Retracing the molecular basis and evolutionary history of the loss of benzaldehyde emission in the genus Capsella

Abstract

The transition from pollinator-mediated outbreeding to selfing has occurred many times in angiosperms. This is generally accompanied by a reduction in traits attracting pollinators, including reduced emission of floral scent. In Capsella, emission of benzaldehyde as a main component of floral scent has been lost in selfing C. rubella by mutation of cinnamate-CoA ligase CNL1. However, the biochemical basis and evolutionary history of this loss remain unknown, as does the reason for the absence of benzaldehyde emission in the independently derived selfer Capsella orientalis.We used plant transformation, in vitro enzyme assays, population genetics and quantitative genetics to address these questions.CNL1 has been inactivated twice independently by point mutations in C. rubella, causing a loss of enzymatic activity. Both inactive haplotypes are found within and outside of Greece, the centre of origin of C. rubella, indicating that they arose before its geographical spread. By contrast, the loss of benzaldehyde emission in C. orientalis is not due to an inactivating mutation in CNL1.CNL1 represents a hotspot for mutations that eliminate benzaldehyde emission, potentially reflecting the limited pleiotropy and large effect of its inactivation. Nevertheless, even closely related species have followed different evolutionary routes in reducing floral scent.

The ecology, evolution, and genetics of plant reproductive systems

“…Jantzen et al . (, in this issue pp. 1349–1360) use a combination of transformation experiments, in vitro assays, and quantitative and population genetics methods to explore aspects of the ‘selfing syndrome’ in the genus Capsella , and find that while there are hotspots for mutations that are associated with scent reduction, independently‐derived selfing species in the genus have undergone different genetic paths to arrive at this phenotype.…”

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

“…Woz ´niak et al [48] performed QTL mapping and transcriptome analyses, demonstrating that low-pleiotropic and organ-specific gene regulatory networks are involved in the evolution of the selfing syndrome, and that petal size reduction at least has a similar genetic basis to C. rubella [48]. By contrast, in the case of the loss of benzaldehyde emission, an inactivating mutation in CNL1 was not responsible in C. orientalis, unlike in C. rubella [49].…”

“…In contrast, the CYP724A1 gene involved in petal size reduction in C. rubella harboured two mutations, and population genetic analysis from 182 C. grandiflora individuals revealed that the more efficiently spliced C. rubella allele, which confers reduced petal size, most likely arose by two de novo mutations in the C. rubella lineage after its divergence from C. grandiflora [19]. The CNL1 , gene involved in reduced scent emission, was inactivated twice independently in C. rubella by different de novo mutations in its coding sequence [20,49].…”

A whiff of the future: functions of phenylalanine‐derived aroma compounds and advances in their industrial production

“…These aroma compounds strongly contribute to specificity in plant–pollinator interactions. For example, loss of benzaldehyde emission in Capsella underlies the transition from animal‐mediated pollination to selfing (Jantzen et al ., 2019; Sas et al ., 2016). In moth‐pollinated petunia, loss of benzaldehyde production led to a shift in pollinator to hummingbirds, which depend largely on their eyesight (Amrad et al ., 2016).…”