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. 2015 Jul;168(3):915-29.
doi: 10.1104/pp.15.00427. Epub 2015 Jun 1.

Salinity Is an Agent of Divergent Selection Driving Local Adaptation of Arabidopsis to Coastal Habitats

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Salinity Is an Agent of Divergent Selection Driving Local Adaptation of Arabidopsis to Coastal Habitats

Silvia Busoms et al. Plant Physiol. .
Free PMC article

Abstract

Understanding the molecular mechanism of adaptive evolution in plants provides insights into the selective forces driving adaptation and the genetic basis of adaptive traits with agricultural value. The genomic resources available for Arabidopsis (Arabidopsis thaliana) make it well suited to the rapid molecular dissection of adaptive processes. Although numerous potentially adaptive loci have been identified in Arabidopsis, the consequences of divergent selection and migration (both important aspects of the process of local adaptation) for Arabidopsis are not well understood. Here, we use a multiyear field-based reciprocal transplant experiment to detect local populations of Arabidopsis composed of multiple small stands of plants (demes) that are locally adapted to the coast and adjacent inland habitats in northeastern Spain. We identify fitness tradeoffs between plants from these different habitats when grown together in inland and coastal common gardens and also, under controlled conditions in soil excavated from coastal and inland sites. Plants from the coastal habitat also outperform those from inland when grown under high salinity, indicating local adaptation to soil salinity. Sodium can be toxic to plants, and we find its concentration to be elevated in soil and plants sampled at the coast. We conclude that the local adaptation that we observe between adjacent coastal and inland populations is caused by ongoing divergent selection driven by the differential salinity between coastal and inland soils.

Figures

Figure 1.
Figure 1.
Maps showing the Arabidopsis distribution model in northeastern Catalonia, Spain. Known locations of Arabidopsis (black circles) overlaid upon a binary map of alimetry (A; 0, white; and 1, blue [0–950 m]), geology (B; 0, white; and 1, orange [granite, granitoid, granodiorite, and hornfels]), and land uses (C; 0, white; and 1, green [sandy, soil with sparse vegetation, rain-fed fruit trees, thickets and meadows, sclerophyllous forest, and residential areas]). D, Areas predicted to contain Arabidopsis (purple polygons) obtained from the interception of the maps in A to C, and a 5- × 5-km grid is used to select random points (red points) outside the prediction locations of Arabidopsis. E, Map of potential geographic distribution of Arabidopsis (purple polygons) and confirmed populations (green points). F, Zoom of the main areas of interest from E, including the two sites chosen for reciprocal transplant experiments at Blanes and Santa Coloma de Farners (red points).
Figure 2.
Figure 2.
Estimation of the genetic structure within the Catalonian Arabidopsis population. Each vertical bar represents an individual plant genotyped at 425 genome-wide SNP markers, and each bar is divided into K colored sections that indicate the fractional membership of an individual in K clusters based on its genotype. The figure of each K is based on the analysis with highest probability for that value of K. Vertical white lines divide demes of coastal and inland origins. Supplemental Table S2 shows details of which demes were genotypes.
Figure 3.
Figure 3.
Mean fitness ± 95% confidence intervals predicted from a Poisson log-normal GLMM of Arabidopsis plants from coastal and inland habitats measured as silique number in both field and controlled common gardens. Plants from coastal (black diamonds) and inland (gray circles) demes cultivated in the coastal common garden in Blanes and the inland common garden in Santa Coloma de Farners in 2013 (A) and 2014 (B) and a controlled environment common garden (C) in soil excavated from the sites used for the coastal and inland common gardens; n = 10 plants per deme and 10 demes each from coastal and inland habitats (for details, see Supplemental Table S2).
Figure 4.
Figure 4.
Mean fitness of Arabidopsis plants from coastal and inland habitats measured as growth (rosette diameter) in both field and controlled common gardens. Plants from coastal (black diamonds) and inland (gray circles) demes cultivated in the coastal common garden in Blanes (A and C) and the inland common garden in Santa Coloma de Farners (B and D) in 2013 (A and B) and 2014 (C and D) and a controlled environment common garden in soil excavated from the sites used for the coastal and inland common gardens in Blanes (E) and the inland common garden in Santa Coloma de Farners (F). Data represent the mean ± se (n = 10 plants per deme and 10 demes each from coastal and inland habitats; for details, see Supplemental Table S2).
Figure 5.
Figure 5.
Clines in the physiochemical properties of soil with distance to the sea. Water-holding capacity (WHC; A; milliliters per gram), carbonate content (B; CaCO3; percentage), pH (C), organic matter (D; percentage), Na+ (E; milligrams per gram), Mg2+ (F; milligrams per gram), chloride (G; milligrams per gram), sulfate (H; milligrams per gram), Na+-K+ ratio (I), and Ca2+-Mg2+ ratio (J) of soil samples collected in May of 2013 and their relationship with distance to the sea (logarithm of meters to sea). Data include three samples of soil per site (for details, see Supplemental Table S2).
Figure 6.
Figure 6.
Differentiation in mineral nutrient content of coastal and inland Arabidopsis demes growing in their native habitats. Leaf concentrations of Na+ (A), K+ (B), Mg2+ (D), and Ca2+ (E; micrograms per gram dry weight) and Na+-K+ (C) and Ca2+-Mg2+ (F) ratios from tissue collected in the field in March of 2013 (black diamonds) and March of 2014 (gray circles). Data represent the mean ± se (n = 30 coastal and 26 inland plants in 2013 and 120 coastal and 107 inland plants in 2014; for details, see Supplemental Table S2).
Figure 7.
Figure 7.
Effects of NaCl treatments on growth and fitness of coastal and inland Arabidopsis demes. A, Plants were grown in potting mix and irrigated with 0, 50, or 100 mm NaCl in one-quarter-strength Hoagland solution, and total silique number was counted at maturity from coastal (black diamonds) and inland (gray circles) demes. B, Rosette diameter of plants. Growth of plants from coastal (black diamonds) and inland (gray circles) demes exposed to 0 (lines), 50 (dashed lines), or 100 mm (dotted lines) NaCl was also measured. In A, plotted values are the predicted means ± 95% confidence intervals obtained from a Poisson log-normal GLMM (n = 4 plants per deme from eight coastal and nine inland demes), and in B, plotted values represent the mean ± se (n = 4 plants per deme from eight coastal and nine inland demes). Plants from coastal (black diamonds) and inland (gray circles) demes were also grown hydroponically and exposed to different concentrations of NaCl in the hydroponic growth solution, and the concentrations of Na+ (C) and K+ (D) and the Na+-K+ ratio (E) in leaves were determined. Data represent the mean ± se (n = 6 plants per deme and 13 demes from coastal and inland habitats; for details, see Supplemental Table S2).

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