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.

Correlational selection and genetic architecture promote the leaf economics spectrum in a perennial grass

The leaf economics spectrum (LES) is hypothesized to result from a trade-off between resource acquisition and conservation. Yet few studies have examined the evolutionary mechanisms behind the LES, perhaps because most species exhibit relatively specialized leaf economics strategies. In a genetic mapping population of the phenotypically diverse grass Panicum virgatum, we evaluate two interacting mechanisms that may drive LES evolution: 1) genetic architecture, where multiple traits are coded by the same gene (pleiotropy) or by genes in close physical proximity (linkage), and 2) correlational selection, where selection acts non-additively on combinations of multiple traits. We found evidence suggesting that shared genetic architecture (pleiotropy) controls covariation between two pairs of leaf economics traits. Additionally, at five common gardens spanning 17 degrees of latitude, correlational selection favored particular combinations of leaf economics traits. Together, these results demonstrate how the LES can evolve within species.

Provenance Variation in Early Survival, Growth, and Carbon Isotope Discrimination of Southwestern Ponderosa Pine Growing in Three Common Gardens across an Elevational Gradient

We investigated early survival, growth, and carbon isotope discrimination of ponderosa pine (Pinus ponderosa Lawson & C. Lawson var. scopulorum Engelm.) seedlings from different provenances using common gardens across an elevational gradient in order to examine the potential for adaptation to extreme environments and constraints to artificial regeneration. Twenty-one provenances from a range of elevations across Arizona and New Mexico were planted in three common gardens: a high-elevation meadow in aspen-mixed conifer forest, a mid-elevation ponderosa pine forest, and a low-elevation pinyon juniper woodland. Two years after planting in 2018, survival was highest at the mid-elevation site (54%), low at the high-elevation site (1.5%), and 0% at the low-elevation site. At the hot and dry low-elevation site, provenances from low-elevations survived longer than provenances from mid- and high-elevations, which suggests greater drought tolerance of low-elevation provenances. Mortality agents changed from abiotic (drought) to biotic (herbivory) with an increase in elevation across sites. High mortality of seedlings planted at high-elevation sites from biotic agents, such as rodents, may challenge efforts to establish ponderosa pine in assisted migration projects. Seedlings had significantly higher growth rate and carbon isotope discrimination (∆13C) at the mid-elevation site than the high-elevation site. Provenances differed significantly in diameter, and ∆13C, but not in height growth rate for the first year after planting. Provenance variation in ∆13C suggests genetic variation in water use efficiency that may be useful for future evaluation of southwestern ponderosa pine seed sources for reforestation.

eQTLs are key players in the integration of genomic and transcriptomic data for phenotype prediction

Multi-omics represent a promising link between phenotypes and genome variation. Few studies yet address their integration to understand genetic architecture and improve predictability. Our study used 241 poplar genotypes, phenotyped in two common gardens, with their xylem and cambium RNA sequenced at one site, yielding large phenotypic, genomic and transcriptomic datasets. For each trait, prediction models were built with genotypic or transcriptomic data and compared to concatenation integrating both omics. The advantage of integration varied across traits and, to understand such differences, we made an eQTL analysis to characterize the interplay between the genome and the transcriptome and classify the predicting features into CIS or TRANS relationships. A strong and significant negative correlation was found between the change in predictability and the change in predictor importance for eQTLs (both TRANS and CIS effects) and CIS regulated transcripts, and mostly for traits showing beneficial integration and evaluated in the site of transcriptomic sampling. Consequently, beneficial integration happens when redundancy of predictors is decreased, leaving the stage to other less prominent but complementary predictors. An additional GO enrichment analysis appeared to corroborate such statistical output. To our knowledge, this is a novel finding delineating a promising way to explore data integration.One-sentence summarySuccessful multi-omics integration when predicting phenotypes makes redundant the predictors that are linked to ubiquitous connections between the omics, according to biological and statistical approaches

Extreme climatic events but not environmental heterogeneity shape within-population genetic variation in maritime pine

How evolutionary forces interact to maintain quantitative genetic variation within populations has been a matter of extensive theoretical debates. While mutation and migration increase genetic variation, natural selection and genetic drift are expected to deplete it. To date, levels of genetic variation observed in natural populations are hard to predict without accounting for other processes, such as balancing selection in heterogeneous environments. We aimed to empirically test three hypotheses: (i) admixed populations have higher quantitative genetic variation due to introgression from other gene pools, (ii) quantitative genetic variation is lower in populations from harsher environments (i.e. experiencing stronger selection), and (iii) quantitative genetic variation is higher in populations from spatially heterogeneous environments. We used phenotypic measurements of five growth, phenological and functional traits from three clonal common gardens, consisting of 523 clones from 33 populations of maritime pine (Pinus pinaster Aiton). Populations from harsher climates (mainly colder areas) showed lower genetic variation for height in the three common gardens. Surprisingly, we did not find any association between within-population genetic variation and environmental heterogeneity or population admixture for any trait. Our results suggest a predominant role of natural selection in driving within-population genetic variation, and therefore indirectly their adaptive potential.

