Tao Wan, Zhiming Liu, Qingfeng Wang

Nature Communications volume 12, Article number: 4247 (2021); Published12 July 2021

ABSTRACT

The gymnosperm Welwitschia mirabilis belongs to the ancient, enigmatic gnetophyte lineage. It is a unique desert plant with extreme longevity and two ever-elongating leaves. We present a chromosome-level assembly of its genome (6.8 Gb/1 C) together with methylome and transcriptome data to explore its astonishing biology. We also present a refined, high-quality assembly of Gnetum montanum to enhance our understanding of gnetophyte genome evolution. The Welwitschia genome has been shaped by a lineage-specific ancient, whole genome duplication (~86 million years ago) and more recently (1-2 million years) by bursts of retrotransposon activity. High levels of cytosine methylation (particularly at CHH motifs) are associated with retrotransposons, whilst long-term deamination has resulted in an exceptionally GC-poor genome. Changes in copy number and/or expression of gene families and transcription factors (e.g. R2R3MYB, SAUR) controlling cell growth, differentiation and metabolism underpin the plant’s longevity and tolerance to temperature, nutrient and water stress.

See: https://www.nature.com/articles/s41467-021-24528-4

Fig. 2: Genome evolutionary history of Welwitschia.

a A circos plot showing the inter-genomic collinearity analysis between the Welwitschia and Gnetum genomes. From outside to inside, each track shows (1) one-to-one orthologous collinear regions between the two genomes with colors showing their orthologs on different chromosomes in the other species; (2) the chromosomes of Welwitschia in black and Gnetum in colors; (3) the coverage of tandem repeats in a 5 Mbp window with green and red bars showing above or below the mean coverage of tandem repeats across the genome for Welwitschia (standard deviation in gray), respectively; (4) the coverage of long terminal repeats (LTRs) in a 5 Mbp window with light green and light red bars showing above or below the mean coverage of tandem repeats across the genome (standard deviation in gray), respectively; and (5) paralogous collinear regions in the Welwitschia genome with at least five anchor pairs. The bands denote collinear regions where one region in Gnetum corresponds to two orthologous regions in Welwitschia. b Two examples illustrating one segment in Gnetum corresponding to two paralogous segments in Welwitschia. Genes in light gray are non-homologs. Genes with the same colors are homologs and homologous genes are connected with dark gray bands when the two segments are alongside. c Distributions of synonymous substitutions per synonymous site (K_S) for the whole paranome of Welwitschia (light gray histogram and dark gray line). The y axis on the left shows the number of retained duplicates and there is a small peak at K_S of 1, which represents a WGD event. The y axis on the right shows the orthologue density between the two species. For one-to-one orthologs between Welwitschia – Gnetum and Welwitschia – Ginkgo (color-filled curves of kernel-density estimates) the peaks represent species divergence events and K_S values correspond with the degree of orthologue divergence. The K_S values for anchor pairs from collinear regions are indicated in orange (left y axis). The pale gray rectangle highlights the K_S regions in which the paralogous genes were used for absolute dating. d Estimation of LTR activity showing a recent burst in Welwitschia less than two million years ago (mya). e In this recent burst of activity, the majority of elements responsible were both autonomous (13,893 copies of Ty1-copia and 9,999 copies of Ty3-gypsy) and non-autonomous LTRs (10,589 copies), with peaks of activity <5 mya. f Heuristic neighbor-joining trees constructed from 3,298 full-length Ty3-gypsy and 2,224 of Ty1-copia sequences from Welwitschia, Gnetum, Ginkgo, and Amborella. There were many more complete elements identified in Ginkgo (4,237) than in the other species, elements that were likely to have been derived from a peak of activity about 15 mya. A few clades of Welwitschia-derived Ty3-gypsy (131 copies) probably arose from the recent activity at ~2 mya (see e). Source data underlying Fig. d–f are provided as a Source Data file.