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Biology subjects

Visser, B.

Publications and source records attributed to Visser, B..

10 recordsLinked to original sources

Amino acids bind to phase-separating proteins and modulate biomolecular condensate stability and dynamics

AbstractBiomolecular condensates (BCs) are versatile intracellular compartments that help organize intracellular space and perform diverse biological functions. In living cells, BCs are surrounded by a complex environment, of which amino acids (AAs) are prominent components. However, it is unclear how AAs interact with condensate components and influence the formation and material properties of condensates. Here, we show that phase separation is suppressed with increasing glycine concentration by using model heterotypic condensates made of nucleophosmin 1 (NPM1) and ribosomal ribonucleic acid (RNA): the condensate density is decreased and the dynamics inside the condensate are increased. We find that glycine weakly binds to amide groups in the protein backbone and aromatic groups in the side chains with a 1[~]2 M affinity, weakening the backbone-backbone interactions between neutral and charged disordered proteins while strengthening the interactions between aromatic stickers. This leads to different modulations of the phase behaviour in condensates formed by cation/{pi}-{pi} interactions and condensates formed by charge complexation. We further show that a similar modulation effect on BCs is observed for other proteinogenic AAs and can be transferred to short peptides. These insights offer a better understanding of BC stability, with implications for new strategies to modulate the dynamic properties of BCs in vivo.

biophysics↗

Controlling interfacial protein adsorption, desorption and aggregation in biomolecular condensates

The aggregation of amyloidogenic proteins is linked to age-related diseases. The presence of interfaces can affect their aggregation mechanism, often speeding up aggregation. -Synuclein (Syn) can adsorb to biomolecular condensates, leading to heterogenous nucleation and faster aggregation. Understanding the mechanism underlying localization of amyloidogenic proteins at condensate interfaces is crucial for developing strategies to prevent or reverse their binding. We show that Syn localization to the surface of peptide-based heterotypic condensates is an adsorption process governed by the proteins condensate-amphiphilic nature. Adsorption occurs in multiple layers and levels off at micromolar concentrations. Based on these findings, we design three strategies to modulate Syn accumulation: (i) addition of biomolecules that decrease the condensate {zeta}-potential, such as NTPs and RNA, (ii) competitive adsorption of proteins targeting the condensate interface, such as G3BP1, DDX4-YFP, EGFP-NPM1, Hsp70, Hsc70, and (iii) preferential adsorption of Syn to membranes. Removing Syn from the condensate interface slows aggregation, highlighting potential cellular control over protein adsorption and implications for therapeutic strategies. Graphical abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=128 SRC="FIGDIR/small/619145v1_ufig1.gif" ALT="Figure 1"> View larger version (39K): org.highwire.dtl.DTLVardef@159b012org.highwire.dtl.DTLVardef@1369671org.highwire.dtl.DTLVardef@ced970org.highwire.dtl.DTLVardef@2578b0_HPS_FORMAT_FIGEXP M_FIG C_FIG

biophysics↗

Genome-enabled analysis of population dynamics and virulence associated loci in the oat crown rust fungus Puccinia coronata f. sp. avenae

Puccinia coronata f. sp. avenae (Pca) is an important fungal pathogen causing crown rust that impacts oat production worldwide. Genetic resistance for crop protection against Pca is often overcome by the rapid virulence evolution of the pathogen. This study investigated the factors shaping adaptive evolution of Pca using pathogen populations from distinct geographic regions within the USA and South Africa (SA). Phenotypic and genome-wide sequencing data of these diverse Pca collections, including 217 isolates, uncovered phylogenetic relationships and established distinct genetic composition between populations from northern and southern regions from the USA and SA. The population dynamics of Pca involve a bidirectional movement of inoculum between northern and southern regions of the USA and contributions from clonality and sexuality. The population from SA is solely clonal. A genome-wide association study (GWAS) employing a haplotype-resolved Pca reference genome was used to define eleven virulence-associated loci corresponding to twenty-five oat differential lines. These regions were screened to determine candidate Avr effector genes. Overall, the GWAS results allowed us to identify the underlying genetic traits controlling pathogen recognition in an oat differential set used in the USA to assign pathogen races (pathotypes). Key GWAS findings support complex genetic interactions in several oat lines suggesting allelism among resistance genes or redundancy of genes included in the differential set, multiple resistance genes recognising genetically linked Avr effector genes, or potentially epistatic relationships. A careful evaluation of the composition of the oat differential set accompanied by the development or implementation of molecular markers is recommended.

