Evolutionary origins of abnormally large shoot sodium accumulation in nonsaline environments within the Caryophyllales

The prevalence of sodium (Na)-'hyperaccumulator' species, which exhibit abnormally large shoot sodium concentrations ([Na]shoot ) when grown in nonsaline environments, was investigated among angiosperms in general and within the Caryophyllales order in particular. Shoot Na concentrations were determined in 334 angiosperm species, representing 35 orders, grown hydroponically in a nonsaline solution. Many Caryophyllales species exhibited abnormally large [Na]shoot when grown hydroponically in a nonsaline solution. The bimodal distribution of the log-normal [Na]shoot of species within the Caryophyllales suggested at least two distinct [Na]shoot phenotypes within this order. Mapping the trait of Na-hyperaccumulation onto the phylogenetic relationships between Caryophyllales families, and between subfamilies within the Amaranthaceae, suggested that the trait evolved several times within this order: in an ancestor of the Aizoaceae, but not the Phytolaccaceae or Nyctaginaceae, in ancestors of several lineages formerly classified as Chenopodiaceae, but not in the Amaranthaceae sensu stricto, and in ancestors of species within the Cactaceae, Portulacaceae, Plumbaginaceae, Tamaricaceae and Polygonaceae. In conclusion, a disproportionate number of Caryophyllales species behave as Na-hyperaccumulators, and multiple evolutionary origins of this trait can be identified within this order.