Auxin-driven ecophysiological diversification of leaves in domesticated tomato

The study of crop diversification has focussed mainly on the genetic changes underlying traits favoured by humans. However, the passage from natural habitats to agronomic settings probably operated changes beyond those comprising the classical domestication syndrome. A deeper understanding of these traits and their genetic signature would be valuable to inform conventional crop breeding and de novo domestication of crop wild relatives. Heterobaric leaves have bundle sheath extensions (BSEs) that compartmentalise the sub-stomatal cavity whereas homobaric leaves do not; BSE development is known to be controlled by the OBSCURAVENOSA (OBV) locus and the obv mutant lacks BSEs whereas leaves carrying the wild type allele have BSEs. Here we identify a non-synonymous amino acid change in the OBV gene that exists as a rare balanced polymorphism in the natural range of wild tomatoes, but has increased in frequency in domesticated tomatoes, suggesting that the latter diversified into heterobaric and homobaric leaf types. The mutation disrupts a C2H2 zinc finger motif in the OBV protein, resulting in the absence of BSEs in leaves and here we show that this and other pleiotropic effects, including changes in leaf insertion angle, leaf margin serration, minor vein density and fruit shape, are controlled by OBV via changes in auxin signalling. Loss of function of the transcriptional regulator AUXIN RESPONSE FACTOR (ARF4) also results in defective BSE development, revealing an additional component of a novel genetic module controlling aspects of leaf development important for ecological adaptation and subject to breeding selections.

A supergene underlies linked variation in color and morphology in a Holarctic songbird

The genetic architecture of a phenotype can have considerable effects on the evolution of a trait or species. Characterizing genetic architecture provides insight into the complexity of a given phenotype and, potentially, the role of the phenotype in evolutionary processes like speciation. We use genome sequences to investigate the genetic basis of phenotypic variation in redpoll finches (Acanthis spp.). We demonstrate that variation in redpoll phenotype is broadly controlled by a ~55-Mb chromosomal inversion. Within this inversion, we find multiple candidate genes related to melanogenesis, carotenoid coloration, and bill shape, suggesting the inversion acts as a supergene controlling multiple linked traits. A latitudinal gradient in ecotype distribution suggests supergene driven variation in color and bill morphology are likely under environmental selection, maintaining supergene haplotypes as a balanced polymorphism. Our results provide a mechanism for the maintenance of ecotype variation in redpolls despite a genome largely homogenized by gene flow.

Equatorial to Polar genomic variability of the microalgae Bathycoccus prasinos

The importance of marine phytoplankton in food webs and biogeochemical cycles makes the study of prokaryotic and eukaryotic phytoplankton species essential to understand changes in the global ecosystem. As plankton is transported by ocean currents, its community composition varies. Some species are abundant in contrasting environments, which raises the question of the genomic basis of their adaptation. Here we exploit the cosmopolitan distribution of the eukaryotic picoalgae Bathycoccus prasinos to investigate its genomic variations among temperate and polar populations. Using multiple metagenomic data, we found that ~5% of genomic positions of B. prasinos are variable, with an overwhelming majority of biallelic patterns. Cold and temperate waters are clearly associated with changes in variant occurrences including striking differences at some non-synonymous positions of several genes. Data from transitional waters showed more balanced polymorphism at most of these positions. The comparison of mesophilic and psychrophilic gene variants of this species suggests that its adaptation to cold waters may involve few amino acid changes at positions of protein structures critical for physical and functional properties. These results provide new insights into the genomic diversity and temperature-associated amino acid changes of a cosmopolitan eukaryotic planktonic species.

Pooled Single-Molecule transcriptomics identifies a giant gene under balancing selection in sunflower

SummaryGenes under balancing selection control phenotypes such as immunity, color or sex, but are difficult to identify. Self-incompatibility genes are under negative frequency-dependent selection, a special case of balancing selection, with up to 30 to 50 alleles segregating per population. We developed a method based on pooled Single-Molecule transcriptomics to identify balanced polymorphisms expressed in tissues of interest. We searched for multi-allelic, non-recombining genes causing self-incompatibility in wild sunflower (Helianthus annuus). A diversity scan in pistil identified a gene,Ha7650b,that displayed balanced polymorphism and colocalized with a quantitative trait locus for self-incompatibility. Unexpectedly,Ha7650bdisplayed gigantism (400 kb), which was caused by increase in intron size as a consequence of suppressed recombination.Ha7650bemerged after a whole-genome duplication (29 millions years ago) followed by tandem duplications and neofunctionalisation.Ha7650bshows expression, genetic location, genomic neighbourhood and predicted function that provide strong evidence that it is involved in self-incompatibility. Pooled Single-Molecule transcriptomics is an affordable and powerful new method that makes it possible to identify diversity and structural outliers simultaneously. It will allow a breakthrough in the discovery of self-incompatibility genes and other expressed genes under balancing selection.

Transspecies beak color polymorphism in the Darwin’s finch radiation

Carotenoid-based polymorphisms are widespread in populations of birds, fish, and reptiles1, but little is known of how they affect fitness and are maintained as species multiply2. We report a combined field and molecular-genetic investigation of a nestling beak color polymorphism in Darwin’s finches. Beaks are pink or yellow, and yellow is recessive3. Here we show that the polymorphism arose in the Galápagos approximately half a million years ago through a regulatory mutation in the BCO2 gene, and is shared by 14 descendant species. The frequency of the yellow genotype is associated with cactus flower abundance in cactus finches, and is altered by introgressive hybridization. The polymorphism is most likely a balanced polymorphism, maintained by ecological selection pressures associated with diet, and augmented by occasional interspecific introgression. Polymorphisms that are hidden as adults, as here, may contribute to evolutionary diversification in underappreciated ways in other systems.