genomics↗

Inbreeding and learning affect fitness and colonization of new host plants, a behavioral innovation in the spider mite Tetranychus urticae

Habitat fragmentation increases the isolation of natural populations resulting in reduced genetic variability and increased species extinction risk. Behavioral innovation through learning, i.e., the expression of a new learned behavior in a novel context, can help animals colonize new suitable and increasingly fragmented habitats. It has remained unclear, however, how reduced genetic variability affects learning for colonizing more or less suitable habitats. Here, we show that inbreeding in a subsocial invertebrate, the spider mite Tetranychus urticae, reduces novel host plant colonization and reproductive fitness. When provided with the possibility to learn from previous experience with a host plant species, outbred mites showed aversive learning ability, but inbred mites did not adapt their behavior. We further found a putative general cost of learning in both inbred and outbred mites. Our results reveal that inbreeding affects the learning component of behavioral innovation for host plant colonization.

ecology↗

Sexual selection drives maladaptive learning under climate warming

O_LIThe impact of learning ability and sexual selection on the climate and biodiversity crisis are currently unclear. C_LIO_LIUsing the African butterfly Bicyclus anynana, which shows strong phenotypic plasticity (i.e., polyphenism) in response to temperature, we tested whether learning affects mate preferences under climate warming. C_LIO_LIWe first modelled climate warming scenarios and then showed experimentally that as temperature becomes an unreliable cue to the onset of the dry season, adult butterflies displayed the wet season rather than the dry season form. C_LIO_LIExperienced females that were exposed to different male seasonal phenotypes during sexual maturation changed sexual preferences. C_LIO_LIFemale fertilization success was reversed for naive compared to experienced females, likely reducing female fitness following climate warming. C_LIO_LIOur results emphasize the importance of sexual selection, learning, and their fitness consequences for understanding (mal)adaptation of natural populations to climate warming. C_LI

evolutionary biology↗

Mosaic evolution of molecular pathways for sex pheromone communication in a butterfly

Unraveling the origin of molecular pathways underlying the evolution of adaptive traits is essential for understanding how new lineages emerge, including the relative contribution of conserved, ancestral traits, and newly evolved, derived traits. Here, we investigated the evolutionary divergence of sex pheromone communication from moths (mostly nocturnal) to butterflies (mostly diurnal) that occurred ~98 million years ago. In moths, females typically emit pheromones to attract male mates, but in butterflies pheromones and used by females for mate choice. The molecular bases of sex pheromone communication are well understood in moths, but have remained virtually unexplored in butterflies. We used a combination of transcriptomics, real time qPCR, and phylogenetics, to identify genes involved in different steps of sex pheromone communication in the butterfly Bicyclus anynana. Our results show that the biosynthesis and reception of sex pheromones relies both on moth-specific gene families (reductases) and on more ancestral insect gene families (desaturases, olfactory receptors, odorant binding proteins). Interestingly, B. anynana further appears to use what was believed to be the moth-specific neuropeptide Pheromone Biosynthesis Activating Neuropeptide (PBAN) for regulation of sex pheromone production. Altogether, our results suggest that a mosaic pattern best explains how sex pheromone communication evolved in butterflies, with some molecular components derived from moths, and others conserved from more ancient insect ancestors. This is the first large-scale analysis of the genetic pathways underlying sex pheromone communication in a butterfly.

evolutionary biology↗

Phenotypic plasticity explains violation of Dollo's law

Over the last few decades, numerous examples have been described where a trait that was once lost during the course of evolution had been regained. Here, we argue that such reverse evolution can also become apparent when trait expression is plastic in response to the environment. We tested this hypothesis for the loss and regain of fat synthesis in parasitic wasps. Wasps from lineages that supposedly regained lipogenic ability ~80 million years ago were grown under a fat-poor or fat-rich environment. In line with our hypothesis, it turned out that fat synthesis had not been lost and regained, but was only switched on in low-fat environments. Functional protein domains of key lipogenesis genes were also found in other parasitoid species, suggesting that plasticity of fat synthesis may be more widespread in parasitoids. Individual-based simulations then revealed that a switch for plastic expression can remain functional in the genome for thousands of generations, even if it is only used sporadically. The evolution of plasticity may thus also explain other examples of apparent reverse evolution.

