regions may promote long-term regional coexistence of the hybrid taxa with their progenitors.ConclusionsThis study provides the first thorough evaluation of the North American complex of woodferns using extensive sampling of taxa and genetic markers. Phylogenies produced from each of three datasets (one plastid and two nuclear) support the "semicristata" hypothesis, including the existence of a missing diploid progenitor, and allow us to reject all competing hypotheses. This study demonstrates the value of using multiple, biparentally inherited markers to evaluate reticulate complexes, assess the frequency of recurrent polyploidization, and determine the relative importance of introgression vs. hybridization in shaping the histories of such groups.

Dataset Information

Reticulate evolution in eukaryotes: Origin and evolution of the nitrate assimilation pathway.

Publications

Reticulate evolution in eukaryotes: Origin and evolution of the nitrate assimilation pathway.

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