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Supergene evolution in a classic plant system - bringing the study of distyly into the genomic era

Periodic Reporting for period 2 - SuperGenE (Supergene evolution in a classic plant system - bringing the study of distyly into the genomic era)

Reporting period: 2019-07-01 to 2020-12-31

A central question in evolutionary biology concerns how adaptive combinations of traits can be maintained. Supergenes offer one solution to this problem: they are clusters of genes that are inherited as a unit and can thus maintain favorable trait combinations. But suppression of recombination at supergenes also comes at the cost of increased accumulation of harmful mutations, which might affect their long-term maintenance. This project aims to improve our understanding of supergene origins and evolution by studies of a classic supergene that governs the balanced floral polymorphism of distyly.

Distyly is an iconic floral polymorphism that ensures outcrossing and efficient pollen transfer to compatible plants. Distyly signifies the presence of two floral morphs, where flowers of different individuals differ reciprocally in the placement of male and female reproductive organs. Distyly has arisen independently many times in different evolutionary lineages, and is a textbook example of convergent evolution. It has been known for a long time that distyly is governed by a supergene, but until recently, the molecular makeup or evolution of distyly supergenes had not been studied in detail.

In this project, we aim to make full use of the latest advances in genomics to elucidate the evolution of a classic supergene that governs distyly in Linum, wild flaxseed species. This system is ideal for this purpose due to the dynamic nature of distyly in Linum. We will establish a genomic framework for studies of the evolution and loss of distyly in wild Linum by generating high-quality contiguous genome assemblies of six Linum species. We will then use these assemblies as a basis for identifying the characterizing the supergene that underlies distyly, and investigate supergene evolution at the genetic and regulatory level. Finally, we will investigate how and when distyly has been lost, and what the population genomic effects are.

The high-quality genomes produced in this project will pave the way for further studies to elucidate the molecular genetics of distyly, an adaptive floral polymorphism studied already by Darwin. The results are of general importance for an improved understanding of the evolution of coadapted gene complexes, and will shed new light on the fascinating phenomenon of supergenes.
A major objective of this project was to generate an improved genomic framework for further studies of distyly evolution and loss in wild Linum species. To this end, we have generated Platinum-quality diploid, phased chromosome-scale genome assemblies of both pin and thrum floral morph Linum individuals. These genome assemblies were generated based on high-coverage PacBio long-read sequencing data, scaffolded with Hi-C data, and polished with Illumina short-read data. The resulting assemblies are highly contiguous and contain the expected number of scaffolds based on the chromosome count of the sequenced species. These assemblies for a basis for further genomic work in Linum.

We have used population resequencing data coupled with our high-quality assemblies to identify the supergene that governs distyly in Linum (the distyly S-locus). To assess how supergene genetic architecture affects evolutionary trajectories at supergenes such as the S-locus, we have conducted forward population genetic simulations. Our results suggest that the genetic architecture of supergenes has major consequences for the expected evolution of S-locus haplotypes. Extending these studies to other distylous and homostylous Linum species will allow further insights into the evolution and loss of distyly.
A major aim of the project was to provide a genomic framework for further studies of distyly in Linum. The highly contiguous genome assemblies we have produced so far using new sequencing technologies and cutting edge methods for genome assembly constitute a major step towards this goal. These assemblies have allowed us to identify a candidate region for the distyly S-locus, which has never been fully sequenced in Linum before. This constitutes a major advance in our understanding of distyly supergene architecture. We are currently combining forward population genetic simulations, molecular population genomic analyses and gene expression analyses to better understand the evolution of the supergene. Extending these studies to other distylous and homostylous Linum species will allow us to assess whether the genetic architecture of distyly is shared across distylous Linum and investigate the evolution and genetic basis of homostyly.

By the end of the project we thus expect to have generated additional Linum high-quality genome assemblies, using the methods we have established so far. We expect to have undertaken molecular evolution and gene expression studies to achieve an improved understanding of the evolutionary trajectories of supergene haplotypes. Finally, we expect to have an improved understanding of the genetic basis and population genomic consequences of loss of distyly, based on a combination of genome assembly and population genomics analyses in homostylous Linum species. Taken together, the results generated in this project are likely to be important for an improved understanding of the evolution of plant mating systems and the evolution of a classic supergene.
Thrum (left) and pin (right) flowers of the distylous Linum tenue studied in the SuperGenE project.