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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. 

Summary Plant adaptation to a desert environment and its endemic heat stress is poorly understood at the molecular level. The naturally heat‐tolerant Brassicaceae speciesAnastatica hierochunticais an ideal extremophyte model to identify genetic adaptations that have evolved to allow plants to tolerate heat stress and thrive in deserts.We generated anA. hierochunticareference transcriptome and identified extremophyte adaptations by comparingArabidopsis thalianaandA. hierochunticatranscriptome responses to heat, and detecting positively selected genes inA. hierochuntica.The two species exhibit similar transcriptome adjustment in response to heat and theA. hierochunticatranscriptome does not exist in a constitutive heat ‘stress‐ready’ state. Furthermore, theA. hierochunticaglobal transcriptome as well as heat‐responsive orthologs, display a lower basal and higher heat‐induced expression than inA. thaliana. Genes positively selected in multiple extremophytes are associated with stomatal opening, nutrient acquisition, and UV‐B induced DNA repair while those unique toA. hierochunticaare consistent with its photoperiod‐insensitive, early‐flowering phenotype.We suggest that evolution of a flexible transcriptome confers the ability to quickly react to extreme diurnal temperature fluctuations characteristic of a desert environment while positive selection of genes involved in stress tolerance and early flowering could facilitate an opportunistic desert lifestyle.