Eric J. B. von Wettberg

Genomic Analysis of Differentiation between Soil Types Reveals Candidate Genes for Local Adaptation in Arabidopsis lyrata

Serpentine soil, which is naturally high in heavy metal content and has low calcium to magnesium ratios, comprises a difficult environment for most plants. An impressive number of species are endemic to serpentine, and a wide range of non-endemic plant taxa have been shown to be locally adapted to these soils. Locating genomic polymorphisms which are differentiated between serpentine and non-serpentine populations would provide candidate loci for serpentine adaptation. We have used the Arabidopsis thaliana tiling array, which has 2.85 million probes throughout the genome, to measure genetic differentiation between populations of Arabidopsis lyrata growing on granitic soils and those growing on serpentinic soils. The significant overrepresentation of genes involved in ion transport and other functions provides a starting point for investigating the molecular basis of adaptation to soil ion content, water retention, and other ecologically and economically important variables. One gene in particular, calcium-exchanger 7, appears to be an excellent candidate gene for adaptation to low Ca∶Mg ratio in A. lyrata.

Genetic Patterns of Domestication in Pigeonpea (Cajanus cajan (L.) Millsp.) and Wild Cajanus Relatives

Pigeonpea (Cajanus cajan) is an annual or short-lived perennial food legume of acute regional importance, providing significant protein to the human diet in less developed regions of Asia and Africa. Due to its narrow genetic base, pigeonpea improvement is increasingly reliant on introgression of valuable traits from wild forms, a practice that would benefit from knowledge of its domestication history and relationships to wild species. Here we use 752 single nucleotide polymorphisms (SNPs) derived from 670 low copy orthologous genes to clarify the evolutionary history of pigeonpea (79 accessions) and its wild relatives (31 accessions). We identified three well-supported lineages that are geographically clustered and congruent with previous nuclear and plastid sequence-based phylogenies. Among all species analyzed Cajanus cajanifolius is the most probable progenitor of cultivated pigeonpea. Multiple lines of evidence suggest recent gene flow between cultivated and non-cultivated forms, as well as historical gene flow between diverged but sympatric species. Evidence supports that primary domestication occurred in India, with a second and more recent nested population bottleneck focused in tropical regions that is the likely consequence of pigeonpea breeding. We find abundant allelic variation and genetic diversity among the wild relatives, with the exception of wild species from Australia for which we report a third bottleneck unrelated to domestication within India. Domesticated C. cajan possess 75% less allelic diversity than the progenitor clade of wild Indian species, indicating a severe “domestication bottleneck” during pigeonpea domestication.

Rootstocks: Diversity, Domestication, and Impacts on Shoot Phenotypes

Grafting is an ancient agricultural practice that joins the root system (rootstock) of one plant to the shoot (scion) of another. It is most commonly employed in woody perennial crops to indirectly manipulate scion phenotype. While recent research has focused on scions, here we investigate rootstocks, the lesser-known half of the perennial crop equation. We review natural grafting, grafting in agriculture, rootstock diversity and domestication, and developing areas of rootstock research, including molecular interactions and rootstock microbiomes. With growing interest in perennial crops as valuable components of sustainable agriculture, rootstocks provide one mechanism by which to improve and expand woody perennial cultivation in a range of environmental conditions.

Exploring germplasm diversity to understand the domestication process in Cicer spp. using SNP and DArT markers

To estimate genetic diversity within and between 10 interfertile Cicer species (94 genotypes) from the primary, secondary and tertiary gene pool, we analysed 5,257 DArT markers and 651 KASPar SNP markers. Based on successful allele calling in the tertiary gene pool, 2,763 DArT and 624 SNP markers that are polymorphic between genotypes from the gene pools were analyzed further. STRUCTURE analyses were consistent with 3 cultivated populations, representing kabuli, desi and pea-shaped seed types, with substantial admixture among these groups, while two wild populations were observed using DArT markers. AMOVA was used to partition variance among hierarchical sets of landraces and wild species at both the geographical and species level, with 61% of the variation found between species, and 39% within species. Molecular variance among the wild species was high (39%) compared to the variation present in cultivated material (10%). Observed heterozygosity was higher in wild species than the cultivated species for each linkage group. Our results support the Fertile Crescent both as the center of domestication and diversification of chickpea. The collection used in the present study covers all the three regions of historical chickpea cultivation, with the highest diversity in the Fertile Crescent region. Shared alleles between different gene pools suggest the possibility of gene flow among these species or incomplete lineage sorting and could indicate complicated patterns of divergence and fusion of wild chickpea taxa in the past.

