The use of extremophyte models to select growth promoting traits during environmental stresses is a recognized yet an underutilized strategy to design stress-resilient plants. Schrenkiella parvula, a leading extremophyte model in Brassicaceae, can grow and complete its life cycle under multiple environmental stresses, including high salinity. While S. parvula is equipped with foundational genomic resources to identify genetic clues that potentially lead to stress adaptations at the phenome level, a comprehensive physiological and structural characterization of salt stress responses throughout its lifecycle is absent. We aimed to identify the influential traits that lead to resilient growth and strategic decisions to ensure survival of the species in an extreme environment, and examined salt-induced changes in the physiology and anatomy of S. parvula throughout its life cycle across multiple tissues. We found that S. parvula maintains or even enhances growth during various developmental stages at salt stress levels known to inhibit growth in Arabidopsis thaliana and most crops. The resilient growth of S. parvula was associated with key traits synergistically allowing continued primary root growth, expansion of xylem vessel elements across the root-shoot continuum, and the high capacity to maintain tissue water levels by developing larger and thicker leaves while facilitating continued photosynthesis during salt stress. In turn, the stress-resilient growth during the vegetative phase of S. parvula allowed a successful transition to a reproductive phase via early flowering followed by the development of larger siliques with viable seeds on salt-treated plants. Additionally, the success of self-fertilization in early flowering stages was dependent on salt-induced filament elongation. Our results suggest that the maintenance of leaf water status and enhancement of selfing in early flowers to ensure reproductive success are among the most influential traits that contribute to the extremophilic lifestyle of S. parvula in its natural habitat.
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.
Alternative splicing extends the coding potential of genomes by creating multiple isoforms from one gene. Isoforms can render transcript specificity and diversity to initiate multiple responses required during transcriptome adjustments in stressed environments. Although the prevalence of alternative splicing is widely recognized, how diverse isoforms facilitate stress adaptation in plants that thrive in extreme environments are unexplored. Here we examine how an extremophyte model, Schrenkiella parvula, coordinates alternative splicing in response to high salinity compared to a salt-stress sensitive model, Arabidopsis thaliana. We use Iso-Seq to generate full length reference transcripts and RNA-seq to quantify differential isoform usage in response to salinity changes. We find that single-copy orthologs where S. parvula has a higher number of isoforms than A. thaliana as well as S. parvula genes observed and predicted using machine learning to have multiple isoforms are enriched in stress associated functions. Genes that showed differential isoform usage were largely mutually exclusive from genes that were differentially expressed in response to salt. S. parvula transcriptomes maintained specificity in isoform usage assessed via a measure of expression disorderdness during transcriptome reprogramming under salt. Our study adds a novel resource and insight to study plant stress tolerance evolved in extreme environments.
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