In plants, phenotypic plasticity, the ability to morphologically adapt to new or broad environmental conditions, is a consequence of long-term evolutionary genetic processes. Thus, plants adapted to low phosphate (P) environments exhibit only limited plasticity to take advantage of nutrient enrichment, a global phenomenon in terrestrial and aquatic environments. In the face of anthropogenic P-enrichment, low nutrient adapted resident plant species are frequently displaced by species with high morphological and genetic plasticity. However, it remains unclear whether plasticity is systemically expressed across molecular, biochemical, physiological, and morphological processes that ultimately contribute to the root and shoot phenotypes of plants. In this study, we demonstrated high plasticity in root-borne traits of sawgrass (Cladium jamaicense), the dominant plant species of the P-impoverished Everglades, and counter the idea of inflexibility in low P adapted species. However, sawgrass expressed inflexibility in processes contributing to shoot phenotypes, in contrast to cattail, which was highly plastic in shoot characteristics in response to P enrichment. In fact, plasticity in cattail shoots is likely a function of its growth response to P that was globally regulated by P-availability at the level of transcription. Plasticity and inflexibility in the growth of both species also diverged in their allocation of P to the chloroplast for growth in cattail versus the vacuole for P storage in sawgrass. In the Everglades, anthropogenic P-enrichment has changed the environment from a P-limited condition, where plasticity in root-borne traits of sawgrass was advantageous, to one of light-competition, where plasticity in shoot-borne traits drives competitive dominance by cattail. We hypothesize that these shifts in plasticity competitive advantage from root to shoots has been a major driver of cattail expansion in the Everglades ecosystem. Further, this understanding of how natural plant species adapt and shift in response to nutrient availability could also be used a model system to optimize agricultural systems to increase efficiencies in food production and protect low nutrient adapted natural systems from cultural eutrophication.