Molecular evolution of anthocyanin pigmentation genes following losses of flower color

Abstract

BackgroundPhenotypic 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).ResultsWe 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.ConclusionsThe 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.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0675-3) contains supplementary material, which is available to authorized users.

A novel R3 MYB transcriptional repressor associated with the loss of floral pigmentation in Iochroma

“…We do not presently know the mutation(s) that caused the observed expression change in MYBL1, but if it were accomplished with a single mutation, the resulting allele could spread quickly through the population given its nearly dominant action (Haldane, 1924(Haldane, , 1927. This stands in contrast to most of the previously identified genetic changes associated with transitions to white flowers, which involve loss-of-function mutations in the R2R3 MYB activators (Quattrocchio et al, 1999;Schwinn et al, 2006;Hoballah et al, 2007). These alleles are recessive and thus would experience a lower probability of fixation, a phenomenon known as 'Haldane's Sieve' (Turner, 1981;Charlesworth, 1992).…”

“…These studies have begun to reveal predictable patterns in pigment evolution (Streisfeld & Rausher, 2011;Sobel & Streisfeld, 2013). For example, evolutionary transitions to white flowers via losses of floral anthocyanin production have consistently involved loss-of-function mutations in R2R3 MYB transcriptional activators (Quattrocchio et al, 1999;Schwinn et al, 2006;Hoballah et al, 2007). Given that a wide range of pathway mutations can give rise to white flowers (de Vlaming et al, 1984;van Houwelingen et al, 1998), this pattern has been attributed to preferential fixation of these R2R3 MYB mutations (Streisfeld & Rausher, 2011).…”

Allelic Variation and Transcriptional Isoforms of Wheat TaMYC1 Gene Regulating Anthocyanin Synthesis in Pericarp

“…This may not be surprising considering that multiple TF genes (e.g., MYB and bHLH TF genes) have been found to regulate anthocyanin biosynthesis in plants (Zhang et al, 2014 ). Additionally, molecular variations in the structural genes of anthocyanin biosynthesis can also affect AP accumulation in plant organs (Kim et al, 2009 ; Ho and Smith, 2016 ). It is possible that the white-grained parent (i.e., Opata) lacks not only a functional TaMYC1 allele but also additional genetic determinant(s) required for AP accumulation (e.g., a MYB TF gene).…”

Stepwise evolution of floral pigmentation predicted by biochemical pathway structure

“…Given that the present macroevolutionary analyses are not conditioned on previous molecular and biochemical studies, the inference that color transitions are often reversible provides independent support for the emerging consensus that flower color evolution is largely driven by changes in gene expression, which leave the structure of the pathway intact (Durbin et al. ; Ho and Smith ; Larter et al. ).…”