Taxus yunnanensis genome offers insights into gymnosperm phylogeny and taxol production

Abstract

Taxol, a natural product derived from Taxus, is one of the most effective natural anticancer drugs and the biosynthetic pathway of Taxol is the basis of heterologous bio-production. Here, we report a high-quality genome assembly and annotation of Taxus yunnanensis based on 10.7 Gb sequences assembled into 12 chromosomes with contig N50 and scaffold N50 of 2.89 Mb and 966.80 Mb, respectively. Phylogenomic analyses show that T. yunnanensis is most closely related to Sequoiadendron giganteum among the sampled taxa, with an estimated divergence time of 133.4−213.0 MYA. As with most gymnosperms, and unlike most angiosperms, there is no evidence of a recent whole-genome duplication in T. yunnanensis. Repetitive sequences, especially long terminal repeat retrotransposons, are prevalent in the T. yunnanensis genome, contributing to its large genome size. We further integrated genomic and transcriptomic data to unveil clusters of genes involved in Taxol synthesis, located on the chromosome 12, while gene families encoding hydroxylase in the Taxol pathway exhibited significant expansion. Our study contributes to the further elucidation of gymnosperm relationships and the Taxol biosynthetic pathway.

Recent advances on phylogenomics of gymnosperms and a new classification

“…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 ).…”

Plant biosynthetic gene clusters in the context of metabolic evolution

“…5C), 76 and taxol biosynthesis in Taxus spp., of the Coniferophyte lineage. 51,77 The lack of described examples outside angiosperms is not likely due to a real scarcity of BGCs in these lineages but rather due to the paucity of genome sequences, a result of genome complexity and investigation bias. As new genomes in these lineages are sequenced, more BGCs will be discovered.…”

Evolution of complex genome architecture in gymnosperms

“…The genomes of 2 iconic species from the Cupressaceae family, the giant sequoia ( Sequoiadendron giganteum , 8.1 Gb) and the coast redwood ( Sequoia sempervirens , a hexaploid genome of 26.5 Gb), were successively decoded with conspicuously enhanced contiguity [ 6 , 38 ]. Additionally, 3 assembly data resources for a single genus, Taxus , were released almost simultaneously, reflecting the great interest in the gymnosperm genomes [ 22 , 39 , 40 ]. Notably, all the records provided impressively complete genomes, as suggested by assembly lengths (contig N50 = 2.44 Mb in Taxus chinensis , 2.89 Mb in Taxus yunnanensis , and 8.60 Mb in Taxus wallichiana ) and the coverage of the core Embryophyta gene library [ 41 ] (Fig.…”

“…Thus, the various ages estimated by different studies of the LTR outbreaks of the same gymnosperm could be partially explained by the different neutral mutation rates assigned (i.e., 7.3 × 10 −10 was used for T. yunnanensis and T. chinensis var. mairei [ 22 , 40 ]). It is worth mentioning that the outlier Welwitschia has suffered from a very recent expansion of both autonomous and nonautonomous LTRs in less than 1 to 2 Ma, which probably resulted from a cascade of events triggered by intense aridity [ 27 ].…”