Heterostyly is a plant sexual polymorphism in which populations are usually composed of two or three floral morphs with the reciprocal placement of stigmas and anthers. The polymorphism is usually associated with a self-incompatibility system preventing self- and intra-morph fertilization, consequently, populations typically practice disassortative mating. Heterostyly occurs in at least 28 angiosperm families and has evolved independently on numerous occasions. Similarities in floral form and function among diverse heterostylous lineages provide outstanding opportunities to investigate the molecular basis of evolutionary convergence.

A team led by Prof. WANG Qingfeng and Prof. CHEN Jinming at Wuhan Botanical Garden, Chinese Academy of Sciences, in collaboration with Prof. Spencer C. H. Barrett's team from the University of Toronto, investigated the genetic architecture of the S-locus supergene (functionally associated genes that are completely linked) in distylous Nymphoides indica, and explored how it may have evolved. N. indica is in a lineage of flowering plants where heterostyly has not been investigated previously.

This study utilized a read-coverage-based genome-wide association analysis to identify a 178 kb hemizygous region in the short-styled morph of N. indica. This region contained three candidate S-locus genes: NinBAS1, NinKHZ2, and NinS1. NinBAS1 was expressed only in the style, NinS1 was expressed only in the stamens, and NinKHZ2 was expressed in both the style and stamens.

This study also explored the potential functions of the S-locus genes and their regulatory networks, as well as the potential roles of transposable elements and gene duplication in the evolution of the heterostyly supergene. The results showed that the density of transposable elements at the S-locus in N. indica was significantly higher than in the rest of the genome. These transposable elements accumulated during the evolution of the S-locus, possibly further inhibiting recombination and leading to gene loss.

Additionally, this study found that brassinosteroids played an important role in the development of styles in N. indica, and the phytochrome-interacting factor molecular regulatory network was significantly enriched in stamens, providing further evidence for the convergent evolution of heterostyly at the molecular level.

This study revealed the genetic basis of heterostyly in the aquatic plant N. indica, expanding the understanding of plant trait diversity and evolution. Furthermore, the high-quality genome resources provided valuable material for future research on the molecular mechanisms of plant adaptive evolution.

This study was published in the prestigious journal New Phytologist, titled "Haplotype-resolved genome assembly provides insights into the evolution of S-locus supergene in distylous Nymphoides indica". YANG Jingshan at Wuhan Botanical Garden and XUE Haoran at the University of Toronto are the co-first authors. Spencer C. H. Barrett at the University of Toronto and WANG Qingfeng and CHEN Jinming at Wuhan Botanical Garden are the co-corresponding authors. This study was supported by the Strategic Priority Research Program of the Chinese Academy of Sciences, the National Natural Science Foundation of China, and the China Youth Innovation Promotion Association of the Chinese Academy of Sciences. (Online: 17 September 2023)