Chromosome amplification and the phenomenon of overcompensation in plants

Background/Question/Methods

Endoreduplication, the replication of the genome without mitosis, leads to endopolyploidy, an increase in cellular chromosome number. Although endoreduplication is widespread among angiosperms and other groups of eukaryotes, the degree to which this process is plastic under varying environmental conditions and its potential adaptive significance are not known. Here, we take the first step toward testing a novel idea – that endoreduplication leads to enhanced growth and reproduction following herbivory, explaining the phenomenon of overcompensation in plants.  Specifically, using flow cytometry, we measured plasticity in chromosome number following the removal of apical dominance (simulating natural herbivory) in two ecotypes of Arabidopsis thaliana: an overcompensator, Columbia, and an undercompensator, Landsberg erecta.  Recombinant inbred lines generated from a cross between these two ecotypes, Columbia and Landsberg erecta, were also assessed to see if there was a general relationship between endoreduplication and fitness.

Results/Conclusions

We report that endopolyploidy of clipped Columbia plants was significantly different than unclipped controls following the removal of apical dominance and regrowth, and that cellular ploidy is positively associated with attributes of fitness (biomass, flower, fruit, and seed production). In contrast, clipped Landsberg erecta showed no significant differences in endopolyploidy and a decrease in seed production compared to unclipped controls; representing a significant genotype X environment interaction between ecotypes. There is also a general relationship between endoreduplication and fitness.  RILs from a cross between Columbia and Landsberg erecta demonstrate that lines that undercompensate have a lower proportion of endopolyploid cells following the removal of apical dominance than those lines that overcompensate following the removal of apical dominance.  Such a strong positive correlation (R²=0.735, P=0.002) between endoreduplication and fitness serves as support for the idea that endoreduplication is involved in determining organismal fitness.  Given that both traits (fitness and endoreduplication) are polygenic, one would expect the relationship to fall apart when crossed if the traits are unrelated, however, the relationship is maintained.  Altering ploidy via endoreduplication adds a previously unknown way in which plants may be able to cope with environmental stress: enhancing regrowth rates and fitness following plant damage.