Multiple paths lead to salt tolerance - pre-adaptation vs dynamic responses from two closely related extremophytes

Abstract

Salinity stress is an ongoing problem for global crop production. Schrenkiella parvula and Eutrema salsugineum are salt-tolerant extremophytes closely related to Arabidopsis thaliana. We investigated multi-omics salt stress responses of the two extremophytes in comparison to A. thaliana. Our results reveal that S. parvula limits Na accumulation while E. salsugineum shows high tissue tolerance to excess Na. Despite this difference, both extremophytes maintained their nutrient balance, while A. thaliana failed to sustain its nutrient content. The root metabolite profiles of the two extremophytes, distinct at control conditions, converged upon prolonged salt stress. This convergence was achieved by a dynamic response in S. parvula roots increasing its amino acids and sugars to the constitutively high basal levels observed in E. salsugineum. The metabolomic adjustments were strongly supported by the transcriptomic responses in the extremophytes. The predominant transcriptomic signals in all three species were associated with salt stress. However, root architecture modulation mediated by negative regulators of auxin and ABA signaling supported minimally affected root growth unique to each extremophyte during salt treatments. Overall, E. salsugineum exhibited more preadapted responses at the metabolome level while S. parvula showed predominant pre-adaptation at the transcriptome level to salt stress. Our work shows that while salt tolerance in these two species shares common features, they substantially differ in pathways leading to convergent adaptive traits.

Effective root responses to salinity stress include maintained cell expansion and carbon allocation

“…S7b, c). These data suggest that S. parvula seedlings maintain a favorable ion balance by limiting Na + influx and maintaining high K + levels upon salt treatment, as was found for adult S. parvula plants (Orsini et al, 2010;Tran et al, 2021b). Interestingly, we found the GO term 'suberin biosynthetic process' was enriched by the up-regulated DEGs at 3h (Fig.…”

“…For instance, the pseudocereal crop Chenopodium quinoa ( C. quinoa) loads Na + into its epidermal bladder cells through HIGH-AFFINITY POTASSIUM TRANSPORTER 1-type channels (Kiani-Pouya et al , 2017; Bohm et al , 2018). Salicornia dolichostachya and the Arabidopsis-relative halophyte Eutrema salsugineum ( E. salsugineum ) and Schrenkiella parvula ( S. parvula ) have constitutive high expression of gene SALT OVERLY SENSITIVE 1 that encodes an ion transporter exporting Na + from cells (Katschnig et al , 2015; Tran et al , 2021b). Genomic studies also found that both C. quinoa and S. parvula have a higher number of genes encoding sugar transporters compared to their glycophytic relatives (Dassanayake et al , 2011; Zou et al , 2017).…”

“…Genomic studies also found that both C. quinoa and S. parvula have a higher number of genes encoding sugar transporters compared to their glycophytic relatives (Dassanayake et al , 2011; Zou et al , 2017). E. salsugineum was reported to have constitutively higher levels of osmolytes such as soluble sugars, proline and gamma-aminobutyric acid compared to Arabidopsis, while S. parvula could rapidly increase and maintain abundant osmolytes and osmoprotectants under prolonged salt stress condition (Bartels & Dinakar, 2013; Tran et al , 2021b). Although roots are the primary target of salt stress, the root adaptive strategies of halophytes are largely unknown.…”

Alternative splicing preferentially increases transcript diversity associated with stress responses in the extremophyteSchrenkiella parvula

“…To quantify isoform abundance in response to high salinity compared to control conditions, RNA was extracted from hydroponically grown S. parvula and A. thaliana (Col-0) as described in Tran et al (2021).…”

Spatiotemporal gene expression atlas of the extremophyteSchrenkiella parvula

“…The copyright holder for this preprint this version posted October 26, 2022. ; https://doi.org/10.1101/2022.10.24.513627 doi: bioRxiv preprint (Wang et al, 2019), physiological assessments (Orsini et al, 2010;Tran et al, 2021), and multiomics datasets generated to investigate adaptations to environmental stress (Tran et al, 2022;Pantha et al, 2021;Wang et al, 2021;Wijesinghege et al, 2022;Oh et al, 2014). Prior studies have also focused on landmark genes in salt stress regulation but with novel adaptations that make their function different in S. parvula to those in salt-sensitive plants (Ali et al, 2016;Ali et al, 2018;Jarvis et al, 2014).…”