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Title: 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.  more » « less
Award ID(s):
1655311 1754075 2031272 1754080
NSF-PAR ID:
10223427
Author(s) / Creator(s):
; ; ; ; ; ; ; ; ; ;
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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  1. Summary

    Petal pigmentation patterning is widespread in flowering plants. The genetics of these pattern elements has been of great interest for understanding the evolution of phenotypic diversification. Here, we investigate the genetic changes responsible for the evolution of an unpigmented petal element on a colored background.

    We used transcriptome analysis, gene expression assays, cosegregation in F2plants and functional tests to identify the gene(s) involved in petal coloration inClarkia gracilisssp.sonomensis.

    We identified an R2R3‐MYB transcription factor (CgsMYB12) responsible for anthocyanin pigmentation of the basal region (‘cup’) in the petal ofC.gracilisssp.sonomensis. A functional mutation inCgsMYB12creates a white cup on a pink petal background. Additionally, we found that twoR2R3‐MYBgenes (CgsMYB6andCgsMYB11) are also involved in petal background pigmentation. Each of these threeR2R3‐MYBgenes exhibits a different spatiotemporal expression pattern. The functionality of theseR2R3‐MYBgenes was confirmed through stable transformation ofArabidopsis.

    Distinct spatial patterns ofR2R3‐MYBexpression have created the possibility that pigmentation in different sections of the petal can evolve independently. This finding suggests that recent gene duplication has been central to the evolution of petal pigmentation patterning inC. gracilisssp.sonomensis.

     
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  3. The origin of phenotypic novelty is a perennial question of genetics and evolution. To date, few studies of biological pattern formation specifically address multi-generational aspects of inheritance and phenotypic novelty. For quantitative traits influenced by many segregating alleles, offspring phenotypes are often intermediate to parental values. In other cases, offspring phenotypes can be transgressive to parental values. For example, in the model organism Mimulus (monkeyflower), the offspring of parents with solid-colored petals exhibit novel spotted petal phenotypes. These patterns are controlled by an activator-inhibitor gene regulatory network with a small number of loci. Here we develop and analyze a model of hybridization and pattern formation that accounts for the inheritance of a diploid gene regulatory network composed of either homozygous or heterozygous alleles. We find that the resulting model of multi-generational Turing-type pattern formation can reproduce transgressive petal phenotypes similar to those observed in Mimulus. The model gives insight into how non-patterned parent phenotypes can yield phenotypically transgressive, patterned offspring, aiding in the development of empirically testable hypotheses. 
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  4. Abstract

    The origin of phenotypic novelty is a perennial question of genetics and evolution. To date, few studies of biological pattern formation specifically address multi-generational aspects of inheritance and phenotypic novelty. For quantitative traits influenced by many segregating alleles, offspring phenotypes are often intermediate to parental values. In other cases, offspring phenotypes can be transgressive to parental values. For example, in the model organismMimulus(monkeyflower), the offspring of parents with solid-colored petals exhibit novel spotted petal phenotypes. These patterns are controlled by an activator-inhibitor gene regulatory network with a small number of loci. Here we develop and analyze a model of hybridization and pattern formation that accounts for the inheritance of a diploid gene regulatory network composed of either homozygous or heterozygous alleles. We find that the resulting model of multi-generational Turing-type pattern formation can reproduce transgressive petal phenotypes similar to those observed inMimulus. The model gives insight into how non-patterned parent phenotypes can yield phenotypically transgressive, patterned offspring, aiding in the development of empirically testable hypotheses.

     
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