Stressors such as soil salinity and dehydration are major constraints on plant growth, causing worldwide crop losses. Compounding these insults, increasing climate volatility requires adaptation to fluctuating conditions. Salinity stress responses are relatively well understood in Arabidopsis thaliana , making this system suited for the rapid molecular dissection of evolutionary mechanisms. In a large-scale genomic analysis of Catalonian A. thaliana , we resequenced 77 individuals from multiple salinity gradients along the coast and integrated these data with 1,135 worldwide A. thaliana genomes for a detailed understanding of the demographic and evolutionary dynamics of naturally evolved salinity tolerance. This revealed that Catalonian varieties adapted to highly fluctuating soil salinity are not Iberian relicts but instead have immigrated to this region more recently. De novo genome assembly of three allelic variants of the high-affinity K ⁺ transporter ( HKT1;1 ) locus resolved structural variation between functionally distinct alleles undergoing fluctuating selection in response to seasonal changes in soil salinity. Plants harboring alleles responsible for low root expression of HKT1;1 and consequently high leaf sodium ( HKT1;1 ^HLS ) were migrants that have moved specifically into areas where soil sodium levels fluctuate widely due to geography and rainfall variation. We demonstrate that the proportion of plants harboring HKT1;1 ^HLS alleles correlates with soil sodium level over time, HKT1;1 ^HLS -harboring plants are better adapted to intermediate levels of salinity, and the HKT1;1 ^HLS allele clusters with high-sodium accumulator accessions worldwide. Together, our evidence suggests that HKT1;1 is under fluctuating selection in response to climate volatility and is a worldwide determinant in adaptation to saline conditions.

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.

Plant development and fitness largely depend on the adequate availability of mineral elements in the soil. Most essential nutrients are available and can be membrane transported either as mono or divalent cations or as mono- or divalent anions. Trivalent cations are highly toxic to membranes, and plants have evolved different mechanisms to handle +3 elements in a safe way. The essential functional role of a few metal ions, with the possibility to gain a trivalent state, mainly resides in the ion’s redox activity; examples are iron (Fe) and manganese. Among the required nutrients, the only element with +3 as a unique oxidation state is the non-metal, boron. However, plants also can take up non-essential trivalent elements that occur in biologically relevant concentrations in soils. Examples are, among others, aluminum (Al), chromium (Cr), arsenic (As), and antimony (Sb). Plants have evolved different mechanisms to take up and tolerate these potentially toxic elements. This review considers recent studies describing the transporters, and specific and unspecific channels in different cell compartments and tissues, thereby providing a global vision of trivalent element homeostasis in plants.

High bicarbonate concentrations of calcareous soils with high pH can affect crop performance due to different constraints. Among these, Fe deficiency has mostly been studied. The ability to mobilize sparingly soluble Fe is a key factor for tolerance. Here, a comparative transcriptomic analysis was performed with two naturally selected Arabidopsis thaliana demes, the carbonate-tolerant A1_(c+) and the sensitive T6_(c−). Analyses of plants exposed to either pH stress alone (pH 5.9 vs. pH 8.3) or to alkalinity caused by 10 mM NaHCO₃ (pH 8.3) confirmed better growth and nutrient homeostasis of A1_(c+) under alkaline conditions. RNA-sequencing (RNA-seq) revealed that bicarbonate quickly (3 h) induced Fe deficiency-related genes in T6_(c−) leaves. Contrastingly, in A1_(c+), initial changes concerned receptor-like proteins (RLP), jasmonate (JA) and salicylate (SA) pathways, methionine-derived glucosinolates (GS), sulfur starvation, starch degradation, and cell cycle. Our results suggest that leaves of carbonate-tolerant plants do not sense iron deficiency as fast as sensitive ones. This is in line with a more efficient Fe translocation to aerial parts. In A1_(c+) leaves, the activation of other genes related to stress perception, signal transduction, GS, sulfur acquisition, and cell cycle precedes the induction of iron homeostasis mechanisms yielding an efficient response to bicarbonate stress.

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.