Edaphic adaptation

Some of the most informative adaptive solutions plants present include many remarkable instances of adaptation to extreme edaphic stress. Therefore I am leveraging genome scanning approaches to understand the solutions evolution offers in some of the many independently-evolved lineages of metal, drought, and serpentine-tolerant plants. Initial results clearly indicate broadly orchestrated, polygenic responses to external selective pressures. These concerted changes indicate that even in the case of an external pressure, well-orchestrated internal adaptations must be marshaled in harmony with one another, calling for a better understanding of internal adaptation (systems-based analysis of compensatory changes in the genome). In addition, these initial results are pointing to striking instances of repeated evolution and specific mechanisms underlying preadaptation to colonization of challenging environments following genome duplication.

Why Serpentine? 

Serpentine soils present a multidimensional hazard to plant life. Not only do they offer marginal levels of essential nutrients such as calcium, phosphorous, potassium, and nitrogen, but they are also usually very porous, with a high propensity toward drought. Low calcium to magnesium ratios are a defining feature of serpentine environments and result in very low calcium uptake. These insults are typically compounded by the presence of phytotoxic levels of heavy metals such as nickel, cadmium, and zinc, which leads to stunting and chlorosis, along with antagonistic effects on iron uptake. As a result, serpentine environments are characterized by minimal ecosystem productivity and high rates of endemism. Evolution has nevertheless produced populations that tolerate these multiple stresses, which by adapting to this ‘serpentine syndrome,’ suggest possible solutions to multiple challenges in crop improvement. 

In contrast to our recent work on adaptation to genome duplication in the same A. arenosa system, we observe a relatively diverse array of genes implicated in serpentine adaptation, from strong sweeps in dehydration tolerance coding loci (ERD4 below), to loci involved in sulfur transport (SULTR1;1 below), heavy metal transport, and root growth. We see clear selective sweeps in many categories consistent with adaptation to ‘serpentine syndrome’: dehydration tolerance, ion transport (Ca, Mg, and K transport-related genes), stress, and root branching and growth.

Example sweeps in nutrient uptake and drought stress candidates in serpentine-adapted A. arenosa

(A) Allele frequency differences (AFD) in two example differentiated regions. Dots represent polymorphic SNPs. X-axis gives chromosome location. Y-axis gives degree of differentiation calculated by plotting the absolute value of the difference in AFD between serpentine-adapted and non-serpentine comparison groups. Arrows indicate gene models. Red arrow indicates sweep candidate with localized differentiation. These candidates, EARLY RESPONSE TO DEHYDRATION-LIKE 4 (ERD4) and SULPHATE TRANSPORTER 1;1 (SULTR1;1), have predicted gene functions are concordant with the challenges surrounding serpentine adaptation. 

(B) Several population differentiation metics plotted in the ERD4 region. X-axis gives chromosome position. Red axis = Fst. Yellow axis = 2dSFS. Blue axis = Diversity/Differentiation residual metric. Colored dotted lines give 0.5% cutoff for each respective metric. Combined with the AFD plots in (A), these indicate that the ERD4 gene coding locus has undergone a selective sweep specifically in the serpentine-adapted population. We see 58 gene coding loci scattered throughout the genome that are all extreme outliers for all of the metrics shown here, indicating that many genes have coevolved together to allow these plants to endure the multiple hazards of colonizing serpentine environments.

In our recent genome scans we see clear signatures of selection, typically consisting of single gene peaks of high differentiation, falling off immediately following the coding locus, due to negligible linkage in A. arenosa. This makes identification of candidate genes unambiguous. In contrast to most (if not all) other genome scans, over 50% of 58 top selective sweep candidates have serpentine-relevant adaptive functions (from published studies, not simply GO assignments). We see obvious highly polygenic adaptation and sweeps in functional classes that are nice matches to what is known about the hazards of life on serpentine: e.g., dehydration tolerance loci, phytotoxic heavy metal transporters, and root macronutrient uptake transporters. Aside from its evolutionary interest, clear signatures of selection on naturally evolved alleles of these gene classes is highly relevant to rational crop improvement. 

We interpret these results as showing us not only adaptations to external challenges, but also compensatory adjustments to the changed physiological state of the cell (as in Yant et al 2013, where we observed coevolution of interacting meiosis proteins). That these serpentine-tolerant lineages are polyploid is an important hint toward possible mechanisms of preadaptation. In particular, we have very recently discovered evidence that polyploid A. arenosa may be a good colonizer of stressful habitats like serpentine in part because of prior adaptation to the physiological challenges of resetting ion homeostasis associated with WGD. We have obtained functional evidence supporting this: the majority of the loci uncovered in this scan have skewed elemental accumulation profiles when the orthologous Arabidopsis thaliana mutant is tested by Inductively-Coupled Plasma Mass Spectrometry (ICP-MS) for relevant element accumulation levels. We think that these results may have broad implications for understanding the evolutionary success of polyploids, and their ability to shift niches relative to diploid relatives, sometimes becoming notoriously invasive colonizers.

The work above is part of a set of ongoing collaborations with David Salt (Aberdeen, Scotland, U.K.).

Other edaphic adaptation projects in the lab are collaborations with Ute Krämer (Bochum, Germany)