Gain and Loss of Floral Scent Production through Changes in Structural Genes during Pollinator-Mediated Speciation

Abstract

The interactions of plants with their pollinators are thought to be a driving force in the evolution of angiosperms. Adaptation to a new pollinator involves coordinated changes in multiple floral traits controlled by multiple genes. Surprisingly, such complex genetic shifts have happened numerous times during evolution. Here we report on the genetic basis of the changes in one such trait, floral scent emission, in the genus Petunia (Solanaceae). The increase in the quantity and complexity of the volatiles during the shift from bee to hawkmoth pollination was due to de novo expression of the genes encoding benzoic acid/salicylic acid carboxyl methyltransferase (BSMT) and benzoyl-CoA:benzylalcohol/2-phenylethanol benzoyltransferase (BPBT) together with moderately increased transcript levels for most enzymes of the phenylpropanoid/benzenoid pathway. Loss of cinnamate-CoA ligase (CNL) function as well as a reduction in the expression of the MYB transcription factor ODO1 explain the loss of scent during the transition from moth to hummingbird pollination. The CNL gene in the hummingbird-adapted species is inactive due to a stop codon, but also appears to have undergone further degradation over time. Therefore, we propose that loss of scent happened relatively early in the transition toward hummingbird pollination, and probably preceded the loss of UV-absorbing flavonols. The discovery that CNL is also involved in the loss of scent during the transition from outcrossing to selfing in Capsella (Brassicaceae) (see the accompanying paper) raises interesting questions about the possible causes of deep evolutionary conservation of the targets of evolutionary change.

Adaptation and Phenotypic Diversification in Arabidopsis through Loss-of-Function Mutations in Protein-Coding Genes

“…Consistent with the less-is-more hypothesis, many cases of gene loss have been reported in diverse organisms, including unicellular organisms such as bacteria (Will et al, 2010;Hottes et al, 2013), and multicellular organisms, such as plants (Zufall and Rausher, 2004;Hoballah et al, 2007;Song et al, 2007;Tang et al, 2007;Gujas et al, 2012;Amrad et al, 2016;Sas et al, 2016;Wu et al, 2017) and animals (Greenberg et al, 2003;Hodgson et al, 2014;Goldman-Huertas et al, 2015), including humans (MacArthur and 1000 Genomes Project Consortium et al, 2012;Narasimhan et al, 2016). LoF mutations have been shown to affect important biological processes, such as development and stress resistance in plants (Gujas et al, 2012;Wu et al, 2017) and intellectual disabilities in humans (Green et al, 2017).…”

Floral Trait Variations Among Wild Tobacco Populations Influence the Foraging Behavior of Hawkmoth Pollinators

“…Chemical signals are particularly suited for rapid and local adaptions to certain pollinators as they are often influenced by relatively small genetic changes (Amrad et al, 2016). Unfortunately, the full biosynthetic pathway producing benzyl acetone, the major flower compound in N. attenuata is still unknown.…”

Floral Scent Evaluation of Three Cut Flowers Through Sensorial and Gas Chromatography Analysis

“…Floral scent is also important in the marketing of ornamental plants and has been described as one of the most important characteristics during the vase life of cut flowers for consumers [3]. However, this characteristic has been insufficiently developed in new cultivars of flowers since the heredity of floral scent is rather complicated, being easily lost and acquired across generations [4]. Moreover, negative selection has been performed by breeders due to the apparent correlation that exists between the presence of floral scent and shorter vase life of the flower [5].…”