Evolutionary walks through flower color space driven by gene expression in Petunia and allies (Petunieae)

Abstract

The structure and function of biochemical and developmental pathways determine the range of accessible phenotypes, which are the substrate for evolutionary change. Accordingly, we expect that observed phenotypic variation across species is strongly influenced by pathway structure, with different phenotypes arising due to changes in activity along pathway branches. Here we use flower color as a model to investigate how the structure of pigment pathways shapes the evolution of phenotypic diversity. We focus on the phenotypically diverse Petunieae clade in the nightshade family, which contains nearly 200 species of Petunia and related genera, as a model to understand how flavonoid pathway gene expression maps onto pigment production. We use multivariate comparative methods to estimate co-expression relationships between pathway enzymes and transcriptional regulators, and then assess how expression of these genes relates to the major axes of variation in floral pigmentation. Our results indicate that coordinated shifts in gene expression predict transitions in both total anthocyanin levels and pigment type, which, in turn, incur trade-offs with the production of UV-absorbing flavonol compounds. These findings demonstrate that the intrinsic structure of the flavonoid pathway and its regulatory architecture underlies the accessibility of pigment phenotypes and shapes evolutionary outcomes for floral pigment production.

Genetic factors explaining anthocyanin pigmentation differences

“…This comparison evaluates whether specific genes are responsible for pigmentation loss in certain lineages. The complex interplay between specific genes and their role in shaping plant pigmentation has been a subject of investigation in numerous studies[83,73,84–87] and has been experimentally tested in families such as Solanaceae[86], as well as in specific genera like Ipomoea[61,63], Iris[88], Antirrhinum[89], and Petunia[76].…”

“…These natural differences in pigmentation provide an excellent system to study evolutionary processes that lead to the inactivation of a pathway. In theory, a biosynthesis pathway could be interrupted at any of the successive steps[75], but previous research suggests that some genes are more often responsible for pigmentation loss than others[62,76]…”

“…These natural differences in pigmentation provide an excellent system to study evolutionary processes that lead to the inactivation of a pathway. In theory, a biosynthesis pathway could be interrupted at any of the successive steps [75], but previous research suggests that some genes are more often responsible for pigmentation loss than others [62,76] This raises the question whether there are "hot spots" in the pathway that are frequently the cause for a pigmentation loss; not due to higher mutation rate, but higher likelihood of mutation fixation. Specifically, we ask three questions: (1) Are anthocyanin pigmentation differences within species caused mainly by transcription factors or structural genes?…”

Multiple mechanisms explain loss of anthocyanins from betalain‐pigmented Caryophyllales, including repeated wholesale loss of a key anthocyanidin synthesis enzyme

“…Anthocyanin‐based floral coloration shows frequent transitions between different hues through changes in concentrations of red pelargonidins, purple cyanidins, and blue delphinidins (Wessinger & Rausher, 2012 ; Wheeler et al ., 2021 ). These transitions can be caused by repeated regulatory changes to the same or similar anthocyanin pathway genes (Larter et al ., 2018 ; Wheeler et al ., 2023 ). The targets of these changes appear to be constrained by pleiotropy and the structure of the anthocyanin biosynthesis pathway (Streisfeld & Rausher, 2011 ; Larter et al ., 2018 ; Wheeler et al ., 2021 ).…”

“…The targets of these changes appear to be constrained by pleiotropy and the structure of the anthocyanin biosynthesis pathway (Streisfeld & Rausher, 2011 ; Larter et al ., 2018 ; Wheeler et al ., 2021 ). Some lineages have also repeatedly evolved white flowers by loss of anthocyanins (Ho & Smith, 2016 ; Wheeler et al ., 2023 ), by diverse mechanisms (Gates et al ., 2018 ; Duncan & Rausher, 2020 ), but with predictable molecular evolutionary consequences for genes in the pathway (Ho & Smith, 2016 ). Interestingly, while some transitions to white flowers involve gene loss or loss of function in anthocyanin pathway genes (Coburn et al ., 2015 ; Lin et al ., 2022 ), others seem to involve primarily regulatory changes (Ho & Smith, 2016 ; Gates et al ., 2018 ), suggesting that some losses of anthocyanins may be more easily reversible.…”