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.

Highlights

  • The gymnosperm Welwitschia mirabilis belongs to the ancient, enigmatic gnetophyte lineage

  • In support of this, when considering synteny by which paralogous genes are retained but gene collinearity has been lost[17], we found an additional 773 paralogous genes located in 222 syntenic regions, giving further strong support to the whole-genome duplication (WGD) in Welwitschia (Supplementary Fig. 3)

  • Welwitschia-like fossils suggest that the Welwitschia lineage existed in diverse morphological forms in northern Gondwana during the Early Cretaceous[71]

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Summary

Introduction

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. The species has a highly distinctive morphology, consisting of just two leaves that grow continuously throughout the plant’s life This can last several thousand years, resulting in the longest-lived leaves in the plant kingdom[2,3,4]. We use genome assembly data together with extensive epigenomic and transcriptomic data to unveil a distinctive genome structure that enhances our understanding of genome evolution in gnetophytes and sheds light on gene families that have given rise to Welwitschia’s unique morphology, extreme longevity, and its ability to survive in harsh, arid environments

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