The genomics and physiology of abiotic stressors associated with global elevational gradients in Arabidopsis thaliana.

Phenotypic and genomic diversity in Arabidopsis thaliana may be associated with adaptation along its wide elevational range, but it is unclear whether elevational clines are consistent among different mountain ranges. We took a multi-regional view of selection associated with elevation. In a diverse panel of ecotypes, we measured plant traits under alpine stressors (low CO2 partial pressure, high light, and night freezing) and conducted genome-wide association studies. We found evidence of contrasting locally adaptive regional clines. Western Mediterranean ecotypes showed low water use efficiency (WUE)/early flowering at low elevations to high WUE/late flowering at high elevations. Central Asian ecotypes showed the opposite pattern. We mapped different candidate genes for each region, and some quantitative trait loci (QTL) showed elevational and climatic clines likely maintained by selection. Consistent with regional heterogeneity, trait and QTL clines were evident at regional scales (c. 2000 km) but disappeared globally. Antioxidants and pigmentation rarely showed elevational clines. High elevation east African ecotypes might have higher antioxidant activity under night freezing. Physiological and genomic elevational clines in different regions can be unique, underlining the complexity of local adaptation in widely distributed species, while hindering global trait-environment or genome-environment associations. To tackle the mechanisms of range-wide local adaptation, regional approaches are thus warranted.

La diversidad fenotípica y genómica en Arabidopsis thaliana puede estar asociada con la adaptación a lo largo de su amplio rango de elevación, pero no está claro si la variación asociada a la elevación es consistente entre diferentes cadenas montañosas. Investigamos la selección asociada con la elevación tomando una visión multiregional. En un panel diverso de ecotipos, medimos fenotipos bajo condiciones estresantes alpinas (baja presión parcial de CO2, mucha luz y congelación nocturna) y realizamos estudios de asociación con el genoma. Encontramos evidencia de clinas de elevación regionales contrastantes. Los ecotipos del Mediterráneo occidental mostraron una eficiencia de uso de agua baja/floración temprana en elevaciones bajas y una eficiencia de uso de agua alta/floración tardía en elevaciones altas. Los ecotipos de Asia Central mostraron el patrón opuesto. Mapeamos diferentes genes candidatos para cada región, y algunos locus mostraron variación en elevación probablemente mantenida por selección. De acuerdo con heterogeneidad regional, las clinas de fenotipo y de frecuencia alélica fueron evidentes a escalas regionales (~2000 km) pero desaparecieron a nivel global. Los antioxidantes y la pigmentación rara vez mostraron clinas, aunque los ecotipos de alta elevación del este de África podrían tener una mayor actividad antioxidante bajo congelación nocturna. Las clinas de elevación fisiológicas y genómicas en diferentes regiones pueden ser únicas, lo que subraya la complejidad de la adaptación local en especies ampliamente distribuidas, al tiempo que obstaculiza las asociaciones globales fenotipo­ambiente o genoma­ambiente. Por lo tanto, para abordar los mecanismos de adaptación local a gran escala, se necesitan enfoques regionales.

Effects of genomic and functional diversity on stand-level productivity and performance of non-native Arabidopsis.

Biodiversity can affect the properties of groups of organisms, such as ecosystem function and the persistence of colonizing populations. Genomic data offer a newly available window to diversity, complementary to other measures like taxonomic or phenotypic diversity. We tested whether native genetic diversity in field experimental stands of Arabidopsis thaliana affected their aboveground biomass and fecundity in their colonized range. We constructed some stands of genotypes that we a priori predicted would differ in performance or show overyielding. We found no relationship between genetic diversity and stand total biomass. However, increasing stand genetic diversity increased fecundity in high-resource conditions. Polyculture (multiple genotype) stands consistently yielded less biomass than expected based on the yields of component genotypes in monoculture. This under-yielding was strongest in stands with late-flowering and high biomass genotypes, potentially due to interference competition by these genotypes. Using a new implementation of association mapping, we identified genetic loci whose diversity was associated with stand-level yield, revealing a major flowering time locus associated with under-yielding of polycultures. Our field experiment supports community ecology studies that find a range of diversity-function relationships. Nevertheless, our results suggest diversity in colonizing propagule pools can enhance population fitness. Furthermore, interference competition among genotypes differing in flowering time might limit the advantages of polyculture.

Competition × drought interactions change phenotypic plasticity and the direction of selection on Arabidopsis traits.

Populations often exhibit genetic diversity in traits involved in responses to abiotic stressors, but what maintains this diversity is unclear. Arabidopsis thaliana exhibits high within-population variation in drought response. One hypothesis is that competition, varying at small scales, promotes diversity in resource use strategies. However, little is known about natural variation in competition effects on Arabidopsis physiology. We imposed drought and competition treatments on diverse genotypes. We measured resource economics traits, physiology, and fitness to characterize plasticity and selection in response to treatments. Plastic responses to competition differed depending on moisture availability. We observed genotype-drought-competition interactions for relative fitness: competition had little effect on relative fitness under well-watered conditions, whereas competition caused rank changes in fitness under drought. Early flowering was always selected. Higher δ13 C was selected only in the harshest treatment (drought and competition). Competitive context significantly changed the direction of selection on aboveground biomass and inflorescence height in well-watered environments. Our results highlight how local biotic conditions modify abiotic selection, in some cases promoting diversity in abiotic stress response. The ability of populations to adapt to environmental change may thus depend on small-scale biotic heterogeneity.

Genomics of sorghum local adaptation to a parasitic plant.

Host-parasite coevolution can maintain high levels of genetic diversity in traits involved in species interactions. In many systems, host traits exploited by parasites are constrained by use in other functions, leading to complex selective pressures across space and time. Here, we study genome-wide variation in the staple crop Sorghum bicolor (L.) Moench and its association with the parasitic weed Striga hermonthica (Delile) Benth., a major constraint to food security in Africa. We hypothesize that geographic selection mosaics across gradients of parasite occurrence maintain genetic diversity in sorghum landrace resistance. Suggesting a role in local adaptation to parasite pressure, multiple independent loss-of-function alleles at sorghum LOW GERMINATION STIMULANT 1 (LGS1) are broadly distributed among African landraces and geographically associated with S. hermonthica occurrence. However, low frequency of these alleles within S. hermonthica-prone regions and their absence elsewhere implicate potential trade-offs restricting their fixation. LGS1 is thought to cause resistance by changing stereochemistry of strigolactones, hormones that control plant architecture and below-ground signaling to mycorrhizae and are required to stimulate parasite germination. Consistent with trade-offs, we find signatures of balancing selection surrounding LGS1 and other candidates from analysis of genome-wide associations with parasite distribution. Experiments with CRISPR-Cas9-edited sorghum further indicate that the benefit of LGS1-mediated resistance strongly depends on parasite genotype and abiotic environment and comes at the cost of reduced photosystem gene expression. Our study demonstrates long-term maintenance of diversity in host resistance genes across smallholder agroecosystems, providing a valuable comparison to both industrial farming systems and natural communities.