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.
High soil carbonate limits crop performance especially in semiarid or arid climates. To understand how plants adapt to such soils, we explored natural variation in tolerance to soil carbonate in small local populations (demes) of Arabidopsis thaliana growing on soils differing in carbonate content. Reciprocal field-based transplants on soils with elevated carbonate (+C) and without carbonate (−C) over several years revealed that demes native to (+C) soils showed higher fitness than those native to (−C) soils when both were grown together on carbonate-rich soil. This supports the role of soil carbonate as a driving factor for local adaptation. Analyses of contrasting demes revealed key mechanisms associated with these fitness differences. Under controlled conditions, plants from the tolerant deme A1 (+C) native to (+C) soil were more resistant to both elevated carbonate and iron deficiency than plants from the sensitive T6 (−C) deme native to (−C) soil. Resistance of A1 (+C) to elevated carbonate was associated with higher root extrusion of both protons and coumarin-type phenolics. Tolerant A1 (+C) also had better Ca-exclusion than sensitive T6 (−C) . We conclude that Arabidopsis demes are locally adapted in their native habitat to soils with moderately elevated carbonate. This adaptation is associated with both enhanced iron acquisition and calcium exclusion.
Bicarbonate plays a fundamental role in the cell pH status in all organisms. In autotrophs, HCO3− may further contribute to carbon concentration mechanisms (CCM). This is especially relevant in the CO2-poor habitats of cyanobacteria, aquatic microalgae, and macrophytes. Photosynthesis of terrestrial plants can also benefit from CCM as evidenced by the evolution of C4 and Crassulacean Acid Metabolism (CAM). The presence of HCO3− in all organisms leads to more questions regarding the mechanisms of uptake and membrane transport in these different biological systems. This review aims to provide an overview of the transport and metabolic processes related to HCO3− in microalgae, macroalgae, seagrasses, and terrestrial plants. HCO3− transport in cyanobacteria and human cells is much better documented and is included for comparison. We further comment on the metabolic roles of HCO3− in plants by focusing on the diversity and functions of carbonic anhydrases and PEP carboxylases as well as on the signaling role of CO2/HCO3− in stomatal guard cells. Plant responses to excess soil HCO3− is briefly addressed. In conclusion, there are still considerable gaps in our knowledge of HCO3− uptake and transport in plants that hamper the development of breeding strategies for both more efficient CCM and better HCO3− tolerance in crop plants.
Purpose Alkaline salinity constrains crop yield. Previously, we observed local adaptation of Arabidopsis thaliana to saline-siliceous soils (pH ≤ 7) and to non-saline carbonate soils. However, no 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 alkaline salinity of A. thaliana that differ in tolerance to either non-alkaline salinity or carbonate. Methods A. thaliana native to saline-siliceous soils (high salinity, HS), non-saline carbonate soils (high alkalinity, HA), or soils with intermediate levels of these factors (medium saline-alkalinity, MSA) were cultivated in common gardens on saline-siliceous or saline-calcareous substrates. Hydroponics and irrigation experiments confirmed the phenotypes. The growth, mineral concentrations, proline content, osmotic potential, genetic variation distribution, and expression levels of selected genes involved in salinity and alkalinity tolerance were assessed. Results HS performed best on saline-siliceous soil and in hydroponics with salinity (pH 5.9). However, HS was more sensitive to saline-alkaline conditions than HA and MSA. The fitness under saline-alkaline conditions was ranked according to MSA > HA > HS. Under alkaline salinity, MSA best maintained ion homeostasis, osmotic balance, and higher expression levels of key genes involved in saline or alkaline tolerance (AHA1, root HKT1 and FRO2, and shoot NHX1 and IRT1). Conclusion In A. thaliana, salinity tolerance evolved on saline-siliceous soils does not provide tolerance to alkaline salinity. Plants native to intermediate conditions (MSA) have more plasticity to adapt to alkaline salinity than those locally adapted to these individual stress factors.
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 (MOT1 DEL ) present in coastal habitats that is associated with lower transcript expression and Mo accumulation. Analysis of the leaf ionome revealed that MOT1 DEL plants accumulate more Cu and less Na + than plants with the non-coastal MOT1 allele, revealing a complex interdependence in homeostasis of these three elements. Our results indicate that under salinity, reduced MOT1 function limits leaf Na + accumulation through ABA signalling. Enhanced ABA biosynthesis requires Cu. This demand is met in Cu deficient coastal soils through MOT1 DEL increasing the expression of SPL7 and the copper transport protein COPT6. MOT1 DEL 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.
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