Abstract
Local adaptation in coastal areas is driven chiefly by tolerance to salinity stress. To survive high salinity, plants have evolved mechanisms to specifically tolerate sodium. However, the pathways that mediate adaptive changes in these conditions reach well beyond Na+ . Here we perform a high-resolution genetic, ionomic, and functional study of the natural variation in Molybdenum transporter 1 (MOT1) associated with coastal Arabidopsis thaliana accessions. We quantify the fitness benefits of a specific deletion-harbouring allele (MOT1DEL ) present in coastal habitats that is associated with lower transcript expression and molybdenum accumulation. Analysis of the leaf ionome revealed that MOT1DEL plants accumulate more copper (Cu) and less sodium (Na+ ) than plants with the noncoastal MOT1 allele, revealing a complex interdependence in homeostasis of these three elements. Our results indicate that under salinity stress, reduced MOT1 function limits leaf Na+ accumulation through abscisic acid (ABA) signalling. Enhanced ABA biosynthesis requires Cu. This demand is met in Cu deficient coastal soils through MOT1DEL increasing the expression of SPL7 and the copper transport protein COPT6. MOT1DEL is able to deliver a pleiotropic suite of phenotypes that enhance salinity tolerance in coastal soils deficient in Cu. This is achieved by inducing ABA biosynthesis and promoting reduced uptake or better compartmentalization of Na+ , leading to coastal adaptation.
Highlights
Our understanding of the genomic basis of adaptive variation is increasing, but there is still very little known about the pleiotropic consequences of adaptive variation
Powerful models of plant adaptation to environmental variation in mineral nutrient and trace elements offer promising starting points from which to improve our understanding of these pleiotropic consequences, which arise from the interconnectedness of ion homeostasis networks (Busoms et al, 2015, 2018; Teres et al, 2019)
We studied the fitness of 10 plants for each deme/Molybdenum Transporter 1 (MOT1) variant at each site, and the other 10 plants were harvested in April 2014 and April 2015 to analyse the leaf ionome
Summary
Our understanding of the genomic basis of adaptive variation is increasing, but there is still very little known about the pleiotropic consequences of adaptive variation. Powerful models of plant adaptation to environmental variation in mineral nutrient and trace elements offer promising starting points from which to improve our understanding of these pleiotropic consequences, which arise from the interconnectedness of ion homeostasis networks (Busoms et al, 2015, 2018; Teres et al, 2019). Combined with genomewide association (GWA) studies, ionomics has allowed a farreaching assessment of adaptive, naturally evolved changes in mineral nutrient uptake and storage (Huang & Salt, 2016). Using such approaches, Baxter et al (2008) identified Molybdenum Transporter 1 (MOT1) as the causal gene driving reduced shoot molybdenum (Mo) in two accessions of Arabidopsis thaliana (Van-0 and Ler-0). The duplication increases the expression of MOT1 and results in higher accumulation of Mo in shoots; the deletion reduces expression of the MOT1 gene and causes a reduction in wholeplant Mo content
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