Anastatica hierochuntica, an Arabidopsis Desert Relative, Is Tolerant to Multiple Abiotic Stresses and Exhibits Species-Specific and Common Stress Tolerance Strategies with Its Halophytic Relative, Eutrema (Thellungiella) salsugineum

Abstract

The search for novel stress tolerance determinants has led to increasing interest in plants native to extreme environments – so called “extremophytes.” One successful strategy has been comparative studies between Arabidopsis thaliana and extremophyte Brassicaceae relatives such as the halophyte Eutrema salsugineum located in areas including cold, salty coastal regions of China. Here, we investigate stress tolerance in the desert species, Anastatica hierochuntica (True Rose of Jericho), a member of the poorly investigated lineage III Brassicaceae. We show that A. hierochuntica has a genome approximately 4.5-fold larger than Arabidopsis, divided into 22 diploid chromosomes, and demonstrate that A. hierochuntica exhibits tolerance to heat, low N and salt stresses that are characteristic of its habitat. Taking salt tolerance as a case study, we show that A. hierochuntica shares common salt tolerance mechanisms with E. salsugineum such as tight control of shoot Na+ accumulation and resilient photochemistry features. Furthermore, metabolic profiling of E. salsugineum and A. hierochuntica shoots demonstrates that the extremophytes exhibit both species-specific and common metabolic strategies to cope with salt stress including constitutive up-regulation (under control and salt stress conditions) of ascorbate and dehydroascorbate, two metabolites involved in ROS scavenging. Accordingly, A. hierochuntica displays tolerance to methyl viologen-induced oxidative stress suggesting that a highly active antioxidant system is essential to cope with multiple abiotic stresses. We suggest that A. hierochuntica presents an excellent extremophyte Arabidopsis relative model system for understanding plant survival in harsh desert conditions.

Dark period transcriptomic and metabolic profiling of two diverse Eutrema salsugineum accessions

“…Overall, SH tissues had higher concentrations of sugars than YK. These measurements of nighttime sugar concentrations were similar to previous results obtained for fructose, glucose, and raffinose in leaves of E. salsugineum harvested during the day (Lee et al, 2012; Eshel et al, 2017). The products of starch breakdown, including maltose and glucose, were more abundant in SH (Table 5 and Supplementary Table 3), suggesting a higher rate of starch metabolism in the lower-biomass SH accession This was consistent with the strong negative correlation between starch content and biomass observed in A. thaliana accessions (Sulpice et al, 2009).…”

“…The derivatization method we utilized has been widely used to detect sugars (Gullberg et al, 2004), but is less accurate for identifying and quantifying amino acids (Kaspar et al, 2009). As a result, despite the fact that Eutrema accumulates higher concentrations of some amino acids than Arabidopsis (Eshel et al, 2017), many amino acids were not detected in our analyses.…”

Halophytism: What Have We Learnt From Arabidopsis thaliana Relative Model Systems?

“…Nevertheless, since there was no comparison with enzyme activities in Arabidopsis, it is difficult to conclude anything about ROS-scavenging mechanisms that are unique to the halophyte. Where such comparative analyses have been performed, antioxidant metabolites such as ascorbate, dehydroascorbate, and caffeic acid are either constitutively higher or accumulate to a greater extent in soil-grown E. salsugineum compared with Arabidopsis (Kazachkova et al, 2013;Eshel et al, 2017). Indeed, the avoidance of singlet oxygen production at PSII has been attributed to induction of the ascorbate-glutathione cycle in E. salsugineum (Wiciarz et al, 2018).…”

The genomic basis of adaptation to calcareous and siliceous soils in Arabidopsis lyrata

“…Since the beginning of the ‐omics era, most integrative efforts have been deployed towards a better understanding of plant adaptation to heavy metal‐rich soils (Arnold et al, ; Hanikenne et al, ; Turner et al, ; Turner, Von Wettberg, & Nuzhdin, ; Wright et al, ) or to extreme salt levels (Dassanayake et al, ; Eshel et al, ; Wu et al, ). Yet, these soils cover a limited range of existing edaphic conditions and impose steep selective clines at study sites (e.g., at the edge of mine tailings).…”