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Two leaves that cannot die: the genome sequence of Welwitschia mirabilis reveals its unique biology and evolutionary history

Liu, Zhiming1; Wan, Tao1; Wang, Qingfeng2

Published Jun 18, 2021 on Dryad. https://doi.org/10.5061/dryad.ht76hdrdr

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Abstract

Welwitschia mirabilis (hereafter Welwitschia), the sole species in Welwitschiales, belongs to gnetophytes, an ancient, enigmatic gymnosperm lineage. It is a strikingly bizarre plant with distinctive morphology of just two large ever-elongating leaves and is remarkable in being able to survive extreme environmental stresses of the Namibian and Angolan deserts. Here, we provide a chromosome-level assembly of its genome (6.8 Gb/1C) and extensive methylome and transcriptome data to reveal the genetics underpinning its intriguing biology. The Welwitschia genome has been shaped by a lineage-specific ancient whole genome duplication ~ 86 million years ago, and more recently (within 10 million years) by bursts of retrotransposon activity. In addition, high levels of cytosine methylation, extremely so for CHH motifs, are associated with retrotransposons, whilst their long-term deamination has resulted in an exceptionally GC-poor genome. High levels of methylation are likely to be responses to maintain genomic integrity in the face of stress-induced retroelement mobility while reduced GC content will confer a genomic advantage under nutrient limitation. Changes in the copy number and/or expression of key gene families and specific transcription factors (e.g. R2R3MYB, SAUR) controlling cell growth, differentiation and metabolism underpin the plant’s extreme longevity under increasing temperature, nutrient and water stress. The Welwitschia chromosome level assembly here, along with a new high-quality assembly for Gnetum montanum, enhances our understanding of genome evolution in gnetophytes. It also provides critical new insights into the extraordinary development of Welwitschia’s ever-growing leaves, enabling its survival in such hostile conditions.