Evolution of salt tolerance in Arabidopsis thaliana on siliceous soils does not confer tolerance to saline calcareous soils

Abstract

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.

At the core of salinity: convergent and divergent transcriptome response pathways to neutral and alkaline salinity in natural populations ofArabidopsis thaliana

“…Reduction of total photosynthetic activity is a common feature of plant stress, and the results confirm that the ability to maintain the photosynthetic capacity is a good indicator of tolerance to either neuSAL or alkSAL in A. thaliana. These observations point to a better performance of demes from pre litoral calcareous soils (V1 PC , LM2 PC ) under alkSAL in terms of growth maintenance and photosynthesis, and agree with the severe reduction in rosette diameter previously reported on coastal demes under alkSAL (Pérez-Martín et al, 2022).…”

“…This suggests that T6 CSadapted to moderate levels of neutral salinity -could be hampered by the alkalinity component of alkSAL. Overall, the observed response of each deme to alkSAL seems driven by other factors than the Na + content in their native soils, as it is the case for neuSAL (Busoms et al, 2018), and reinforces the statement that tolerance to salinity in siliceous soils does not confer tolerance to alkaline salinity (Pérez-Martín et al, 2022).…”

“…V1 PC and LM2 PC have been previously classified as good performers under alkSAL based on growth, reproductive and physiological traits when compared to coastal T6 CS and Ro2 CS , and the most tolerance phenotypes under neutral and alkaline salinity were observed for T6 and V1, respectively (Pérez-Martín et al, 2022). Therefore, nutrient ratios with reported biological importance under salinity conditions were compared in T6 CS – as tolerant to neuSAL but sensitive to alkSAL – and V1 PC – as sensitive to neuSAL but good performer under alkSAL , to further explain the implications of the differential nutrient accumulation under each type of salinity (Figure 1D; Dataset S4).…”

A genome‐wide association study identifies novel players in Na and Fe homeostasis in Arabidopsis thaliana under alkaline‐salinity stress

“…The importance of these genes for tolerance to saline alkaline conditions is further highlighted by the fact that, excepting HKT‐1 , for which absence of allelic variation in the study accessions has been confirmed, the study populations bearing alternative and common allelic variants for each identified locus do not differ in the expression of well‐stablished genes involved in Na and Fe homeostasis such as SOS1 , FRO1 and IRT1 . Recent studies have shown that accessions with tolerance to moderate salinity regulate Na:K ratios under salinity by enhancing HKT1 expression in roots but are unable to increase HKT1 root expression under alkaline salinity (Pérez‐Martín et al., 2022 ). This suggests that mechanisms for a better maintenance of Na:K balance under salinity conditions are likely to differ from those under alkaline salinity and that the latter need to be better understood.…”

Endophytic Fungi Regulate HbNHX1 Expression and Ion Balance in Hordeum bogdanii under Alkaline Stress

“…In Arabidopsis and rice, plants overexpressing NHXs can retain K + in the cytoplasm under saline conditions, thereby improving salt tolerance [ 10 , 11 ]. Pérez-Martín et al [ 12 ] found that high expression of NHX1 in Arabidopsis leaves under saline and alkaline environment can enhance salt tolerance by promoting Na + partition and osmotic regulation. Plants can improve their tolerance to Na + by collaborating with microorganisms [ 13 ].…”