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.
Noccaea brachypetala is a close relative of Noccaea caerulescens, a model plant species used in metal hyperaccumulation studies. In a previous survey in the Catalan Pyrenees, we found two occidental and two oriental N. brachypetala populations growing on non-metalliferous soils, with accumulated high concentrations of Cd and Zn. Our hypothesis was that the microbiome companion of the plant roots may influence the ability of these plants to absorb metals. We performed high-throughput sequencing of the bacterial and fungal communities in the rhizosphere soil and rhizoplane fractions. The rhizobiomes and shoot ionomes of N. brachypetala plants were analyzed along with those from other non-hyperaccumulator Brassicaceae species found at the same sampling locations. The analyses revealed that microbiome richness and relative abundance tended to increase in N. brachypetala plants compared to non-hyperaccumulator species, regardless of plant location. We confirmed that the root compartment is a key factor in describing the community composition linked to the cohabiting Brassicaceae species, and the rhizoplane fraction contained the specific and rare taxa associated with each species. N. brachypetala plants harbored a similar relative abundance of fungi compared to the other plant hosts, but there was a notable reduction in some specific taxa. Additionally, we observed an enrichment in the hyperaccumulator rhizoplane of previously described metal-tolerant bacteria and bacteria involved in nitrogen cycling. The bacteria involved in the nitrogen cycle could contribute indirectly to the hyperaccumulator phenotype by improving soil quality and fertility. Our results indicate that N. brachypetala captures a particular prokaryotic community from the soil. This particular prokaryotic community may benefit the extraction of metal ions and/or improve plant nutrition. Our research identified satellite groups associated with the root niche of a hyperaccumulator plant that may assist in improving biological strategies in heavy metal remediation.
SUMMARY In nature, multiple stress factors occur simultaneously. The screening of natural diversity panels and subsequent Genome‐Wide Association Studies (GWAS) is a powerful approach to identify genetic components of various stress responses. Here, the nutritional status variation of a set of 270 natural accessions of Arabidopsis thaliana grown on a natural saline‐carbonated soil is evaluated. We report significant natural variation on leaf Na (LNa) and Fe (LFe) concentrations in the studied accessions. Allelic variation in the NINJA and YUC8 genes is associated with LNa diversity, and variation in the ALA3 is associated with LFe diversity. The allelic variation detected in these three genes leads to changes in their mRNA expression and correlates with plant differential growth performance when plants are exposed to alkaline salinity treatment under hydroponic conditions. We propose that YUC8 and NINJA expression patters regulate auxin and jasmonic signaling pathways affecting plant tolerance to alkaline salinity. Finally, we describe an impairment in growth and leaf Fe acquisition associated with differences in root expression of ALA3, encoding a phospholipid translocase active in plasma membrane and the trans Golgi network which directly interacts with proteins essential for the trafficking of PIN auxin transporters, reinforcing the role of phytohormonal processes in regulating ion homeostasis under alkaline salinity.
Purpose Alkaline salinity constrains crop yield. Previously, we found local adaptation of Arabidopsis thaliana demes to saline-siliceous soils (pH≤7) and to non-saline carbonate soils. However, any 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 saline-alkaline conditions of A. thaliana demes differing in salinity and carbonate tolerance.Methods A. thaliana native to saline-siliceous soils (G3), to non-saline carbonate soils (G1), or to soils with intermediate levels of these factors (G2) were cultivated in common gardens on saline-siliceous or saline-calcareous substrate. Hydroponics and irrigation experiments confirmed the phenotypes. Growth, mineral concentrations, genome differences, and expression of candidate genes were assessed in the different groups.Results G3 performed best on saline-siliceous soil and in hydroponics with salinity (pH 5.9). However, G3 was more sensitive to saline-alkaline conditions than G1 and G2. Fitness under saline-alkaline conditions was G2 > G1>G3 and G2 best maintained ion homeostasis under alkaline salinity. Whole genome scan did not differentiate among the groups, while distinctive patterns for FRO2, NINJA, and CCB4 were found and confirmed by qPCR.Conclusion In A. thaliana, salinity tolerance evolved on saline-siliceous soils does not provide tolerance to alkaline salinity. Plants from soils with intermediate conditions (G2) have more plasticity to adapt to alkaline salinity than those locally adapted to these individual stress factors. Higher expression of NINJA and CCB4 may contribute to this better adaptation.
Soil contamination by lead (Pb) has become one of the major ecological threats to the environment. Understanding the mechanisms of Pb transport and deposition in plants is of great importance to achieve a global Pb reduction. We exposed a collection of 360 Arabidopsis thaliana natural accessions to a Pb-polluted soil. Germination rates, growth, and leaf Pb concentrations showed extensive variation among accessions. These phenotypic data were subjected to genome wide association studies (GWAs) and we found a significant association on chromosome 1 for low leaf Pb accumulation. Genes associated with significant SNP markers were evaluated and we selected EXTENSIN18 (EXT18) and TLC (TRAM-LAG1-CLN8) as candidates for having a role in Pb homeostasis. Six Pb-tolerant accessions, three of them exhibiting low leaf Pb content, and three of them with high leaf Pb content; two Pb-sensitive accessions; two knockout T-DNA lines of GWAs candidate genes (ext18, tlc); and Col-0 were screened under control and high-Pb conditions. The relative expression of EXT18, TLC, and other genes described for being involved in Pb tolerance was also evaluated. Analysis of Darwinian fitness, root and leaf ionome, and TEM images revealed that Pb-tolerant accessions employ two opposing strategies: (1) low translocation of Pb and its accumulation into root cell walls and vacuoles, or (2) high translocation of Pb and its efflux to inactive organelles or intracellular spaces. Plants using the first strategy exhibited higher expression of EXT18 and HMA3, thicker root cell walls and Pb vacuolar sequestration, suggesting that these genes may contribute to the deposition of Pb in the roots. On the other hand, plants translocating high amounts of Pb showed upregulation of TLC and ABC transporters, indicating that these plants were able to properly efflux Pb in the aerial tissues. We conclude that EXT18 and TLC upregulation enhances Pb tolerance promoting its sequestration: EXT18 favors the thickening of the cell walls improving Pb accumulation in roots and decreasing its toxicity, while TLC facilitates the formation of dictyosome vesicles and the Pb encapsulation in leaves. These findings are relevant for the design of phytoremediation strategies and environment restoration.
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