The snapdragon genomes reveal the evolutionary dynamics of theSlocus supergene

Abstract

Multi-allelic S-locus, containing pistil S-RNase and dozens of S-locus F-box (SLF), is known to take responsibility for genetic control of self-incompatibility (SI) in Plantaginaceae. Loss of SI is a prerequisite for mating system transition from self-incompatible to self-compatible, which is very frequent in flowering plants. The transition to selfing is excepted to have noticeable effects on adaptive potential and genome evolution. However, there have been limited comparative studies on the evolutionary shift and S-locus from genome-wide perspective due to lack of high-quality genomic data to date. The genus Antirrhinum has long been used as model plant to study self- incompatibility, here, through integrating sequencing data from multiple platforms, we present the chromosome-level reference and haplotype- resolved genome assembly of an A.hispanicum line, AhS7S8. Comparative genomics approach revealed that the self-incompatible A.hispanicum diverged from its self-compatible relative A.majus approximately 3.6 million years ago (Mya) just after Zanclean flood. The expanded gene families enriched in distinct functional terms implied quite different evolutionary trajectory of outcrossing and selfing snapdragon, and contributed to the adaptation of snapdragon with different mating system. Particularly, we successfully reconstructed two complete S-haplotypes spanning ∼1.2Mb, each consists of 32 SLFs and a S-RNase, as well as a pseudo S-haplotype from self-compatible A.majus. Multiple copies of SLFs derived from proximal or tandem duplication via retroelement-mediated way at a very early time, announcing the ancient history of S-locus. Furthermore, we detected a candidate cis-transcription factor associated with regulating SLFs expression, and two miRNAs may control expression of this TF in a higher position. In general, our abundant genomic data provide excellent resources to study mating system transition of snapdragon, and facilitate the functional genomics and evolutional research of S-RNase based self-incompatibility system.

The role of promiscuous molecular recognition in the evolution of RNase-based self-incompatibility

“…Linking our model to population genetic and genomic data should be very insightful and allow testing some of the model’s qualitative predictions, as well as refining the model and calibrating its parameters. These include estimation of the number of residues distinguishing between different RNase alleles [17], and assessment of between- and within-haplotype SLF diversity [21, 58]. Our model offers predictions regarding the within-class allelic diversity and its dependence on the class size, which could then be contrasted with genomic data.…”

“…It would be very interesting to further test this experimentally. The number of SLF alleles per haplotype determined empirically for species with CNSR SI ranged between 17 to 44 [21, 34, 60, 58, 61], which should be a proxy for the number of distinct specificities. The number of compatibility classes in our model depends positively correlates with the population and E th (probability of proteins to interact at random).…”

A chromosome-level reference genome of an aromatic medicinal plant Adenosma buchneroides

“…Up to now, many efforts on the regulation mechanism of aromatic component biosynthesis has been made in the genus Thymus (Lamiaceae). Though most recently, several pseudo-chromosome level genomes of Plantaginaceae were published [9][10][11] . The molecular basis and evolution of those components biosynthesis in A. buchneroides (Plantaginaceae) are rarely reported due to the lack of a high-quality reference genome.…”