Plasticity in ploidy underlies plant fitness compensation to herbivore damage

How plants mitigate damage by animal herbivores is a fundamental ecological and evolutionary question of plant-animal interactions. Some plants can increase their fitness when damaged in a phenomenon termed 'overcompensation'. Despite overcompensation being observed in a variety of plant species, its mechanistic basis remains elusive. Recent research has shown that the Arabidopsis thaliana genotype Columbia-4 employs endoreduplication, the replication of the genome without mitosis, following damage and that it overcompensates for seed yield. The related genotype Landsberg erecta, in contrast, does not increase its endoreduplication following damage and suffers reduced seed yield. While these results suggest that a plant's ability to plastically increase its ploidy during regrowth may promote its mitigation of damage, no studies have explicitly linked the endoreduplication genetic pathway to the regrowth and fitness of damaged plants. By comparing fitness and ploidy between undamaged and damaged plants of Columbia-4, Landsberg erecta and their offspring, we provide evidence that endoreduplication is directly involved in compensatory performance. We then overexpressed an endoreduplication regulator and compared this mutant's endoreduplication and compensation with its background genotype Columbia-0, an undercompensator. Enhancing Columbia-0's ability to endoreduplicate during regrowth led to the complete mitigation of the otherwise detrimental effects of damage on its fitness. These results suggest that the ability of these plants to increase their ploidy via endoreduplication directly impacts their abilities to compensate for damage, providing a novel mechanism by which some plants can mitigate or even benefit from apical damage with potential across the wide range of plant taxa that endoreduplicate.