skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.


Title: A Multigenerational Turing Model Reproduces Transgressive Petal Spot Phenotypes in Hybrid Mimulus
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.  more » « less
Award ID(s):
1951646 2031275
PAR ID:
10472142
Author(s) / Creator(s):
; ; ;
Publisher / Repository:
Springer Science + Business Media
Date Published:
Journal Name:
Bulletin of Mathematical Biology
Volume:
85
Issue:
12
ISSN:
0092-8240
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. 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. 
    more » « less
  2. 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. 
    more » « less
  3. Bomblies, K (Ed.)
    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
  4. Abstract Cryptic genetic variants exert minimal phenotypic effects alone but are hypothesized to form a vast reservoir of genetic diversity driving trait evolvability through epistatic interactions1–3. This classical theory has been reinvigorated by pan-genomics, which is revealing pervasive variation within gene families,cis-regulatory regions and regulatory networks4–6. Testing the ability of cryptic variation to fuel phenotypic diversification has been hindered by intractable genetics, limited allelic diversity and inadequate phenotypic resolution. Here, guided by natural and engineeredcis-regulatory cryptic variants in a paralogous gene pair, we identified additional redundanttransregulators, establishing a regulatory network controlling tomato inflorescence architecture. By combining coding mutations withcis-regulatory alleles in populations segregating for all four network genes, we generated 216 genotypes spanning a wide spectrum of inflorescence complexity and quantified branching in over 35,000 inflorescences. Analysis of this high-resolution genotype–phenotype map using a hierarchical model of epistasis revealed a layer of dose-dependent interactions within paralogue pairs enhancing branching, culminating in strong, synergistic effects. However, we also identified a layer of antagonism between paralogue pairs, whereby accumulating mutations in one pair progressively diminished the effects of mutations in the other. Our results demonstrate how gene regulatory network architecture and complex dosage effects from paralogue diversification converge to shape phenotypic space, producing the potential for both strongly buffered phenotypes and sudden bursts of phenotypic change. 
    more » « less
  5. 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. 
    more » « less