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ABSTRACT Biologists have long been interested in understanding genetic constraints on the evolution of development. For example, noncoding changes in a gene might be favored over coding changes if they are less constrained by pleiotropic effects. Here, we evaluate the importance of coding‐sequence changes to the recent evolution of a novel anthocyanin pigmentation trait in the monkeyflower genusMimulus. The magenta‐floweredMimulus luteusvar.variegatusrecently gained petal lobe anthocyanin pigmentation via a single‐locus Mendelian difference from its sister taxon, the yellow‐floweredM. l. luteus. Previous work showed that the differentially expressed transcription factor geneMYB5a/NEGANis the single causal gene. However, it was not clear whetherMYB5acoding‐sequence evolution (in addition to the observed patterns of differential expression) might also have contributed to increased anthocyanin production inM. l. variegatus. Quantitative image analysis of tobacco leaves, transfected withMYB5acoding sequence from each taxon, revealed robust anthocyanin production driven by both alleles. Counter to expectations, significantly higher anthocyanin production was driven by the allele from the low‐anthocyaninM. l. luteus, a result that was confirmed through both a replication of the initial study and analysis by an alternative method of spectrophotometry on extracted leaf anthocyanins. Together with previously published expression studies, our findings support the hypothesis that petal pigment inM. l. variegatuswas not gained by protein‐coding changes, but instead solely via noncoding cis‐regulatory evolution. Finally, while constructing the transgenes needed for this experiment, we unexpectedly discovered two sites inMYB5athat appear to be post‐transcriptionally edited—a phenomenon that has been rarely reported, and even less often explored, for nuclear‐encoded plant mRNAs.
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The regulatory network for petal anthocyanin pigmentation is shaped by the MYB5a/NEGAN transcription factor in Mimulus
Abstract Much of the visual diversity of angiosperms is due to the frequent evolution of novel pigmentation patterns in flowers. The gene network responsible for anthocyanin pigmentation, in particular, has become a model for investigating how genetic changes give rise to phenotypic innovation. In the monkeyflower genus Mimulus, an evolutionarily recent gain of petal lobe anthocyanin pigmentation in M. luteus var. variegatus was previously mapped to genomic region pla2. Here, we use sequence and expression analysis, followed by transgenic manipulation of gene expression, to identify MYB5a—orthologous to the NEGAN transcriptional activator from M. lewisii—as the gene responsible for the transition to anthocyanin-pigmented petals in M. l. variegatus. In other monkeyflower taxa, MYB5a/NEGAN is part of a reaction-diffusion network that produces semi-repeating spotting patterns, such as the array of spots in the nectar guides of both M. lewisii and M. guttatus. Its co-option for the evolution of an apparently non-patterned trait—the solid petal lobe pigmentation of M. l. variegatus—illustrates how reaction-diffusion can contribute to evolutionary novelty in non-obvious ways. Transcriptome sequencing of a MYB5a RNAi line of M. l. variegatus reveals that this genetically simple change, which we hypothesize to be a regulatory mutation in cis to MYB5a, has cascading effects on gene expression, not only on the enzyme-encoding genes traditionally thought of as the targets of MYB5a but also on all of its known partners in the anthocyanin regulatory network.
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- PAR ID:
- 10223427
- Editor(s):
- Bomblies, K
- Date Published:
- Journal Name:
- Genetics
- Volume:
- 217
- Issue:
- 2
- ISSN:
- 1943-2631
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1093/genetics/iyaa036
