Evolution of cold tolerance in the highly stress tolerant samphires and relatives (Salicornieae: Amaranthaceae)

Cold climate is considered one of the main barriers to plant distributions, confining many clades to their ancestrally tropical biome. However, recent evidence suggests biome transitions may be more frequent than previously thought. Here, we study the evolution of cold tolerance in the globally distributed and highly stress tolerant Salicornieae (Salicornioideae, Amaranthaceae s.l.). We first generate a phylogeny comprising almost all known species (85-90%), using newly generated and published sequences. Next, we use geographical occurrence data to document in which clades and geographic regions cold tolerant species occur, and reconstruct how cold tolerance evolved. Finally, we test for correlated evolution between cold tolerance and the annual life form. We find that cold tolerance has evolved independently in up to four Northern Hemisphere lineages. Annuals are more likely to evolve cold tolerance in certain clades; however, other clades comprise highly cold tolerant perennials, indicating the presence of different strategies for adapting to cold environments. Our findings add to mounting evidence for multiple independent out-of-the-tropics transitions among close relatives of flowering plants and raise new questions on the ecological and physiological mechanism(s) of cold adaptation in Salicornieae.