Polyploid Plants Maintain Heterostyly Through Ancient Genetic Architecture

Heterostyly is a floral polymorphism in which populations within a species contain two (distyly) or three (tristyly) floral morphs, characterized by reciprocal positioning of stigmas and anthers. This arrangement enhances pollination accuracy, reduces sexual interference, and promotes cross-pollination. Controlled by the S-locus supergene, heterostyly was vividly described by Charles Darwin as “a most complex marriage arrangement” (Darwin 1864, Journal of the Proceedings of the Linnean Society). Whole-genome duplication (WGD), or polyploidization, often disrupts complex genetic systems, and has traditionally been thought to cause the breakdown of heterostyly into homostyly. However, previous molecular studies of heterostyly have been restricted to diploid species, molecular evidence from polyploid systems has been lacking.

A landmark study led by South China Botanical Garden of the Chinese Academy of Sciences (SCBG) and Shandong University of Technology, recently published in New Phytologist (IF_5-year: 10.3), challenges this paradigm by uncovering the genetic architecture of heterostyly in the tetraploid species Schizomussaenda henryi (Rubiaceae). This work reports the first chromosome-level genome assembly of S. henryi, and by conducting comparative genomic and transcriptomic analyses revealed that the distyly-associated S-locus remains intact and fully functional after polyploidization. The S-locus is present only in short-styled individuals, occurs in a hemizygous state, and consists of four tightly linked genes. Among them, SchzAUX22, an auxin response factor, was identified as a key candidate gene regulating distyly development. Phylogenetic and k-mer analyses indicate that S. henryi likely originated from an allopolyploidization event approximately 3.6 million years ago. By calculating the synonymous substitution rate (Ks) between S-locus genes and their homologs, it is found that the S-locus arose around 50 million years ago—long predating polyploidization. These findings demonstrate that polyploidization does not inevitably lead to the breakdown of heterostyly, highlighting the resilience of this supergene system.

This study represents the first genome-level deciphering of the molecular mechanisms underlying heterostyly in polyploid plants, offering novel insights into the evolution of floral polymorphism and breeding systems in angiosperms. Prof. LUO Zhonglai (Shandong University of Technology) is the first author. Prof. ZHANG Dianxiang and Dr. SHI Miaomiao (SCBG), together with Prof. LUO Zhonglai, serve as co-corresponding authors. This research was supported by the National Natural Science Foundation of China and the Guangdong Natural Resources Funds. Article link: https://nph.onlinelibrary.wiley.com/doi/10.1111/nph.70521

Figure. A. The L-morph and S-morph flowers ofSchizomussaenda henryi. B. Circos map illustrating basic information on the S. henryi genome (S-morph). C. Model of the genomic structure of S-locus genes in S. henryi. D. Ks distributions of paralogous genes in S. henryi (S-morph), Mussaenda pubescens, Coffea canephora (Rubiaceae) and Thymus quinquecostatus (Lamiaceae). (image by SHI et al)