A multiscale approach to understanding the shared blue-orange flower color polymorphism in two Lysimachia species

• Published in: BMC plant biology 2024-09, Vol.24 (1), p.905-14, Article 905
• Main Authors: Sánchez-Cabrera, Mercedes, Narbona, Eduardo, Arista, Montserrat, Ortiz, Pedro L, Jiménez-López, Francisco J, Fuller, Amelia, Carter, Benjamin, Whittall, Justen B
• Format: Article
• Language: English
• Subjects: Anthocyanin; Anthocyanins - genetics; Anthocyanins - metabolism; Biochemistry; Botanical research; Climate; Color; Color of plants; Flavonoid; Flavonoids; Flavonoids - metabolism; Flower color polymorphism; Flowers; Flowers - genetics; Fruits; Gene expression; Gene Expression Regulation, Plant; Genes; Genetic aspects; Genetic polymorphisms; Interspecific hybridization; Lysimachia; Lysimachia arvensis; Lysimachia monelli; Multiscale analysis; Niches; Optical properties; Petal transcriptome; Phylogenetics; Physiological aspects; Pigmentation - genetics; Pollinators; Polymorphism; Polymorphism, Genetic; Primulaceae - genetics; Reflectance; Speciation; Species; Species Specificity; Spectra; Transcriptome; Transcriptomes
• ISSN: 1471-2229; 1471-2229
• DOI: 10.1186/s12870-024-05481-y

Polymorphisms are common in nature, but they are rarely shared among closely related species. Polymorphisms could originate through convergence, ancestral polymorphism, or introgression. Although shared neutral genomic variation across species is commonplace, few examples of shared functional traits exist. The blue-orange petal color polymorphisms in two closely related species, Lysimachia monelli and L. arvensis were investigated with UV-vis reflectance spectra, flavonoid biochemistry, and transcriptome comparisons followed by climate niche analysis. Similar color morphs between species have nearly identical reflectance spectra, flavonoid biochemistry, and ABP gene expression patterns. Transcriptome comparisons reveal two orange-specific genes directly involved in both blue-orange color polymorphisms: DFR-2 specificity redirects flux from the malvidin to the pelargonidin while BZ1-2 stabilizes the pelargonidin with glucose, producing the orange pelargonidin 3-glucoside. Moreover, a reduction of F3'5'H expression in orange petals also favors pelargonidin production. The climate niches for each color morph are the same between the two species for three temperature characteristics but differ for four precipitation variables. The similarities in reflectance spectra, biochemistry, and ABP genes suggest that a single shift from blue-to-orange shared by both lineages is the most plausible explanation. Our evidence suggests that this persistent flower color polymorphism may represent an ancestrally polymorphic trait that has transcended speciation, yet future analyses are necessary to confidently reject the alternative hypotheses.