evolutionary biology↗

Emergence of the Ug99 lineage of the wheat stem rust pathogen through somatic hybridisation

Parasexuality contributes to diversity and adaptive evolution of haploid (monokaryotic) fungi. However non-sexual genetic exchange mechanisms are not defined in dikaryotic fungi (containing two distinct haploid nuclei). Newly emerged strains of the wheat stem rust pathogen, Puccinia graminis f. sp. tritici (Pgt), such as Ug99, are a major threat to global food security. Here we show that Ug99 arose by somatic hybridisation and nuclear exchange between dikaryons. Fully haplotype-resolved genome assembly and DNA proximity analysis revealed that Ug99 shares one haploid nucleus genotype with a much older African lineage of Pgt, with no recombination or reassortment. Generation of genetic variation by nuclear exchange may favour the evolution of dikaryotism by providing an advantage over diploidy.

genetics↗

Common practice tissue extraction in solvent does not reflect actual emission of a sex pheromone during courtship in a butterfly

Olfactory communication can be of critical importance for mate choice decisions. Lepidoptera are key model systems for understanding olfactory communication, particularly considering sex pheromone signaling in the context of sexual selection. Solvent extraction or rinsing of pheromone-producing structures is a widespread method for quantifying sex pheromones, but such measures reflect what is stored and may not represent what is actually emitted by an individual during courtship. Here, we address this point for the first time by quantifying the components of the male sex pheromone (MSP) of interacting Bicyclus anynana butterflies, a species for which much information is available onthe role played by MSPs in affecting mating success. Using headspace sampling during courtship and solvent extraction after completion of experiments using the same males, we were able to track individual traits. Our results show that solvent extracts do not reflect quantities of MSP components emitted by live butterflies. We further show that MSP amounts obtained using headspace sampling correlated with male mating success, but solvent extracts did not. Our results further strongly suggest that males actively control MSP emission when faced with increased male-male competition. Common practice solvent extracts may thus not serve as an adequate proxy for male sex pheromone signaling as they are perceived by choosy females. Our study serves as a proof of principle that quantification of male sex pheromone components depends on the method of collection, which could apply to many other insects using short-range chemical signals. This affects our understanding of how sexual selection shapes the evolution of sexually-selected chemical traits.

evolutionary biology↗

Partial restoration of mutational robustness after addition of genetic polymorphism and in the presence of sexual selection

The interaction between mutational (i.e. genetic) robustness, cryptic genetic variation and epistasis is currently under much debate, as is the question whether mutational robustness evolved under direct selection or as a by-product of environmental robustness. Here we report that mutational robustness was restored in a mutant line of the butterfly Bicyclus anynana after the spontaneous mutation, comet, appeared in a genetically polymorphic wild type population. The comet mutation modified two phenotypic traits known to be under sexual selection in this butterfly: the dorsal forewing eyespot, which is normally round, but became comet-shaped, and the androconia, the structures producing the male sex pheromone, which were reduced in size. The comet mutant line remained phenotypically stable for [~]7 seven years, but when outcrossed to the genetically polymorphic wild type population, the outcrossed comet line surprisingly recovered the wild type phenotype within 8 generations. This suggests that mutational robustness against the comet mutation was recovered in the comet outcrossed line by epistatic interactions with the genetic polymorphism originating from wild types. The extent of wild type phenotype recovery in the comet outcrossed line was trait- and developmental temperature-dependent, such that mutational robustness was partially recovered at high, but not at low developmental temperatures. We hypothesized that sexual selection through mate choice, which is sex-reversed between developmental temperatures in this butterfly, could produce mutational robustness at a high (but not at a low) temperature. Females are the choosy sex and exert stabilizing or directional selection on male secondary sexual wing traits but only at higher temperatures. Male mating success experiments under semi-natural conditions then revealed that males with the typical comet mutant phenotype suffered from lower mating success compared to wild type males, while mating success of comet males resembling wild types was partially restored. Altogether, we document the roles of cryptic genetic variation and epistasis in restoration of mutational robustness against a spontaneous mutation with known fitness effects, and we provide experimental evidence, for the first time to our knowledge, that sexual selection can produce mutational robustness.

evolutionary biology↗