Biology subjects

Cooley, A. M.

Publications and source records attributed to Cooley, A. M..

7 recordsLinked to original sources

bioRxiv2023

A multi-generational Turing model reproduces transgressive petal phenotypes in hybrid Mimulus.

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 inheritance in diploid gene regulatory networks composed of either homozygous or heterozygous alleles. We find that the resulting model of multi-generational Turing-type pattern formation can reproduce the transgressive petal phenotypes 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.

plant biology↗

bioRxiv2022

Protein-coding evolution does not explain divergence in petal anthocyanin pigmentation between two monkeyflower species

Phenotypic transitions in related taxa often share a common genetic basis, which suggests that there are constraints that shape the process of evolution at the genetic level. For example, noncoding changes in a gene might be favored relative to coding changes due to being 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 genus Mimulus. The magenta-flowered Mimulus luteus var. variegatus recently gained petal lobe anthocyanin pigmentation via a single-locus Mendelian difference from its sister taxon, the yellow-flowered M. l. luteus. Previous work showed that the differentially expressed transcription factor gene MYB5a/NEGAN is the single causal gene. However, it was not clear whether MYB5a coding-sequence evolution (in addition to the observed patterns of differential expression) might also have contributed to increased anthocyanin production in M. l. variegatus. Quantitative image analysis of tobacco leaves, transfected with highly expressed MYB5a coding sequence from each taxon, revealed robust anthocyanin production driven by both alleles compared to a negative control. Counter to expectations, significantly higher anthocyanin production was driven by the coding sequence from the low-anthocyanin taxon M. l. luteus. Together with previously-published expression studies, this supports the hypothesis that petal pigment in M. l. variegatus was not gained by protein-coding changes, but instead via non- coding cis-regulatory evolution. Finally, while constructing the transgenes needed for this experiment, we unexpectedly discovered two sites in MYB5a that appear to be post- transcriptionally edited - a phenomenon that has been rarely reported, and even less often explored, for nuclear-encoded plant mRNAs.

molecular biology↗

bioRxiv2022

Genetic architecture of spatially complex color patterning in hybrid Mimulus

Coloration in living organisms varies in hue, saturation, and pattern. Here we use genetic mapping to investigate all three elements in monkeyflowers Mimulus luteus var. variegatus and M. cupreus, whose flower petals differ in both yellow carotenoid and magenta anthocyanin pigmentation and whose hybrids exhibit anthocyanin pattern variation not seen in either parent. We report two QTLs associated with carotenoid intensity, and show that lighter yellow petals accumulate relatively high proportions of beta-carotene at the expense of downstream carotenoids. We propose that the derived loss of carotenoid saturation in M. l. variegatus is due to a function-reducing mutation in a Beta-Carotene Hydroxylase candidate gene, coupled with a reduction in the availability of carotenoid-storing chromoplasts influenced by the ORANGE candidate gene. We next identify five QTLs associated with the spatial patterning of anthocyanin pigment. Two QTLs, 9b and 23, each contain genes in the anthocyanin-activating subgroup of the MYB family. We hypothesize that MYB5a/NEGAN, at QTL-9b, activates spot formation in hybrids as part of a Turing-type reaction-diffusion system, while a MYB at QTL-23 activates solid, unpatterned anthocyanin pigment and may also be able to activate the variegatus allele of MYB5a/NEGAN. In addition to the apparently stochastic placement of most spots (consistent with a Turing mechanism), some pattern aspects - notably spots at the petal tips - appear to conform to a positional specification model in which spot location is predetermined. Collectively, this work begins to identify how combinations of yellow and red hues, shifts in carotenoid intensity, and two cryptic patterning systems all contribute to the complexity of color divergence between two close relatives.

genetics↗

bioRxiv2020

Genetic architecture of a body color cline in Drosophila americana

Phenotypic variation within a species is often structured geographically in clines. In Drosophila americana, a longitudinal cline for body color exists within North America that appears to be due to local adaptation. The tan and ebony genes have been hypothesized to contribute to this cline, with alleles of both genes that lighten body color found in D. americana. These alleles are similar in sequence and function to the allele fixed in D. americanas more lightly pigmented sister species, Drosophila novamexicana. To test this hypothesis, we examined the frequency and geographic distribution of D. novamexicana-like alleles of tan and ebony in D. americana. Among alleles from over 100 strains of D. americana isolated from 21 geographic locations, we failed to identify additional alleles of tan or ebony with as much sequence similarity to D. novamexicana as the alleles previously described. However, using genetic analysis of 51 D. americana strains derived from 20 geographic locations, we identified one new allele of ebony and one new allele of tan segregating in D. americana that are functionally equivalent to the D. novamexicana allele. An additional 5 alleles of tan also showed marginal evidence of functional similarity. Given the rarity of these alleles, however, we conclude that they are unlikely to be driving the pigmentation cline. Indeed, phenotypic distributions of the 51 backcross populations analyzed indicate a more complex genetic architecture, with diversity in the number and effects of loci altering pigmentation observed both within and among populations of D. americana. This genetic heterogeneity poses a challenge to association studies and genomic scans for clinal variation, but might be common in natural populations.