Genetic Diversity and Demographic History of Cajanus spp. Illustrated from Genome-Wide SNPs

Understanding genetic structure of Cajanus spp. is essential for achieving genetic improvement by quantitative trait loci (QTL) mapping or association studies and use of selected markers through genomic assisted breeding and genomic selection. After developing a comprehensive set of 1,616 single nucleotide polymorphism (SNPs) and their conversion into cost effective KASPar assays for pigeonpea (Cajanus cajan), we studied levels of genetic variability both within and between diverse set of Cajanus lines including 56 breeding lines, 21 landraces and 107 accessions from 18 wild species. These results revealed a high frequency of polymorphic SNPs and relatively high level of cross-species transferability. Indeed, 75.8% of successful SNP assays revealed polymorphism, and more than 95% of these assays could be successfully transferred to related wild species. To show regional patterns of variation, we used STRUCTURE and Analysis of Molecular Variance (AMOVA) to partition variance among hierarchical sets of landraces and wild species at either the continental scale or within India. STRUCTURE separated most of the domesticated germplasm from wild ecotypes, and separates Australian and Asian wild species as has been found previously. Among Indian regions and states within regions, we found 36% of the variation between regions, and 64% within landraces or wilds within states. The highest level of polymorphism in wild relatives and landraces was found in Madhya Pradesh and Andhra Pradesh provinces of India representing the centre of origin and domestication of pigeonpea respectively.

Whole-genome resequencing of 292 pigeonpea accessions identifies genomic regions associated with domestication and agronomic traits

Pigeonpea (Cajanus cajan), a tropical grain legume with low input requirements, is expected to continue to have an important role in supplying food and nutritional security in developing countries in Asia, Africa and the tropical Americas. From whole-genome resequencing of 292 Cajanus accessions encompassing breeding lines, landraces and wild species, we characterize genome-wide variation. On the basis of a scan for selective sweeps, we find several genomic regions that were likely targets of domestication and breeding. Using genome-wide association analysis, we identify associations between several candidate genes and agronomically important traits. Candidate genes for these traits in pigeonpea have sequence similarity to genes functionally characterized in other plants for flowering time control, seed development and pod dehiscence. Our findings will allow acceleration of genetic gains for key traits to improve yield and sustainability in pigeonpea.

Adapting genomics to study the evolution and ecology of agricultural systems

In the face of global change, agriculture increasingly requires germplasm with high yields on marginal lands. Identifying pathways that are adaptive under marginal conditions is increasingly possible with advances at the intersection of evolutionary ecology, population genetics, and functional genomics. Trait-based (reverse ecology) approaches have connected flowering time in Arabidopsis thaliana to single alleles with environment-specific effects. Similarly, genetic dissection of rice flooding tolerance enabled the production of near-isogenic lines exhibiting tolerance and high yields. An alternative gene-forward (forward ecology) approach identified candidate genes for local adaptation of Arabidopsis lyrata to heavy-metal rich soils. A global perspective on plant adaptation and trait correlations provides a foundation for breeding tolerant crops and suggests populations adapted to marginal habitats be conservation priorities.

