Abstract
We identified three novel members of the R2R3‐MYB clade of anthocyanin regulators in the genome of the purple flowering Petunia inflata S6 wild accession, and we called them ANTHOCYANIN SYNTHESIS REGULATOR (ASR). Two of these genes, ASR1 and ASR2, are inactivated by two different single base mutations in their coding sequence. All three of these genes are absent in the white flowering species P. axillaris N and P. parodii, in the red flowering P. exserta, and in several Petunia hybrida lines, including R27 and W115. P. violacea and other P. hybrida lines (M1, V30, and W59) instead harbor functional copies of the ASR genes. Comparative, functional and phylogenic analysis of anthocyanin R2R3‐MYB genes strongly suggest that the ASR genes cluster is a duplication of the genomic fragment containing the other three R2R3‐MYB genes with roles in pigmentation that were previously defined, the ANTHOCYANIN4‐DEEP PURPLE‐PURPLE HAZE (AN4‐DPL‐PHZ) cluster. An investigation of the genomic fragments containing anthocyanin MYBs in different Petunia accessions reveals that massive rearrangements have taken place, resulting in large differences in the regions surrounding these genes, even in closely related species. Yeast two‐hybrid assays showed that the ASR proteins can participate in the WMBW (WRKY, MYB, B‐HLH, and WDR) anthocyanin regulatory complex by interacting with the transcription factors AN1 and AN11. All three ASRs can induce anthocyanin synthesis when ectopically expressed in P. hybrida lines, but ASR1 appeared to be the most effective. The expression patterns of ASR1 and ASR2 cover several different petunia tissues with higher expression at early stages of bud development. In contrast, ASR3 is only weakly expressed in the stigma, ovary, and anther filaments. The characterization of these novel ASR MYB genes completes the picture of the MYB members of the petunia anthocyanin regulatory MBW complex and suggests possible mechanisms of the diversification of pigmentation patterns during plant evolution.
Highlights
Pigmentation is a suitable model to study how new patterns are generated during the evolution of species
The understanding of how gene expression patterns are generated and how they diverged during evolution is an important question in both developmental and evolution biology
R2R3‐MYBs play in plants a central role in the regulation of the spatiotemporal pattern of expression of structural genes involved in the synthesis and accumulation of pigments, such as anthocyanins (Quattrocchio et al, 1999), condensed tannins (Baudry et al, 2004), betalains (Hatlestad et al, 2015), and the copigments flavonols (Sheehan et al, 2016), and are main players in determining pigmentation patterns
Summary
Pigmentation is a suitable model to study how new patterns are generated during the evolution of species. The spotted pattern of the petals of Lilium hybrids has been shown to be associated with LhMYB6 or LhMYB12 (Yamagishi, Shimoyamada, Nakatsuka, & Masuda, 2010), while in Clarkia, the expression domain of an SG6 MYB, CgMYB1, determines the position of a spot in the flower (Martins, Berg, Blinka, Rausher, & Baum, 2013; Martins, Jiang, & Rausher, 2017) These examples show that duplication and diversification of R2R3‐ MYB genes controlling anthocyanin synthesis result in different expression patterns of these regulators, leading to considerable possibilities of variation in temporal and spatial anthocyanin accumulation in plants (Albert et al, 2011; Bombarely et al, 2016; Schwinn et al, 2006). ASRs, similar to other SG6 MYB members, are involved in the WMBW regulatory complex, where they interact with AN1 and AN11 and contribute to anthocyanin synthesis by upregulating anthocyanin structural genes
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