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

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.