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

Ho WW, Smith SD - BMC Evol. Biol. (2016)

Bottom Line: Phenotypic transitions, such as trait gain or loss, are predicted to carry evolutionary consequences for the genes that control their development.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).Despite the increase, the values for dN/dS in both pigmented and unpigmented lineages were consistent overall with purifying selection acting on these loci.

View Article: PubMed Central - PubMed

Affiliation: Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, USA.

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.

No MeSH data available.


Related in: MedlinePlus

Core anthocyanin biosynthetic pathway adapted from Rausher [56]. Enzymes include: CHS, chalcone synthase; CHI, chalcone isomerase; F3H, flavanone-3-hydroxylase; DFR, dihydroflavonol reductase; ANS, anthocyanidin synthase; and UF3GT, UDP-glucose flavonoid 3-O-glucosyl transferase. Several of the steps required for anthocyanin pigment production are shared with other uncolored flavonoid compounds (e.g., flavones and flavonols). The enzymes examined in this study are shaded in gray
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Fig2: Core anthocyanin biosynthetic pathway adapted from Rausher [56]. Enzymes include: CHS, chalcone synthase; CHI, chalcone isomerase; F3H, flavanone-3-hydroxylase; DFR, dihydroflavonol reductase; ANS, anthocyanidin synthase; and UF3GT, UDP-glucose flavonoid 3-O-glucosyl transferase. Several of the steps required for anthocyanin pigment production are shared with other uncolored flavonoid compounds (e.g., flavones and flavonols). The enzymes examined in this study are shaded in gray

Mentions: In order to test these possible effects of trait loss on molecular evolution, we focus on a set of three anthocyanin pathway genes, Chi (chalcone isomerase), F3h (flavanone-3-hydroxylase), and Dfr (dihydroflavonol-4-reductase). The Dfr gene represents the most downstream step among these three, and it appears to be exclusively involved in anthocyanin biosynthesis in Solanaceae ([42], Fig. 2). Thus, it might be predicted to experience the strongest effects of relaxed constraint following loss of floral anthocyanins. By contrast, the other two upstream enzymes are required for the production of multiple flavonoids, including anthocyanins, flavones, and flavonols (Fig. 2). The uncolored flavones and flavonols are primarily involved in responses to UV stress [43, 44], but also play a role in male fertility and signaling in some species [45, 46]. Thus, Chi and F3h might remain under purifying selection despite the loss of floral pigmentation because of their pathway position and functional significance. The dynamics of Chi evolution may also be influenced by the fact that, unlike the single copy Dfr and F3h, this enzyme is encoded by two loci (Chi-A, the principally active copy, and Chi-B, only expressed in young anthers) [47, 48]. In this analysis, we focus on the Chi-A copy (hereafter ‘Chi’) that is required for floral pigmentation in Solanaceae [48, 49]. The extent to which these genes experience relaxed selective pressures following the loss of floral pigmentation has important consequences for the evolutionary trajectory of these plant lineages, as the molecular decay of any of these loci would significantly reduce the potential for future regain of this trait.Fig. 2


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

Ho WW, Smith SD - BMC Evol. Biol. (2016)

Core anthocyanin biosynthetic pathway adapted from Rausher [56]. Enzymes include: CHS, chalcone synthase; CHI, chalcone isomerase; F3H, flavanone-3-hydroxylase; DFR, dihydroflavonol reductase; ANS, anthocyanidin synthase; and UF3GT, UDP-glucose flavonoid 3-O-glucosyl transferase. Several of the steps required for anthocyanin pigment production are shared with other uncolored flavonoid compounds (e.g., flavones and flavonols). The enzymes examined in this study are shaded in gray
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4862180&req=5

Fig2: Core anthocyanin biosynthetic pathway adapted from Rausher [56]. Enzymes include: CHS, chalcone synthase; CHI, chalcone isomerase; F3H, flavanone-3-hydroxylase; DFR, dihydroflavonol reductase; ANS, anthocyanidin synthase; and UF3GT, UDP-glucose flavonoid 3-O-glucosyl transferase. Several of the steps required for anthocyanin pigment production are shared with other uncolored flavonoid compounds (e.g., flavones and flavonols). The enzymes examined in this study are shaded in gray
Mentions: In order to test these possible effects of trait loss on molecular evolution, we focus on a set of three anthocyanin pathway genes, Chi (chalcone isomerase), F3h (flavanone-3-hydroxylase), and Dfr (dihydroflavonol-4-reductase). The Dfr gene represents the most downstream step among these three, and it appears to be exclusively involved in anthocyanin biosynthesis in Solanaceae ([42], Fig. 2). Thus, it might be predicted to experience the strongest effects of relaxed constraint following loss of floral anthocyanins. By contrast, the other two upstream enzymes are required for the production of multiple flavonoids, including anthocyanins, flavones, and flavonols (Fig. 2). The uncolored flavones and flavonols are primarily involved in responses to UV stress [43, 44], but also play a role in male fertility and signaling in some species [45, 46]. Thus, Chi and F3h might remain under purifying selection despite the loss of floral pigmentation because of their pathway position and functional significance. The dynamics of Chi evolution may also be influenced by the fact that, unlike the single copy Dfr and F3h, this enzyme is encoded by two loci (Chi-A, the principally active copy, and Chi-B, only expressed in young anthers) [47, 48]. In this analysis, we focus on the Chi-A copy (hereafter ‘Chi’) that is required for floral pigmentation in Solanaceae [48, 49]. The extent to which these genes experience relaxed selective pressures following the loss of floral pigmentation has important consequences for the evolutionary trajectory of these plant lineages, as the molecular decay of any of these loci would significantly reduce the potential for future regain of this trait.Fig. 2

Bottom Line: Phenotypic transitions, such as trait gain or loss, are predicted to carry evolutionary consequences for the genes that control their development.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).Despite the increase, the values for dN/dS in both pigmented and unpigmented lineages were consistent overall with purifying selection acting on these loci.

View Article: PubMed Central - PubMed

Affiliation: Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, USA.

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.

No MeSH data available.


Related in: MedlinePlus