Haplotype‐resolved genome assembly provides insights into the evolution of S‐locus supergene in distylous Nymphoides indica

Abstract

Summary Distyly has evolved independently in numerous animal‐pollinated angiosperm lineages. Understanding of its molecular basis has been restricted to a few species, primarily Primula. Here, we investigate the genetic architecture of the single diallelic locus (S‐locus) supergene, a linkage group of functionally associated genes, and explore how it may have evolved in distylous Nymphoides indica, a lineage of flowering plants not previously investigated. We assembled haplotype‐resolved genomes, used read‐coverage‐based genome‐wide association study (rb‐GWAS) to locate the S‐locus supergene, co‐expression network analysis to explore gene networks underpinning the development of distyly, and comparative genomic analyses to investigate the origins of the S‐locus supergene. We identified three linked candidate S‐locus genes – NinBAS1, NinKHZ2, and NinS1 – that were only evident in the short‐styled morph and were hemizygous. Co‐expression network analysis suggested that brassinosteroids contribute to dimorphic sex organs in the short‐styled morph. Comparative genomic analyses indicated that the S‐locus supergene likely evolved via stepwise duplications and has been affected by transposable element activities. Our study provides novel insight into the structure, regulation, and evolution of the supergene governing distyly in N. indica. It also provides high‐quality genomic resources for future research on the molecular mechanisms underlying the striking evolutionary convergence in form and function across heterostylous taxa.

ThePrimula edelbergii S-locus is an example of a jumping supergene

“…We then asked whether the S -locus was hemizygous also in P. edelbergii , as found in all other heterostylous species studied to date (Fawcett et al, 2023; Gutiérrez-Valencia et al, 2022; Li et al, 2016; Shore et al, 2019; Yang et al, 2023; Zhao et al, 2023), by checking whether the S -locus region was characterized by halved sequencing depth, an approach commonly used to detect hemizygous supergenes (Gutiérrez-Valencia et al, 2021). The S -locus had approximately the same sequencing depth as the rest of chromosome 2 (mean S -locus depth: 154.6x; mean chromosome 2 depth: 156.1x; Figure 4d ).…”

“…Recently, research on the S-locus has expanded from Primula to other genera that independently evolved heterostyly, including Turnera (Henning et al, 2022;Matzke et al, 2020Matzke et al, , 2021Shore et al, 2019), Fagopyrum (Fawcett et al, 2023;Yasui et al, 2012Yasui et al, , 2016, Linum (Gutiérrez-Valencia et al, 2022), Gelsemium (Zhao et al, 2023), and Nymphoides (Yang et al, 2023). Surprisingly, in all these cases the S-locus was found to be hemizygous in thrums and absent from pins, pointing to a remarkable consistency in the genomic architecture of the S-locus across heterostylous taxa.…”

Genetic causes and genomic consequences of breakdown of distyly inLinum trigynum

“…While earlier theory posited that rare recombination events between the recessive and dominant alleles at the S -locus were the cause for distyly breakdown (Dowrick 1956, Charlesworth and Charlesworth 1979a), recent findings have indicated that distyly S- loci harbor presence-absence variation and that thrums are predominantly hemizygous at the S -locus rather than heterozygous (Li et al 2016, Shore et al 2019, Gutiérrez-Valencia et al 2022a, Fawcett et al 2023, Yang et al 2023, Zhao et al 2023). These findings make previous models of breakdown less likely and indicate that mutations either at the S- locus or at unlinked modifier loci are more plausible causes for the evolutionary shift from distyly to homostyly.…”

“…It is only recently that distyly supergenes have begun to be sequenced and characterized in detail (reviewed in Gutiérrez-Valencia et al 2021). So far, characterization of independently evolved distyly supergenes in six systems ( Primula : Li et al 2016, Turnera : Shore et al 2019; Linum : Gutiérrez-Valencia et al 2022a, Fagopyrum : Yasui et al 2012, Fawcett et al 2023, Gelsemium : Zhao et al 2023; Nymphoides indica : Yang et al 2023) suggest a remarkable degree of convergence in the genetic architecture of distyly supergenes. Common features of independently evolved distyly supergenes include a genetic architecture featuring length differences between the dominant and recessive supergene haplotypes, resulting in hemizygosity in thrum individuals and thrum-specific expression of S- linked genes (Gutiérrez-Valencia et al 2022a).…”

Genetic Causes and Genomic Consequences of Breakdown of Distyly in Linum trigynum

“…It is only recently that distyly supergenes have begun to be sequenced and characterized in detail (reviewed in Gutiérrez-Valencia et al 2021 ). So far, characterization of independently evolved distyly supergenes in six systems ( Fagopyrum : Yasui et al 2012 ; Fawcett et al 2023 ; Primula : Li et al 2016 ; Turnera : Shore et al 2019 ; Linum : Gutiérrez-Valencia et al 2022a ; Nymphoides indica : Yang et al 2023 ; Gelsemium : Zhao et al 2023 ) suggest a remarkable degree of convergence in the genetic architecture of distyly supergenes. Common features of independently evolved distyly supergenes include a genetic architecture featuring length differences between the dominant and recessive supergene haplotypes, resulting in hemizygosity in thrum individuals and thrum-specific expression of S- linked genes ( Gutiérrez-Valencia et al 2022a ).…”