From atoms to genomes: fitness tradeoffs between polyploidy and potassium limitation in A. thaliana

Whole genome duplication can create polyploids, individuals with three or more chromosome sets. Polyploidy is known to have occurred throughout plant lineages and is hypothesized to have driven adaptive radiation though the mechanism is unclear. A number of independent genome duplication events are estimated to have occurred at the Cretaceous–Tertiary (KT) boundary, which is associated with the impact of a large meteorite 65 MYA and many others, including yeast, are estimated to be 200 MYA. Polyploidy may have provided an advantage during the period of extreme environmental instability and mass extinction following this meteorite impact (Fawcetta et al., 2009). Data mining of the ionomic profiles of Arabidopsis accessions identified Wa-1, a wild caught tetraploid, as the highest potassium accumulator. Using a RIL population developed from the interploidy cross Col x Wa-1 and multiple wild-caught and laboratory-induced autopolyploids we have demonstrated that polyploidy increases shoot potassium accumulation, as well other symplastically transported ions. Via reciprocal grafting experiments and mutants with altered root development we have demonstrated that shoot potassium levels are controlled by changes in root ploidy and that changes in root cell size are sufficient to recapitulate this phenotype. While tetraploid Arabidopsis is typically less fecund, the alteration in tetraploid physiology is sufficient to provide a fitness advantage to tetraploid Arabidopsis accessions under low potassium. In addition, the lines exhibit lower sodium accumulation and better K/Na ratio under sodium stress. Thus, tetraploidy provides an environmentally contingent fitness advantage over diploidy. Previously increased resistance to salinity in yeast and citrus (Saleh et al., 2008; Dhar et al., 2011), and water stress in plum and paper birch (Pustovoitova et al., 1996; Li et al., 1996) have been noted. A vast continental saline desert occurred over much of Pangea, which finally broke up 192 MYA, coinciding with some estimates for whole genome duplications. It is possible that salinity tolerance and edaphic selection, rather than genomic organization and “evolvabilty”, may have played a role in the widespread distribution of polyploidy in plants.