New genomic resources and comparative analyses reveal differences in floral gene expression in selfing and outcrossing Collinsia sister species

Abstract

The evolutionary transition from outcross-fertilization to self-fertilization is one of the most common in angiosperms and is often associated with a parallel shift in floral morphological and developmental traits, such as reduced flower size and pollen to ovule ratios, known as the ‘selfing syndrome’. How these convergent phenotypes arise, the extent to which they are shaped by selection, and the nature of their underlying genetic basis are unsettled questions in evolutionary biology. The genus Collinsia (Plantaginaceae) includes seven independent transitions from outcrossing or mixed mating to high selfing rates accompanied by selfing syndrome traits. Accordingly, Collinsia represents an ideal system for investigating this parallelism, but requires genomic resource development. We present a high quality de novo genome assembly for the highly selfing species C. rattanii. To begin addressing the basis of selfing syndrome developmental shifts, we evaluate and contrast patterns of gene expression from floral transcriptomes across three stages of bud development for C. rattanii and its outcrossing sister species C. linearis. Relative to C. linearis, total gene expression is less variable among individuals and bud stages in C. rattanii. In addition, there is a common pattern among differentially expressed genes: lower expression levels that are more constant across bud development in C. rattanii relative to C. linearis. Transcriptional regulation of enzymes involved in pollen formation specifically in early bud development may influence floral traits that distinguish selfing and outcrossing Collinsia species through pleiotropic functions. Future work will include additional Collinsia outcrossing-selfing species pairs to identify genomic signatures of parallel evolution.

The Snapdragon Genomes Reveal the Evolutionary Dynamics of the S-Locus Supergene

“…2 B ), indicating Antirrhinum have at least experienced another one WGD after the gamma-whole-genome triplication (WGT) ( Jiao et al 2012 ). The distributions plots of Ks for A. hispanicum , Collinsia rattanii ( Frazee et al 2021 ), and A. linkianum paranomes showed a distinct peak at 2.21 echoing the well-reported gamma-WGT that occurred ∼117 Mya in the common ancestors of all eudicots ( Jiao et al 2012 ) ( fig. 2 B and supplementary fig.…”

The snapdragon genomes reveal the evolutionary dynamics of theSlocus supergene

“…To approximately date the WGD in snapdragon, the distributions of synonymous substitutions per site ( Ks ) among paralogous genes within a genome were examined. The distributions plots of synonymous substitutions per synonymous site for SI-Ah, Collinsia rattanii (Frazee et al 2021) and Antirrhinum linkianum paranomes showed a distinct peak at 2.23 corresponding to the well-reported gamma WGT shared by all eudicots (Fig. 2D and S14), as well as an additional peak at ∼0.78 corresponding to relatively recent duplication event shared among Plantaginaceae members.…”

The selfing syndrome and beyond: diverse evolutionary consequences of mating system transitions in plants

“…The genetic basis of the selfing syndrome has been studied in multiple genera, including Leptosiphon, Mimulus, Solanum, Ipomoea, Capsella, Collinsia and Arabidopsis, mostly through transcriptome analysis or quantitative genetic approaches such as qualitative trait locus (QTL) mapping [24,[34][35][36][37][38][39]. In general, QTL studies have identified several small-to largeeffect loci for each trait, but in most cases, the causal genes underlying QTLs have not been determined until recently.…”