Parental environments and interactions with conspecifics alter salinity tolerance of offspring in the annual Medicago truncatula

Summary 1. Based on expectations of the stress-gradient hypothesis for conspecific interactions, stress-sensitive genotypes may be able to persist in stressful environments when positive interactions between individuals occur under stressful environments. Additionally, we test how parental environmental effects alter responses to stress and outcomes of conspecific interactions in stress. While the stress-gradient hypothesis focuses on plant growth, earlier flowering may provide stress avoidance in short-lived organisms. 2. We studied responses to soil salinity and conspecific neighbour using genotypes of Medicago truncatula (Fabaceae) originating from saline or non-saline environments, utilizing seeds from parental plants grown in saline or non-saline environments. During the early stages of reproduction, we quantified leaf number, as a measure of vegetative growth, and number of flowers, as a measure of early reproduction potential. 3. Based on leaf counts, non-saline genotypes were better competitors than saline-origin genotypes and benefited from neighbouring plants in saline environments. This positive interaction was detected only when seeds were matured on parental plants grown in non-saline environments. Saline-origin genotypes displayed greater salinity tolerance in early flowering than non-saline genotypes. Plants with neighbours had greater early flowering, regardless of origin, consistent with facilitative interactions in stressful environments. 4. Transgenerational plastic responses influenced neighbouring plant interactions on plant growth, and results suggest that facilitative interactions may be transient only persisting for one generation. However, earlier flowering of non-saline genotypes when grown with a neighbouring plant is consistent with facilitative interactions resulting in reproductive benefits in saline environments, if earlier flowering is favoured in saline environments. 5. Synthesis. Adaptation to stressful environments allows tolerant genotypes to persist in these environments. Less appreciated is that stress-sensitive genotypes lacking such adaptations may persist in stressful environments via positive interactions with other individuals. Thus, positive interactions between individuals may explain the persistence of stress-sensitive genotypes within a population adapted to stressful environments.

More cells, bigger cells or simply reorganization? Alternative mechanisms leading to changed internode architecture under contrasting stress regimes

Shading and mechanical stress (MS) modulate plant architecture by inducing different developmental pathways. Shading results in increased stem elongation, often reducing whole-plant mechanical stability, while MS inhibits elongation, with a concomitant increase in stability. Here, we examined how these organ-level responses are related to patterns and processes at the cellular level by exposing Impatiens capensis to shading and MS. Shading led to the production of narrower cells along the vertical axis. By contrast, MS led to the production of fewer, smaller and broader cells. These responses to treatments were largely in line with genetic differences found among plants from open and closed canopy sites. Shading- and MS-induced plastic responses in cellular characteristics were negatively correlated: genotypes that were more responsive to shading were less responsive to MS and vice versa. This negative correlation, however, did not scale to mechanical and architectural traits. Our data show how environmental conditions elicit distinctly different associations between characteristics at the cellular level, plant morphology and biomechanics. The evolution of optimal response to different environmental cues may be limited by negative correlations of stress-induced responses at the cellular level.

Salinity adaptation and the contribution of parental environmental effects in medicago truncatula

High soil salinity negatively influences plant growth and yield. Some taxa have evolved mechanisms for avoiding or tolerating elevated soil salinity, which can be modulated by the environment experienced by parents or offspring. We tested the contribution of the parental and offspring environments on salinity adaptation and their potential underlying mechanisms. In a two-generation greenhouse experiment, we factorially manipulated salinity concentrations for genotypes of Medicago truncatula that were originally collected from natural populations that differed in soil salinity. To compare population level adaptation to soil salinity and to test the potential mechanisms involved we measured two aspects of plant performance, reproduction and vegetative biomass, and phenological and physiological traits associated with salinity avoidance and tolerance. Saline-origin populations had greater biomass and reproduction under saline conditions than non-saline populations, consistent with local adaptation to saline soils. Additionally, parental environmental exposure to salt increased this difference in performance. In terms of environmental effects on mechanisms of salinity adaptation, parental exposure to salt spurred phenological differences that facilitated salt avoidance, while offspring exposure to salt resulted in traits associated with greater salt tolerance. Non-saline origin populations expressed traits associated with greater growth in the absence of salt while, for saline adapted populations, the ability to maintain greater performance in saline environments was also associated with lower growth potential in the absence of salt. Plastic responses induced by parental and offspring environments in phenology, leaf traits, and gas exchange contribute to salinity adaptation in M. truncatula. The ability of plants to tolerate environmental stress, such as high soil salinity, is likely modulated by a combination of parental effects and within-generation phenotypic plasticity, which are likely to vary in populations from contrasting environments.