Two Genetic Differences between Closely Related Zika Virus Strains Determine Pathogenic Outcome in Mice

ABSTRACT Recent Zika virus (ZIKV) outbreaks and unexpected clinical manifestations of ZIKV infection have prompted an increase in ZIKV-related research. Here, we identify two strain-specific determinants of ZIKV virulence in mice. We found that strain H/PF/2013 caused 100% lethality in Ifnar1−/− mice, whereas PRVABC59 caused no lethality; both strains caused 100% lethality in Ifnar1−/− Ifngr1−/− double-knockout (DKO) mice. Deep sequencing revealed a high-frequency variant in PRVABC59 not present in H/PF/2013: a G-to-T change at nucleotide 1965 producing a Val-to-Leu substitution at position 330 of the viral envelope (E) protein. We show that the V330 variant is lethal on both virus strain backgrounds, whereas the L330 variant is attenuating only on the PRVABC59 background. These results identify a balanced polymorphism in the E protein that is sufficient to attenuate the PRVABC59 strain but not H/PF/2013. The consensus sequences of H/PF/2013 and PRVABC59 differ by 3 amino acids, but these were not responsible for the difference in virulence between the two strains. H/PF/2013 and PRVABC59 differ by an additional 31 noncoding or silent nucleotide changes. We made a panel of chimeric viruses with identical amino acid sequences but nucleotide sequences derived from H/PF/2013 or PRVABC59. We found that 6 nucleotide differences in the 3′ quarter of the H/PF/2013 genome were sufficient to confer virulence in Ifnar1−/− mice. Altogether, our work identifies a large and previously unreported difference in virulence between two commonly used ZIKV strains, in two widely used mouse models of ZIKV pathogenesis (Ifnar1−/− and Ifnar1−/− Ifngr1−/− DKO mice). IMPORTANCE Contemporary ZIKV strains are closely related and often used interchangeably in laboratory research. Here, we identify two strain-specific determinants of ZIKV virulence that are evident in only Ifnar1−/− mice but not Ifnar1−/− Ifngr1−/− DKO mice. These results identify a balanced polymorphism in the E protein that is sufficient to attenuate the PRVABC59 strain but not H/PF/2013. We further identify a second virulence determinant in the H/PF/2013 strain, which is driven by the viral nucleotide sequence but not the amino acid sequence. Altogether, our work identifies a large and previously unreported difference in virulence between two commonly used ZIKV strains, in two widely used mouse models of ZIKV pathogenesis. Our results highlight that even very closely related virus strains can produce significantly different pathogenic phenotypes in common laboratory models.

Domain-Specific Antibodies Reveal Differences in the Membrane Topologies of Apolipoprotein L1 in Serum and Podocytes

BackgroundCirculating APOL1 lyses trypanosomes, protecting against human sleeping sickness. Two common African gene variants of APOL1, G1 and G2, protect against infection by species of trypanosomes that resist wild-type APOL1. At the same time, the protection predisposes humans to CKD, an elegant example of balanced polymorphism. However, the exact mechanism of APOL1-mediated podocyte damage is not clear, including APOL1's subcellular localization, topology, and whether the damage is related to trypanolysis.MethodsAPOL1 topology in serum (HDL particles) and in kidney podocytes was mapped with flow cytometry, immunoprecipitation, and trypanolysis assays that tracked 170 APOL1 domain-specific monoclonal antibodies. APOL1 knockout podocytes confirmed antibody specificity.ResultsAPOL1 localizes to the surface of podocytes, with most of the pore-forming domain (PFD) and C terminus of the Serum Resistance Associated-interacting domain (SRA-ID), but not the membrane-addressing domain (MAD), being exposed. In contrast, differential trypanolytic blocking activity reveals that the MAD is exposed in serum APOL1, with less of the PFD accessible. Low pH did not detectably alter the gross topology of APOL1, as determined by antibody accessibility, in serum or on podocytes.ConclusionsOur antibodies highlighted different conformations of native APOL1 topology in serum (HDL particles) and at the podocyte surface. Our findings support the surface ion channel model for APOL1 risk variant–mediated podocyte injury, as well as providing domain accessibility information for designing APOL1-targeted therapeutics.

Long-read bitter gourd (Momordica charantia) genome and the genomic architecture of nonclassic domestication

The genetic architecture of quantitative traits is determined by both Mendelian and polygenic factors, yet classic examples of plant domestication focused on selective sweep of newly mutated Mendelian genes. Here we report the chromosome-level genome assembly and the genomic investigation of a nonclassic domestication example, bitter gourd (Momordica charantia), an important Asian vegetable and medicinal plant of the family Cucurbitaceae. Population resequencing revealed the divergence between wild and South Asian cultivars about 6,000 y ago, followed by the separation of the Southeast Asian cultivars about 800 y ago, with the latter exhibiting more extreme trait divergence from wild progenitors and stronger signs of selection on fruit traits. Unlike some crops where the largest phenotypic changes and traces of selection happened between wild and cultivar groups, in bitter gourd large differences exist between two regional cultivar groups, likely reflecting the distinct consumer preferences in different countries. Despite breeding efforts toward increasing female flower proportion, a gynoecy locus exhibits complex patterns of balanced polymorphism among haplogroups, with potential signs of selective sweep within haplogroups likely reflecting artificial selection and introgression from cultivars back to wild accessions. Our study highlights the importance to investigate such nonclassic example of domestication showing signs of balancing selection and polygenic trait architecture in addition to classic selective sweep in Mendelian factors.