Genomic insights into inter‐ and intraspecific mating system shifts in Primulina

Abstract

The mating system shift from outcrossing to selfing is one of the most frequent evolutionary trends in flowering plants. However, the genomic consequences of this shift remain poorly understood. Specifically, the relative importance of the demographic and genetic processes causing changes in genetic variation and selection efficacy associated with the evolution of selfing is unclear. Here we sequenced the genomes of two Primulina species with contrasting mating systems: P. eburnea (outcrossing) versus P. tabacum (outcrossing, mixed-mating and selfing populations). Whole-genome resequencing data were used to investigate the genomic consequences of mating system shifts within and between species. We found that highly selfing populations of P. tabacum display loss of genetic diversity, increased deleterious mutations, higher genomic burden and fewer adaptive substitutions. However, compared with outcrossing populations, mixed-mating populations did not display loss of genetic diversity and accumulation of genetic load. We find no evidence of population bottlenecks associated with the shift to selfing, which suggests that the genetic effects of selfing on N e and possibly linked selection, rather than demographic history, are the primary drivers of diversity reduction in highly selfing populations. Our results highlight the importance of distinguishing the relative contribution of mating system and demography on the genomic consequences associated with mating system evolution in plants.

Genetic causes and genomic consequences of breakdown of distyly inLinum trigynum

“…While detailed analyses separately assessing selection on specific classes of genes, such as those involved in the evolution of the selfing syndrome or pollen competition (Gutiérrez-Valencia et al 2022b) would be warranted for a more complete understanding of the impact of shifts to selfing on selection across the genome, our results so far demonstrate genomic signatures consistent with relaxed purifying and positive selection on nonsynonymous mutations in association with loss of distyly. These results are in line with those in a previous study on the genomic impact of loss of distyly in Primula (Wang et al 2021), and with a wealth of studies on the genomic impact of shifts to selfing in other plant lineages (e.g, Slotte et al 2010, Slotte et al 2013, Laenen et al 2018, Mattila et al 2020, Yi et al 2022). Comparative population genomic analyses of multiple shifts from distyly to homostyly in Linum will be valuable to better understand the general population genomic effects of this major evolutionary transition.…”

Parallel evolution of morphological and genomic selfing syndromes accompany the breakdown of heterostyly

“…Persistently high selfing rates (e.g. s > 90%) is generally considered a key requirement for the gradual evolution of the genomic selfing syndrome, although a small degree of outcrossing may be sufficient to purge deleterious mutations and limit populations from being trapped in the evolutionary ‘dead end’ of genomic decay (Barrett et al ., 2014; Kamran‐Disfani & Agrawal, 2014; Laenen et al ., 2018; Yi et al ., 2022). In our study, selfing rates in homostylous populations ranged from 0.718 to 0.776 and from 0.896 to 0.906 for the younger and older selfing lineages, respectively (Fig.…”

Genome-wide analysis of the cellulose toolbox of Primulina eburnea, a calcium-rich vegetable

“…Building on the recent availability of the P. eburnea genome [ 43 ], the present study reports a comprehensive genome-wide identification of cellulose biosynthesis gene families in P. eburnea . Combining the phylogenetic relationships and expression profiles, we highlighted the evolutionary histories of these families and predicted the toolbox genes through nitrogen fertilization experiments.…”

“…However, the genetic basis for vegetable domestication in Primulina has not yet been reported. The recent availability of the P. eburnea genome [ 43 ] provided an opportunity to conduct comprehensive genome-wide identification and analysis of cellulose biosynthetic genes, as reported in the present study. By combining a genome-wide survey of the genes included in the eight gene families involved with cellulose biosynthesis with comparative phylogenetic analyses, we identified 36 P. eburnea genes.…”