Evolution of Salt Tolerance in Arabidopsis Thaliana on Siliceous Soils Does Not Convey Tolerance to Saline Calcareous Soils

Purpose Alkaline salinity constrains crop yield. Previously, we found local adaptation of Arabidopsis thaliana demes to saline-siliceous soils (pH≤7) and to non-saline carbonate soils. However, any natural population of A. thaliana was localized on saline-alkaline soils. This suggests that salinity tolerance evolved on saline-siliceous soils may not confer tolerance to alkaline salinity. This hypothesis was explored by addressing physiological and molecular responses to saline-alkaline conditions of A. thaliana demes differing in salinity and carbonate tolerance.Methods A. thaliana native to saline-siliceous soils (G3), to non-saline carbonate soils (G1), or to soils with intermediate levels of these factors (G2) were cultivated in common gardens on saline-siliceous or saline-calcareous substrate. Hydroponics and irrigation experiments confirmed the phenotypes. Growth, mineral concentrations, genome differences, and expression of candidate genes were assessed in the different groups.Results G3 performed best on saline-siliceous soil and in hydroponics with salinity (pH 5.9). However, G3 was more sensitive to saline-alkaline conditions than G1 and G2. Fitness under saline-alkaline conditions was G2 > G1>G3 and G2 best maintained ion homeostasis under alkaline salinity. Whole genome scan did not differentiate among the groups, while distinctive patterns for FRO2, NINJA, and CCB4 were found and confirmed by qPCR.Conclusion In A. thaliana, salinity tolerance evolved on saline-siliceous soils does not provide tolerance to alkaline salinity. Plants from soils with intermediate conditions (G2) have more plasticity to adapt to alkaline salinity than those locally adapted to these individual stress factors. Higher expression of NINJA and CCB4 may contribute to this better adaptation.

Whole genome sequence analysis of blood lipid levels in >66,000 individuals

Plasma lipids are heritable modifiable causal factors for coronary artery disease, the leading cause of death globally. Despite the well-described monogenic and polygenic bases of dyslipidemia, limitations remain in discovery of lipid-associated alleles using whole genome sequencing, partly due to limited sample sizes, ancestral diversity, and interpretation of potential clinical significance. Increasingly larger whole genome sequence datasets with plasma lipids coupled with methodologic advances enable us to more fully catalog the allelic spectrum for lipids. Here, among 66,329 ancestrally diverse (56% non-European ancestry) participants, we associate 428M variants from deep-coverage whole genome sequences with plasma lipids. Approximately 400M of these variants were not studied in prior lipids genetic analyses. We find multiple lipid-related genes strongly associated with plasma lipids through analysis of common and rare coding variants. We additionally discover several significantly associated rare non-coding variants largely at Mendelian lipid genes. Notably, we detect rare LDLR intronic variants associated with markedly increased LDL-C, similar to rare LDLR exonic variants. In conclusion, we conducted a systematic whole genome scan for plasma lipids expanding the alleles linked to lipids for multiple ancestries and characterize a clinically-relevant rare non-coding variant model for lipids.

Whole genome scan reveals the multigenic basis of recent tidal marsh adaptation in a sparrow

Natural selection acts on functional molecular variation to create local adaptation, the “good fit” we observe between an organism’s phenotype and its environment. Genomic comparisons of lineages in the earliest stages of adaptive divergence have high power to reveal genes under natural selection because molecular signatures of selection on functional loci are maximally detectable when overall genomic divergence is low. We conducted a scan for local adaptation genes in the North American swamp sparrow (Melospiza georgiana), a species that includes geographically connected populations that are differentially adapted to freshwater vs. brackish tidal marshes. The brackish tidal marsh form has rapidly evolved tolerance for salinity, a deeper bill, and darker plumage since colonizing coastal habitats within the last 15,000 years. Despite their phenotypic differences, background genomic divergence between these populations is very low, rendering signatures of natural selection associated with this recent coastal adaptation highly detectable. We recovered a multigenic snapshot of ecological selection via a whole genome scan that revealed robust signatures of selection at 31 genes with functional connections to bill shape, plumage melanism and salt tolerance. As in Darwin’s finches, BMP signaling appears responsible for changes in bill depth, a putative magic trait for ecological speciation. A signal of selection at BNC2, a melanocyte transcription factor responsible for human skin color saturation, implicates a shared genetic mechanism for sparrow plumage color and human skin tone. Genes for salinity tolerance constituted the majority of adaptive candidates identified in this genome scan (23/31) and included vasoconstriction hormones that can flexibly modify osmotic balance in tune with the tidal cycle by influencing both drinking behavior and kidney physiology. Other salt tolerance genes had potential pleiotropic effects on bill depth and melanism (6/31), offering a mechanistic explanation for why these traits have evolved together in coastal swamp sparrows, and in other organisms that have converged on the same “salt marsh syndrome”. As a set, these candidates capture the suite of physiological changes that coastal swamp sparrows have evolved in response to selection pressures exerted by a novel and challenging habitat.