Between species, these mutations typically occur in transcription factors which leads to downregulation of anthocyanin biosynthetic genes ( Quattrocchio et al., 1999 Schwinn et al., 2006 Hoballah et al., 2007 Lowry et al., 2012 Streisfeld et al., 2013 Yuan et al., 2013b Esfeld et al., 2018). Losses of pigmentation tend to be relatively simple, with loss-of-function mutations in single genes of major phenotypic effect. In floral color adaptation there are three general types of phenotypic transitions as follows: loss of color, shifts in color hue, and gain of color ( Rausher, 2008). Extensive knowledge of flavonoid pathway biosynthesis and regulation provides a foundation to study process of floral color evolution.
Flavonoids are synthesized as a part of the complex metabolic network of phenylpropanoids, which includes a large variety of primary and secondary compounds, such as lignins, volatile signals, developmental regulators, and defense compounds ( Winkel, 2006 Yang et al., 2017).
The two most common branches of the flavonoid pathway are the anthocyanins (red, purple, and blue pigments responsible for visible color) and flavonols (responsible for ultraviolet color). Many studies have demonstrated the importance of flower color for pollinators ( Yuan et al., 2013a) and some have directly linked single genes to pollinator preference ( Hoballah et al., 2007 Hopkins and Rausher, 2011 Yuan et al., 2013b Sheehan et al., 2016 Kellenberger et al., 2019).Īnthocyanins are the major floral pigments in the angiosperms and are produced by the flavonoid pathway ( Winkel-Shirley, 2001).
Color is a trait that can be easily be quantitated and monitored in different tissues during development. Adaptation to shifts in pollinator availability is widely accepted to be a driving force in the rapid diversification of the angiosperms ( Johnson, 2006 Sapir and Armbruster, 2010 Schiestl and Johnson, 2013 van der Niet et al., 2014). The relative importance of such large-effect mutations, however, remains contentious ( Rockman, 2012) highlighting the need to examine genetic mechanisms with a critical eye.Ī prime example of the relevance of mutations of large phenotypic effect has been pollinator-mediated selection on floral traits. At the same time, evidence for adaptation proceeding via few loci of large effect also abounds ( Doebley, 2004 Hoekstra et al., 2006 Nadeau et al., 2016 Todesco et al., 2020). Today, there is abundant experimental evidence that the genetic basis of natural variation in individual traits can be extremely complex with many loci involved ( Atwell et al., 2010 Chan et al., 2010 Turchin et al., 2012 Kooke et al., 2016 Guo et al., 2018 Sohail et al., 2019). However, contemporaries of Fisher as well as more recent theory suggest that a single bout of adaptation could involve loci with a distribution of effect sizes, with both large-effect and small-effect mutations ( Orr, 1998 Orteu and Jiggins, 2020). In his theoretical work, Fisher predicted that mutations of small effect were most likely to produce phenotypes with increased fitness ( Fisher, 1918, 1930). Whether adaptation involves single genes of large phenotypic effect or proceeds through many genes with small individual effects is a crucial question in evolutionary biology ( Orr and Coyne, 1992 Orr, 2005 Chevin and Beckerman, 2012 Barton et al., 2016 Boyle et al., 2017). This study presents a rare case of a genetically complex evolutionary transition toward the gain of a novel red color. Furthermore, the downregulation of an acyltransferase promotes reddish hues in typically purple pigments by preventing acyl group decoration of anthocyanins. An essential shift in anthocyanin hydroxylation occurred through rebalancing the expression of three hydroxylating genes. We show that moderate upregulation and a shift in tissue specificity of an AN2 paralog, DEEP PURPLE, restores anthocyanin biosynthesis in P.
exserta retains a nonfunctional copy of the key MYB transcription factor AN2. The presence of a red color is remarkable because the genus cannot synthesize red anthocyanins and P. Here we report on the complex evolution of a novel red floral color in the hummingbird-pollinated Petunia exserta (Solanaceae) from a colorless ancestor. The majority of evolutionary transitions to red color proceeded from purple lineages and tend to be genetically simple, almost always involving a few loss-of-function mutations of major phenotypic effect. Red flower color has arisen multiple times and is generally associated with hummingbird pollination.
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