Extreme haplotype variation in the desiccation-tolerant clubmoss Selaginella lepidophylla - PubMed (original) (raw)

Extreme haplotype variation in the desiccation-tolerant clubmoss Selaginella lepidophylla

Robert VanBuren et al. Nat Commun. 2018.

Abstract

Plant genome size varies by four orders of magnitude, and most of this variation stems from dynamic changes in repetitive DNA content. Here we report the small 109 Mb genome of Selaginella lepidophylla, a clubmoss with extreme desiccation tolerance. Single-molecule sequencing enables accurate haplotype assembly of a single heterozygous S. lepidophylla plant, revealing extensive structural variation. We observe numerous haplotype-specific deletions consisting of largely repetitive and heavily methylated sequences, with enrichment in young Gypsy LTR retrotransposons. Such elements are active but rapidly deleted, suggesting "bloat and purge" to maintain a small genome size. Unlike all other land plant lineages, Selaginella has no evidence of a whole-genome duplication event in its evolutionary history, but instead shows unique tandem gene duplication patterns reflecting adaptation to extreme drying. Gene expression changes during desiccation in S. lepidophylla mirror patterns observed across angiosperm resurrection plants.

PubMed Disclaimer

Conflict of interest statement

The authors declare no competing financial interests.

Figures

Fig. 1

Fig. 1

Genome assembly graph of S. lepidophylla. Each line (node) represents a contig with connections (edges) representing ambiguities in the graph structure. A subset of the graph showing heterozygous bubbles is enlarged. Contig color is randomly assigned

Fig. 2

Fig. 2

Extensive haplotype-specific LTR retrotransposon accumulation and deletion. a Typical micro-collinearity between two S. lepidophylla haplotypes. b Estimated insertions times of intact Copia and Gypsy LTR retrotransposons. c Composition of haplotype specific and paired collinear regions. The proportion of genes and LTRs in the 105 manually curated insertions (left) and flanking collinear regions (right) are plotted. d Micro-collinearity between two haplotypes showing a large 57 kb deletion in contig 142. Green and blue bars delineate gene orientation. Predicted LTR elements are depicted in orange and the three complete Gypsy LTRs are denoted by arrows. The three complete Gypsy LTRs have insertion times of <0.1 Ma

Fig. 3

Fig. 3

Global methylation patterns in the S. lepidophylla genome. a S. lepidophylla lacks gene body methylation. Levels of CHH (green), CHG (blue) and CpG (red) methylation are plotted in the upstream (transcriptional start site; TSS), downstream (transcriptional termination site (TTS), and body of genes. b Intact LTR retrotransposons are highly methylated with decreasing levels at the 5′- and 3′-flanking regions. c Methylation levels are highly variable across the genome with strong correlation of LTR retrotransposon density. Top, genome landscape of genomic features across Contig 1. Bottom, heatmap of genomic features and methylation levels, where blue indicates low abundance and red signifies high abundance

Fig. 4

Fig. 4

Genomic features of the rehydration and desiccation processes. a Overview of sampling for the rehydration and desiccation time course. Samples were taken from plants that were desiccated for 3 years (0), 1, 6, and 24 h post rehydration (recovery), 120 h post rehydration (fully recovered), and after a 24 h dehydration (de24 h). b Scaled transcript expression profiles (in transcripts per million, TPM) of representative gene co-expression clusters with decreased (10, 16, 34) and increased expression (5, 14, 34) during rehydration. c Heatmap of log2 transformed early light-induced protein (ELIP) expression with the two arrays of tandem duplicated genes in S. lepidophylla orthologous to the only ELIP in to S. moellendorffii highlighted on the left

Similar articles

Cited by

References

    1. Oliver MJ, Tuba Z, Mishler BD. The evolution of vegetative desiccation tolerance in land plants. Plant Ecol. 2000;151:85–100. doi: 10.1023/A:1026550808557. - DOI
    1. Costa M, et al. A footprint of desiccation tolerance in the genome of Xerophyta viscosa. Nat. Plants. 2017;3:17038. doi: 10.1038/nplants.2017.38. - DOI - PubMed
    1. Proctor M. The physiological basis of bryophyte production. Bot. J. Linn. Soc. 1990;104:61–77. doi: 10.1111/j.1095-8339.1990.tb02211.x. - DOI
    1. Lüttge, U., Beck, E. & Bartels, D. Plant desiccation tolerance. Vol. 215 (Springer, 2011).
    1. VanBuren R, et al. Single-molecule sequencing of the desiccation-tolerant grass Oropetium thomaeum. Nature. 2015;527:508–511. doi: 10.1038/nature15714. - DOI - PubMed

Publication types

MeSH terms

Substances

LinkOut - more resources