The Cycas genome and the early evolution of seed plants

Abstract

Cycads represent one of the most ancient lineages of living seed plants. Identifying genomic features uniquely shared by cycads and other extant seed plants, but not non-seed-producing plants, may shed light on the origin of key innovations, as well as the early diversification of seed plants. Here, we report the 10.5-Gb reference genome of Cycas panzhihuaensis, complemented by the transcriptomes of 339 cycad species. Nuclear and plastid phylogenomic analyses strongly suggest that cycads and Ginkgo form a clade sister to all other living gymnosperms, in contrast to mitochondrial data, which place cycads alone in this position. We found evidence for an ancient whole-genome duplication in the common ancestor of extant gymnosperms. The Cycas genome contains four homologues of the fitD gene family that were likely acquired via horizontal gene transfer from fungi, and these genes confer herbivore resistance in cycads. The male-specific region of the Y chromosome of C. panzhihuaensis contains a MADS-box transcription factor expressed exclusively in male cones that is similar to a system reported in Ginkgo, suggesting that a sex determination mechanism controlled by MADS-box genes may have originated in the common ancestor of cycads and Ginkgo. The C. panzhihuaensis genome provides an important new resource of broad utility for biologists.

Recent advances on phylogenomics of gymnosperms and a new classification

“…Nuclear genomes of Gnetaceae and Welwitschiaceae were published recently ( Wan et al., 2018 , 2021 ). Phylogenomic results based on thousands of single-copy nuclear genes reinforce the gnepine hypothesis and negate the monophyly of conifers ( Ran et al., 2018a ; Stull et al., 2021 ; Liu et al., 2022 ). Accordingly, the traditional concept of conifers should be revised in a new classification.…”

“…Third, the subclass Pinidae is paraphyletic according to recent studies, with Gnetidae nested within Pinidae and they together form a monophyletic group sister to a clade including the remaining conifers (conifer II, Ran et al., 2018a ; Stull et al., 2021 ). Recent phylogenomic results have reinforced this gnepine hypothesis ( Ran et al., 2018a ; Stull et al., 2021 ; Liu et al., 2022 ). Fourth, the sequence of the three families within the Gnetidae is not in accordance with their relationships.…”

“…(2011) treated Ginkgo as a separate subclass (Ginkgoidae) parallel to the other three subclasses including Cycadidae, Pinidae, and Gnetidae. Recent phylogenomics based on thousands of single-copy nuclear genes have consistently suggested that ginkgophyte is sister to cycadophyte ( Ran et al., 2018a ; Stull et al., 2021 ; Liu et al., 2022 ). Considering its unusual morphology and phylogeny, we treat Ginkgo as a class here in this updated classification of gymnosperms.…”

“…This unique set of characters has led many people to believe that the gnetophytes are direct ancestors (pseudanthial hypothesis) or relatives of ancestors of the angiosperms (anthophyte and euanthial hypotheses) ( Yang et al., 2004 ; Friis et al., 2011 ). However, molecular phylogenetic studies have indicated that gnetophytes constitute a monophyletic group that is either sister to the Pinaceae (gnepine hypothesis, Gugerli et al., 2001 ; Ran et al., 2018a ; Stull et al., 2021 ; Liu et al., 2022 ), or to the Cupressophytes, including Sciadopityaceae, Cupressaceae and Taxaceae (gnecup hypothesis, Wu et al., 2013 ), or to the conifers (gnetifer hypothesis, Ran et al., 2010 ), or to other living gymnosperms ( Wang and Ran, 2014 ), or to other living seed plants ( Wang and Ran, 2014 ; Song et al., 2021 ; Niu et al., 2022 ). Nuclear genomes of Gnetaceae and Welwitschiaceae were published recently ( Wan et al., 2018 , 2021 ).…”

“…However, traditional classification based on morphology classified them into different orders ( Pilger and Melchior, 1954 ; Delectis Florae Reipublicae Popularis Sinicae Agendae Academiae Sinicae Edita, 1978 ) as the two families possess quite different morphology of female cones: Podocarpaceae possess reduced and usually fleshy cones, while Araucariaceae have typical woody cones. However, recent phylogenetic studies have consistently suggested that Podocarpaceae and Araucariaceae form a clade sister to another clade including Sciadopityaceae, Cupressaceae, and Taxaceae ( Li et al., 2017 ; Ran et al., 2018a ; Stull et al., 2021 ; Liu et al., 2022 ). Hence, we classify the two families in the order Araucariales.…”