Differential gene expression associated with a floral scent polymorphism in the evening primrose Oenothera harringtonii (Onagraceae)

Jeremie B Fant,Lindsey L Bechen,Norman J Wickett,Matthew G Johnson,Robert A Raguso,Geoffrey T Broadhead,Rick P Overson,Tania Jogesh,Rachel A Levin,Krissa A Skogen

doi:10.1186/s12864-022-08370-6

Abstract

BackgroundPlant volatiles play an important role in both plant-pollinator and plant-herbivore interactions. Intraspecific polymorphisms in volatile production are ubiquitous, but studies that explore underlying differential gene expression are rare. Oenothera harringtonii populations are polymorphic in floral emission of the monoterpene (R)-(−)-linalool; some plants emit (R)-(−)-linalool (linalool+ plants) while others do not (linalool- plants). However, the genes associated with differential production of this floral volatile in Oenothera are unknown. We used RNA-Seq to broadly characterize differential gene expression involved in (R)-(−)-linalool biosynthesis. To identify genes that may be associated with the polymorphism for this trait, we used RNA-Seq to compare gene expression in six different Oenothera harringtonii tissues from each of three linalool+ and linalool- plants.ResultsThree clusters of differentially expressed genes were enriched for terpene synthase activity: two were characterized by tissue-specific upregulation and one by upregulation only in plants with flowers that produce (R)-(−)-linalool. A molecular phylogeny of all terpene synthases identified two putative (R)-(−)-linalool synthase transcripts in Oenothera harringtonii, a single allele of which is found exclusively in linalool+ plants.ConclusionsBy using a naturally occurring polymorphism and comparing different tissues, we were able to identify candidate genes putatively involved in the biosynthesis of (R)-(−)-linalool. Expression of these genes in linalool- plants, while low, suggests a regulatory polymorphism, rather than a population-specific loss-of-function allele. Additional terpene biosynthesis-related genes that are up-regulated in plants that emit (R)-(−)-linalool may be associated with herbivore defense, suggesting a potential economy of scale between plant reproduction and defense.

Highlights

Plant volatiles play an important role in both plant-pollinator and plant-herbivore interactions
The flowers of three individuals (A-C) emitted large amounts of (R)-(−)linalool, whereas those from another three individuals did not emit any (Table 1; Fig. 1A). This pattern is consistent with phenotypic data from the source populations for these plants (Additional file 4), confirming that linalool chemotypes breed true in greenhousegrown plants
When the linalool peaks from linalool+ populations (Florence, Maverick, Baculite Mesa) were found to align with the retention time of the (R)-(−) enantiomer, but not with that of the (S)-(+) enantiomer or the linalool peak from Clarkia breweri, we re-injected an O. harringtonii headspace sample from the Florence population, to which a small amount of the (R)-(−) enantiomer was added

Summary

Introduction

Plant volatiles play an important role in both plant-pollinator and plant-herbivore interactions. The biosynthetic pathways that produce floral volatiles are increasingly well-characterized [14], and recent studies have used transcriptomics-based approaches to identify homologous genes from these pathways in nonmodel plant species [15,16,17,18]. Despite these advances [19, 20], relatively few studies have identified the genetic mechanisms that impact how these pathways modify floral scent or how selection acts on the resulting intraspecific variation. There have been few opportunities to study the genetic underpinnings of volatile terpenoid polymorphism in floral scent

Methods

Results

Conclusion