A genome for gnetophytes and early evolution of seed plants

Abstract

Gnetophytes are an enigmatic gymnosperm lineage comprising three genera, Gnetum, Welwitschia and Ephedra, which are morphologically distinct from all other seed plants. Their distinctiveness has triggered much debate as to their origin, evolution and phylogenetic placement among seed plants. To increase our understanding of the evolution of gnetophytes, and their relation to other seed plants, we report here a high-quality draft genome sequence for Gnetum montanum, the first for any gnetophyte. By using a novel genome assembly strategy to deal with high levels of heterozygosity, we assembled >4 Gb of sequence encoding 27,491 protein-coding genes. Comparative analysis of the G. montanum genome with other gymnosperm genomes unveiled some remarkable and distinctive genomic features, such as a diverse assemblage of retrotransposons with evidence for elevated frequencies of elimination rather than accumulation, considerable differences in intron architecture, including both length distribution and proportions of (retro) transposon elements, and distinctive patterns of proliferation of functional protein domains. Furthermore, a few gene families showed Gnetum-specific copy number expansions (for example, cellulose synthase) or contractions (for example, Late Embryogenesis Abundant protein), which could be connected with Gnetum's distinctive morphological innovations associated with their adaptation to warm, mesic environments. Overall, the G. montanum genome enables a better resolution of ancestral genomic features within seed plants, and the identification of genomic characters that distinguish Gnetum from other gymnosperms. NATuRe PLANTS ArticlesNATurE PLANTs phylogenetic position of gnetophytes, with topologies differing depending on the type of sequence data (for example, plastid versus nuclear genes, nucleotide versus amino acid data) and analytical approach used (for example, maximum parsimony, maximum likelihood, Bayesian, multispecies coalescent based methods) [6][7][8] . Consequently, several possible hypotheses have been put forward that place gnetophytes as sister to (1) Pinaceae ('Gnepine' hypothesis); (2) cupressophytes ('Gnecup' hypothesis); (3) all conifers ('Gnetifer' hypothesis); (4) all other gymnosperms; or (5) all seed plants 9 . Currently, the emerging consensus, based on both older and more recent studies, and recently released data from the 1KP initiative (see https://sites.google.com/a/ualberta.ca/onekp/, and Wickett et al. 8 ), indicates that gnetophytes are sister to, or within, the conifers.So far, the availability of whole genome sequences for gymnosperms has been limited to conifers (specifically to Pinaceae) [10][11][12][13] and G. biloba 14 , with no whole genome assemblies available for the two remaining major seed plant lineages-cycads and gnetophytes. This deficiency, together with the conflicting phylogenetic evidence for relationships among these groups, is impeding our understanding of genome evolution across all seed plants. Here, we present a high-quality draft genome of Gnetum ...

Genic evidence that gnetophytes are sister to all other seed plants

“…Assuming so, there remains the potential for profound shifts in our understanding of the origin and divergence of many genetic, genomic, biochemical, metabolic and morphological characters in seed plant evolution. For example, the two paralogues GgWOXX and GgWOXY should be consider to have been lost in the their MRCA of other seed plants after the split with gnetophytes (Wan et al, 2018). And if gymnosperms may not be monophyletic, then many characters used to be considered to be derived in gnetophytes (Wan et al, 2018) may in fact be ancestral characters (Fig.…”

Insights on the persistence of pines (Pinusspecies) in the Late Cretaceous and their increasing dominance in the Anthropocene

“…Ectomycorrhizal associations were common in early gymnosperms, such as members of Gnetales and Cupressaceae. These turned out to be an apomor- (Gao & Lan, 2016;Wan et al, 2018).…”

“…Development of pine‐ectomycorrhizal associations coincides with diversification, establishment, and dominance of pines progressively at different stages in the history of its evolution. About 270 Myr ago in the Permian, gymnosperms in the families, Gnetaceae or Aurocariaceae, shifted habitat preferences toward mesic sites and their stress tolerance mechanisms became redundant (Gao & Lan, ; Wan et al., ). Ectomycorrhiza played an important role in the diversification of pines in the Late Cretaceous, particularly in extreme environments.…”

From genes to networks

“…The sequencing and assembly of high-quality 'platinum' genomes [6][7][8] further empowers plant scientists to pursue the details of genetic regulation and deepen our understanding of plant evolution. For example, in this issue, Wan and colleagues 9 report a high-quality draft genome of Gnetum montanum, a gymnosperm and the first sequenced species for gnetophytes. They revealed unique genomic features of this species that seem to place it closer to the basal lineage of angiosperms, indicating an early evolutionary path for seed plants.…”