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Summary Boron toxicity is a world‐wide problem for crops, yet we have a limited understanding of the genetic responses and adaptive mechanisms to this stress in plants.We employed a cross‐species comparison between boron stress‐sensitiveArabidopsis thalianaand its boron stress‐tolerant extremophyte relativeSchrenkiella parvula, and a multi‐omics approach integrating genomics, transcriptomics, metabolomics and ionomics to assess plant responses and adaptations to boron stress.Schrenkiella parvulamaintains lower concentrations of total boron and free boric acid than Arabidopsis when grown with excess boron.Schrenkiella parvulaexcludes excess boron more efficiently than Arabidopsis, which we propose is partly driven by SpBOR5, a boron transporter that we functionally characterize in this study. Both species use cell walls as a partial sink for excess boron. When accumulated in the cytoplasm, excess boron appears to interrupt RNA metabolism. The extremophyteS. parvulafacilitates critical cellular processes while maintaining the pool of ribose‐containing compounds that can bind with boric acid.TheS. parvulatranscriptome is pre‐adapted to boron toxicity. It exhibits substantial overlaps with the Arabidopsis boron‐stress responsive transcriptome. Cell wall sequestration and increases in global transcript levels under excess boron conditions emerge as key mechanisms for sustaining plant growth under boron toxicity. 

SUMMARY Schrenkiella parvula, a leading extremophyte model in Brassicaceae, can grow and complete its lifecycle under multiple environmental stresses, including high salinity. Yet, the key physiological and structural traits underlying its stress‐adapted lifestyle are unknown along with trade‐offs when surviving salt stress at the expense of growth and reproduction. We aimed to identify the influential adaptive trait responses that lead to stress‐resilient and uncompromised growth across developmental stages when treated with salt at levels known to inhibit growth in Arabidopsis and most crops. Its resilient growth was promoted by traits that synergistically allowed primary root growth in seedlings, the expansion of xylem vessels across the root‐shoot continuum, and a high capacity to maintain tissue water levels by developing thicker succulent leaves while enabling photosynthesis during salt stress. A successful transition from vegetative to reproductive phase was initiated by salt‐induced early flowering, resulting in viable seeds. Self‐fertilization in salt‐induced early flowering was dependent upon filament elongation in flowers otherwise aborted in the absence of salt during comparable plant ages. The maintenance of leaf water status promoting growth, and early flowering to ensure reproductive success in a changing environment, were among the most influential traits that contributed to the extremophytic lifestyle ofS. parvula.