Convergence and molecular evolution of floral fragrance after independent transitions to self–fertilization

Abstract

The study of the independent evolution of similar characters can highlight important ecological and genetic factors that drive phenotypic evolution. The transition from reproduction by outcrossing to self-fertilization has occurred frequently throughout plant evolution. A common trend in this transition is the reduction of flower features in the selfing lineages, including display size, flower signals and pollinators' rewards. These changes are believed to evolve because resources invested in building attractive flowers are reallocated to other fitness functions as the pressures to attract pollinators decrease. We investigated the similarities in the evolution of flower fragrance after independent transitions to self-fertilization in Capsella. We identified a large number of compounds that are similarly changed in different selfer lineages, such that the composition of the flower scent can predict the mating system in this genus. We further demonstrate that the emission of some of these compounds convergently evolved based on mutations in different genes. In one of the Capsella selfing lineages, the loss of β-ocimene emission was caused by a mutation altering subcellular localization of the ortholog of TERPENE SYNTHASE 2 without apparent effects on its biosynthetic activity. This mutation appears to have been selected at the early stage of this selfing lineage establishment through the capture of a variant segregating in the ancestral outcrossing population. The large extent of convergence in the independent evolution of flower scent, together with the evolutionary history and molecular consequences of a causal mutation, suggest that the emission of specific volatiles has important fitness consequences in self-fertilizing plants without obvious energetic benefits.

Testing the effect of individual scent compounds on pollinator attraction in nature using quasi‐isogenic Capsella lines

“…We used two Capsella qILs (lines 11.3.2_R and 11.3.6_G), which only differ in about 10 kb around the CNL1 locus that controls the emission of benzaldehyde (BAld, see Fig. S2 of Sas et al, 2016), and two near‐isogenic lines, which differ in approximately 200 kb around the TPS2 locus causing the loss of β‐ocimene emission (Wozniak et al, 2022) (lines TPS02‐I‐234 with a recombination breakpoint between scaffold_7:9,330,436 and scaffold_7:9,354,677 and TPS02‐III‐145 with a recombination breakpoint between scaffold_7:9,452,872 and scaffold_7:9,569,768). The genetic background of the two lines was largely derived from near‐isogenic lines after backcrossing to C. rubella for several generations.…”

“…The genetic background of the two lines was largely derived from near‐isogenic lines after backcrossing to C. rubella for several generations. Plants with the C. grandiflora alleles at the CNL1 or TPS2 loci emit BAld or β‐ocimene, respectively, while plants with the C. rubella alleles do not (Sas et al, 2016; Wozniak et al, 2022).…”

“…Capsella rubella and C. orientalis show the classical selfing syndrome, with a reduction in traits associated with pollinator attraction (Sicard and Lenhard, 2011). In C. rubella , two loci have been identified that underlie the reduction in floral scent compared to C. grandiflora (Sas et al, 2016; Jantzen et al, 2019a; Wozniak et al, 2022). These, provide important genetic information for developing gene editing methods to investigate the ecological consequence of changes in pollinator‐attraction due to alteration of individual floral scent volatiles.…”

“…These, provide important genetic information for developing gene editing methods to investigate the ecological consequence of changes in pollinator‐attraction due to alteration of individual floral scent volatiles. In particular, the loss of benzaldehyde (BAld) emission in C. rubella is due to inactivating mutations in the CNL1 gene coding for cinnamate‐CoA ligase, with all tested C. rubella accessions harboring one of two independently arisen inactive haplotypes (Sas et al, 2016; Jantzen et al, 2019a; Wozniak et al, 2022). CNL1 catalyzes the first committed step toward biosynthesis of benzenoids via the peroxisomal β‐oxidative pathway.…”

“…CNL1 catalyzes the first committed step toward biosynthesis of benzenoids via the peroxisomal β‐oxidative pathway. Similarly, the loss of β‐ocimene emission in C. rubella results from inactivation of a key biosynthetic enzyme, TERPENOID SYNTHASE2 (TPS2) (Wozniak et al, 2022). In other plant species, the emission of BAld has been reported to be attractive to two types of pollinators (e.g., bees and syrphid flies) and herbivores (Theis, 2006).…”