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Molecular evolution of anthocyanin pigmentation genes following losses of flower color.

ABSTRACT: BACKGROUND:Phenotypic transitions, such as trait gain or loss, are predicted to carry evolutionary consequences for the genes that control their development. For example, trait losses can result in molecular decay of the pathways underlying the trait. Focusing on the Iochrominae clade (Solanaceae), we examine how repeated losses of floral anthocyanin pigmentation associated with flower color transitions have affected the molecular evolution of three anthocyanin pathway genes (Chi, F3h, and Dfr). RESULTS:We recovered intact coding regions for the three genes in all of the lineages that have lost floral pigmentation, suggesting that molecular decay is not associated with these flower color transitions. However, two of the three genes (Chi, F3h) show significantly elevated dN/dS ratios in lineages without floral pigmentation. Maximum likelihood analyses suggest that this increase is due to relaxed constraint on anthocyanin genes in the unpigmented lineages as opposed to positive selection. Despite the increase, the values for dN/dS in both pigmented and unpigmented lineages were consistent overall with purifying selection acting on these loci. CONCLUSIONS:The broad conservation of anthocyanin pathway genes across lineages with and without floral anthocyanins is consistent with the growing consensus that losses of pigmentation are largely achieved by changes in gene expression as opposed to structural mutations. Moreover, this conservation maintains the potential for regain of flower color, and indicates that evolutionary losses of floral pigmentation may be readily reversible.

SUBMITTER: Ho WW

PROVIDER: S-EPMC4862180 | biostudies-literature | 2016 May

REPOSITORIES: biostudies-literature

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Molecular evolution of anthocyanin pigmentation genes following losses of flower color.

Ho Winnie W WW Smith Stacey D SD

BMC evolutionary biology 20160510

<h4>Background</h4>Phenotypic transitions, such as trait gain or loss, are predicted to carry evolutionary consequences for the genes that control their development. For example, trait losses can result in molecular decay of the pathways underlying the trait. Focusing on the Iochrominae clade (Solanaceae), we examine how repeated losses of floral anthocyanin pigmentation associated with flower color transitions have affected the molecular evolution of three anthocyanin pathway genes (Chi, F3h, a ...[more]

PMID: 27161359

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Project description:BackgroundThe Rhododendron sanguineum complex is endemic to alpine mountains of northwest Yunnan and southeast Tibet of China. Varieties in this complex exhibit distinct flower colors even at the bud stage. However, the underlying molecular regulations for the flower color variation have not been well characterized. Here, we investigated this via measuring flower reflectance profiles and comparative transcriptome analyses on three coexisting varieties of the R. sanguineum complex, with yellow flush pink, bright crimson, and deep blackish crimson flowers respectively. We compared the expression levels of differentially-expressed-genes (DEGs) of the anthocyanin / flavonoid biosynthesis pathway using RNA-seq and qRT-PCR data. We performed clustering analysis based on transcriptome-derived Single Nucleotide Polymorphisms (SNPs) data, and finally analyzed the promoter architecture of DEGs.ResultsReflectance spectra of the three color morphs varied distinctively in the range between 400 and 700 nm, with distinct differences in saturation, brightness, hue, and saturation/hue ratio, an indirect measurement of anthocyanin content. We identified 15,164 orthogroups that were shared among the three varieties. The SNP clustering analysis indicated that the varieties were not monophyletic. A total of 40 paralogous genes encoding 12 enzymes contributed to the flower color polymorphism. These anthocyanin biosynthesis-related genes were associated with synthesis, modification and transportation properties (RsCHS, RsCHI, RsF3H, RsF3'H, RsFLS, RsANS, RsAT, RsOMT, RsGST), as well as genes involved in catabolism and degradation (RsBGLU, RsPER, RsCAD). Variations in sequence and cis-acting elements of these genes might correlate with the anthocyanin accumulation, thus may contribute to the divergence of flower color in the R. sanguineum complex.ConclusionsOur results suggested that the varieties are very closely related and flower color variations in the R. sanguineum complex correlate tightly with the differential expression levels of genes involved in the anabolic and catabolic synthesis network of anthocyanin. Our study provides a scenario involving intricate relationships between genetic mechanisms for floral coloration accompanied by gene flow among the varieties that may represent an early case of pollinator-mediated incipient sympatric speciation.

