The Saururus chinensis genome provides insights into the evolution of pollination strategies and herbaceousness in magnoliids

SUMMARY

Saururus chinensis, an herbaceous magnoliid without perianth, represents a clade of early‐diverging angiosperms that have gone through woodiness–herbaceousness transition and pollination obstacles: the characteristic white leaves underneath inflorescence during flowering time are considered a substitute for perianth to attract insect pollinators. Here, using the newly sequenced S. chinensis genome, we revisited the phylogenetic position of magnoliids within mesangiosperms, and recovered a sister relationship for magnoliids and Chloranthales. By considering differentially expressed genes, we identified candidate genes that are involved in the morphogenesis of the white leaves in S. chinensis. Among those genes, we verified – in a transgenic experiment with Arabidopsis – that increasing the expression of the “pseudo‐etiolation in light” gene ( ScPEL) can inhibit the biosynthesis of chlorophyll. ScPEL is thus likely responsible for the switches between green and white leaves, suggesting that changes in gene expression may underlie the evolution of pollination strategies. Despite being an herbaceous plant, S. chinensis still has vascular cambium and maintains the potential for secondary growth as a woody plant, because the necessary machinery, i.e., the entire gene set involved in lignin biosynthesis, is well preserved. However, similar expression levels of two key genes (CCR and CAD) between the stem and other tissues in the lignin biosynthesis pathway are possibly associated with the herbaceous nature of S. chinensis. In conclusion, the S. chinensis genome provides valuable insights into the adaptive evolution of pollination in Saururaceae and reveals a possible mechanism for the evolution of herbaceousness in magnoliids.

Significance Statement

The Saururus chinensis genome provides an important new resource for the understanding of the “rapid radiation” of early angiosperms, coined by Darwin as an “abominable mystery,” and recovered a sister relationship for magnoliids and Chloranthales. Experiments and bioinformatics analyses reveal the molecular mechanism for the pollination‐related organ morphogenesis (white leaves during flowering time) in S. chinensis and an adaptive evolution of pollination strategy in Saururaceae, and provide valuable insights into the woodiness–herbaceousness transition in magnoliids.