Abstract

Green plants (Viridiplantae) include around 450,000–500,000 species1,2 of great diversity and have important roles in terrestrial and aquatic ecosystems. Here, as part of the One Thousand Plant Transcriptomes Initiative, we sequenced the vegetative transcriptomes of 1,124 species that span the diversity of plants in a broad sense (Archaeplastida), including green plants (Viridiplantae), glaucophytes (Glaucophyta) and red algae (Rhodophyta). Our analysis provides a robust phylogenomic framework for examining the evolution of green plants. Most inferred species relationships are well supported across multiple species tree and supermatrix analyses, but discordance among plastid and nuclear gene trees at a few important nodes highlights the complexity of plant genome evolution, including polyploidy, periods of rapid speciation, and extinction. Incomplete sorting of ancestral variation, polyploidization and massive expansions of gene families punctuate the evolutionary history of green plants. Notably, we find that large expansions of gene families preceded the origins of green plants, land plants and vascular plants, whereas whole-genome duplications are inferred to have occurred repeatedly throughout the evolution of flowering plants and ferns. The increasing availability of high-quality plant genome sequences and advances in functional genomics are enabling research on genome evolution across the green tree of life.

Highlights

  • Phylogenomic approaches are widely used to resolve species relationships[5] as well as the evolution of genomes, gene families and gene function[6]

  • Our findings suggest that extensive gene-family expansions or genome duplications preceded the evolution of major innovations in the history of green plants

  • Article a b c d e f g h i j k l m n o p are limitations to the inference of whole-genome duplications (WGDs) events using this approach, we found that comparisons of these results with 65 overlapping published genome-based WGD inferences revealed 6 false-negative results in our tree-based estimates and no false-positive results (Supplementary Table 2)

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Summary

One Thousand Plant Transcriptomes Initiative

Green plants (Viridiplantae) include around 450,000–500,000 species[1,2] of great diversity and have important roles in terrestrial and aquatic ecosystems. Viridiplantae comprise an estimated 450,000–500,000 species[1,2], encompass a high level of diversity and evolutionary timescales[3], and have important roles in all terrestrial and most aquatic ecosystems. This ecological diversity derives from developmental, morphological and physiological innovations that enabled the colonization and exploitation of novel and emergent habitats. We evaluated gene history discordance among single-copy genes This is expected in the face of rapid species diversification, owing to incomplete sorting of ancestral variation between speciation events[7]. Our findings suggest that extensive gene-family expansions or genome duplications preceded the evolution of major innovations in the history of green plants

Integrated analysis of genome evolution
Primary acquisition of the plastid
The history of Viridiplantae
Glaucophytes Rhodophytes Outgroup
Santalales Vitales Saxifragales Core rosids
Ferns and lycophytes b Bryophytes
Mean number of inferred WGDs in the ancestry of each species
Fold changes of expansions and contractions
Online content
Methods
Phylogeny reconstruction
Code availability
Reporting Summary
Statistical parameters
Data collection Data analysis
Findings
Data exclusions
Full Text
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