Project description:Background and aimsAngiosperms display remarkable diversity in flower colour, implying that transitions between pigmentation phenotypes must have been common. Despite progress in understanding transitions between anthocyanin (blue, purple, pink or red) and unpigmented (white) flowers, little is known about the evolutionary patterns of flower-colour transitions in lineages with both yellow and anthocyanin-pigmented flowers. This study investigates the relative rates of evolutionary transitions between different combinations of yellow- and anthocyanin-pigmentation phenotypes in the tribe Antirrhineae.MethodsWe surveyed taxonomic literature for data on anthocyanin and yellow floral pigmentation for 369 species across the tribe. We then reconstructed the phylogeny of 169 taxa and used phylogenetic comparative methods to estimate transition rates among pigmentation phenotypes across the phylogeny.Key resultsIn contrast to previous studies we found a bias towards transitions involving a gain in pigmentation, although transitions to phenotypes with both anthocyanin and yellow taxa are nevertheless extremely rare. Despite the dominance of yellow and anthocyanin-pigmented taxa, transitions between these phenotypes are constrained to move through a white intermediate stage, whereas transitions to double-pigmentation are very rare. The most abundant transitions are between anthocyanin-pigmented and unpigmented flowers, and similarly the most abundant polymorphic taxa were those with anthocyanin-pigmented and unpigmented flowers.ConclusionsOur findings show that pigment evolution is limited by the presence of other floral pigments. This interaction between anthocyanin and yellow pigments constrains the breadth of potential floral diversity observed in nature. In particular, they suggest that selection has repeatedly acted to promote the spread of single-pigmented phenotypes across the Antirrhineae phylogeny. Furthermore, the correlation between transition rates and polymorphism suggests that the forces causing and maintaining variance in the short term reflect evolutionary processes on longer time scales.

Project description:BackgroundA puzzle in evolution is the understanding of how the environment might drive subtle phenotypic variation, and whether this variation is adaptive. Under the neutral evolutionary theory, subtle phenotypes are almost neutral with little adaptive value. To test this idea, we studied the infraspecific variation in flower shape and color in Mammillaria haageana, a species with a wide geographical distribution and phenotypic variation, which populations are often recognized as infraspecific taxa.ResultsWe collected samples from wild populations, kept them in the greenhouse for at least one reproductive year, and collected newly formed flowers. Our first objective was to characterize tepal natural variation in M. haageana through geometric morphometric and multivariate pigmentation analyses. We used landmark-based morphometrics to quantify the trends of shape variation and tepal color-patterns in 20 M. haageana accessions, belonging to five subspecies, plus 8 M. albilanata accessions for comparison as the sister species. We obtained eight geometric morphometric traits for tepal shape and color-patterns. We found broad variation in these traits between accessions belonging to the same subspecies, without taxonomic congruence with those infraspecific units. Also the phenetic cluster analysis showed different grouping patterns among accessions. When we correlated these phenotypes to the environment, we also found that solar radiation might explain the variation in tepal shape and color, suggesting that subtle variation in flower phenotypes might be adaptive. Finally we present anatomical sections in M. haageana subsp. san-angelensis to propose some of the underlying tepal structural features that may give rise to tepal variation.ConclusionsOur geometric morphometric approach of flower shape and color allowed us to identify the main trends of variation in each accession and putative subspecies, but also allowed us to correlate these variation to the environment, and propose anatomical mechanisms underlying this diversity of flower phenotypes.

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Molecular evolution of anthocyanin pigmentation genes following losses of flower color.

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Molecular evolution of anthocyanin pigmentation genes following losses of flower color.

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