evolutionary biology↗

bioRxiv2020

MYB5a/NEGAN activates petal anthocyanin pigmentation and shapes the MBW regulatory network in Mimulus luteusvar. variegatus

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 DNA sequence analysis and spatiotemporal patterns of gene expression to identify MYB5a - homologous to the NEGAN transcriptional activator from M. lewisii - as a likely candidate gene within the pla2 region. Transgenic manipulation of gene expression confirms that MYB5a is both necessary and sufficient for petal lobe anthocyanin pigmentation. The deployment of MYB5a/NEGAN to the petal lobe stands in contrast to its more restricted role as a nectar guide anthocyanin activator in other Mimulus species. Transcriptome sequencing of a MYB5a RNAi line reveals the degree to which other regulators of the anthocyanin pathway - including R3 MYB repressors and bHLH and WD40 co-activators - are responsive to the level of expression of MYB5a. Overall, this work reveals that a 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 genes downstream of MYB5a but also on all of its known partners in the anthocyanin regulatory network. O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=108 SRC="FIGDIR/small/030536v3_ufig1.gif" ALT="Figure 1"> View larger version (20K): org.highwire.dtl.DTLVardef@120d538org.highwire.dtl.DTLVardef@8e6085org.highwire.dtl.DTLVardef@162f684org.highwire.dtl.DTLVardef@26860f_HPS_FORMAT_FIGEXP M_FIG Graphical abstract.Solid black arrows indicate the direction (though not magnitude) of gene expression change, following RNAi knockdown of MYB5a/NEGAN in M. l. variegatus. The number of black arrows corresponds to the number of gene copies identified in the transcriptome. Grey symbols denote positive and negative regulatory interactions. RTO is an R3 MYB protein that inhibits anthocyanin biosynthesis by sequestering bHLH proteins away from the MBW complex. C_FIG

genetics↗

bioRxiv2018

Mechanisms driving endosperm-based hybrid incompatibilities: insights from hybrid monkeyflowers

Angiosperm endosperm requires genomic and epigenomic interactions between maternal and paternal genomes for proper seed development. Genomic imprinting, an epigenetic phenomenon where the expression of certain genes is predominantly contributed by one parent, is an essential part of this process and unique to endosperm. Perturbation of imprinting can be fatal to developing seeds, and can be caused by interspecific or interploidy hybridization. However, underlying mechanisms driving these endosperm-based hybridization barriers are not well understood or described. Here we investigate the consequences of genomic imprinting in a naturally occurring interploidy and interspecies hybrid between the diploid, Mimulus guttatus, and the allotetraploid (with two subgenomes), M. luteus (Phrymaceae). We find that the two parental species differ in patterns of DNA methylation, gene expression, and imprinting. Hybrid crosses in both directions, which suffer from endosperm abnormalities and decreased germination rates, display altered methylation patterns compared to parent endosperm. Furthermore, imprinting and expression patterns appear perturbed in hybrid endosperm, where we observe global expression dominance of each of the two M. luteus subgenomes, which share similar expression patterns, over the M. guttatus genome, regardless of crossing direction. We suggest that epigenetic repatterning within the hybrid may drive global shifts in expression patterns and be the result of diverged epigenetic/regulatory landscapes between parental genomes. This may either establish or exacerbate dosage-based epistatic incompatibilities between the specific imprinting patterns that have diverged between parental species, thus driving potentially rapid endosperm-based hybridization barriers.

evolutionary biology↗

bioRxiv2016

Subgenome dominance in an interspecific hybrid, synthetic allopolyploid, and a 140 year old naturally established neo-allopolyploid monkeyflower.

The importance and applications of polyploidy have long been recognized, from shaping the evolutionary success of flowering plants to improving agricultural productivity. Recent studies have shown that one of the parental subgenomes in ancient polyploids is generally more dominant - having both retained more genes and being more highly expressed - a phenomenon termed subgenome dominance. How quickly one subgenome dominates within a newly formed polyploid, if immediate or after millions of years, and the genomic features that determine which genome dominates remain poorly understood. To investigate the rate of subgenome dominance emergence, we examined gene expression, gene methylation, and transposable element (TE) methylation in a natural less than 140 year old allopolyploid (Mimulus peregrinus), a resynthesized interspecies triploid hybrid (M. robertsii), a resynthesized allopolyploid (M. peregrinus), and diploid progenitors (M. guttatus and M. luteus). We show that subgenome expression dominance occurs instantly following the hybridization of two divergent genomes and that subgenome expression dominance significantly increases over generations. Additionally, CHH methylation levels are significantly reduced in regions near genes and within transposons in the first generation hybrid, intermediate in the resynthesized allopolyploid, and are repatterned differently between the dominant and submissive subgenomes in the natural allopolyploid. Our analyses reveal that the subgenome differences in levels of TE methylation mirror the increase in expression bias observed over the generations following the hybridization. These findings not only provide important insights into genomic and epigenomic shock that occurs following hybridization and polyploid events, but may also contribute to uncovering the mechanistic basis of heterosis and subgenomic dominance.

genomics↗