Phenological Plasticity and Adaptive Potential of Sugar Maple Populations

Global changes affect the growing conditions of terrestrial ecosystems, mismatching the phenological adaptation of plants to local climates at mid and high latitudes. Their long lifespan and slow reproductive cycles prevent trees from tracking the quick shift in their usual climatic conditions, thus endangering the survival of local populations. In this study, we explored the phenological plasticity and adaptive potential of bud burst in sugar maple (Acer saccharum Marsh.) seedlings from 30 Canadian origins with contrasting climates planted in two common gardens near and at the northern boundary of the species range. Bud development and leafing occurred in April-May, with complete bud burst lasting between 21 and 29 days. On average, bud swelling differed by 12 days between common gardens. However, this difference decreased to 4 days for complete leafing. Both factors site and seed origin affected bud burst, which represented the phenological plasticity and adaptation of sugar maple, respectively. Overall, the former (7.4–88.3%) contributed more than the latter (9.2–25.5%) to the variance in bud burst, despite the wide climatic range among the provenance origins compared with that at the two common gardens. Adaptation to local conditions provide the genetic tools for the survival of species across wide climatic ranges. Plasticity enables physiological responses of individuals to quick environmental changes. Our study demonstrated the major role of plasticity in bud phenology, and revealed the importance of investing resources in mechanisms dealing with the climatic challenges due to inter-annual variations in weather events.

Field Performances of Mediterranean Oaks in Replicate Common Gardens for Future Reforestation under Climate Change in Central and Southern Europe: First Results from a Four-Year Study

Climate change imposes severe stress on European forests, with forest degradation already visible in several parts of Europe. Thus adaptation of forestry applications in Mediterranean areas and central Europe is necessary. Proactive forestry management may include the planting of Mediterranean oak species in oak-bearing Central European regions. Five replicate common gardens of Greek and Italian provenances of Quercus ilex, Q. pubescens and Q. frainetto seedlings (210 each per plantation) were established in Central Italy, NE Greece (two) and Southern Germany (two, including Q. robur) to assess their performance under different climate conditions. Climate and soil data of the plantation sites are given and seedling establishment was monitored for survival and morphological parameters. After 3 years (2019) survival rates were satisfactory in the German and Italian sites, whereas the Greek sites exerted extremely harsh conditions for the seedlings, including extreme frost and drought events. In Germany, seedlings suffered extreme heat and drought periods in 2018 and 2019 but responded well. Provenances were ranked for each country for their performance after plantation. In Greece and Italy, Q. pubescens was the best performing species. In Germany, Q. pubescens and Q. robur performed best. We suggest that Greek or Italian provenances of Q. pubescens may be effectively used for future forestation purposes in Central Europe. For the establishment of Quercus plantations in Northern Greece, irrigation appears to be a crucial factor in seedling establishment.

QTL x environment interactions underlie ionome divergence in switchgrass

Ionomics measures elemental concentrations in biological organisms and provides a snapshot of physiology under different conditions. In this study, we evaluate genetic variation of the ionome in outbred, perennial switchgrass in three environments across the species’ native range, and explore patterns of genotype-by-environment interactions. We grew 725 clonally replicated genotypes of a large full sib family from a four-way linkage mapping population, created from deeply diverged upland and lowland switchgrass ecotypes, at three common gardens. Concentrations of 18 mineral elements were determined in whole post-anthesis tillers using ion coupled plasma mass spectrometry (ICP-MS). These measurements were used to identify quantitative trait loci (QTL) with and without QTL-by-environment interactions (QTLxE) using a multi-environment QTL mapping approach. We found that element concentrations varied significantly both within and between switchgrass ecotypes, and GxE was present at both the trait and QTL level. Concentrations of 14 of the 18 elements were under some genetic control, and 77 QTL were detected for these elements. 74% of QTL colocalized multiple elements, half of QTL exhibited significant QTLxE, and roughly equal numbers of QTL had significant differences in magnitude and sign of their effects across environments. The switchgrass ionome is under moderate genetic control and by loci with highly variable effects across environments.