Transcriptomics of plant responses to apical damage reveals no negative correlation between tolerance and defense

While one may expect the loss of plant tissue by animal herbivores to be universally detrimental to a plant’s fitness, a wide range of tolerance responses exists, including undercompensation (lower fitness when damaged), equal compensation, and even overcompensation (increased fitness when damaged). Theory predicts that these responses could be constrained by the investment into defensive chemicals and structures produced for improving resistance in damaged tissues, and thus tolerance and induced defense could be considered alternative strategies to the selection pressure imposed by herbivory. To determine which genetic pathways underlie differences in compensatory (i.e., growth and fitness) responses to damage by tissue loss, and to test their relation with pathways involved in defense, we performed a controlled greenhouse study to measure total gene expression via RNA-sequencing of undamaged and mechanically damaged plants of three Arabidopsisthaliana genotypes that differ in their compensatory performances: Columbia-4, Landsberg erecta, and a recombinant inbred line (RIL) from a Columbia-4 × Landsberg erecta cross. Among the many genetic pathways that responded to clipping, Columbia-4 significantly up-regulated genes involved in secondary defense chemistry and equally compensated for fitness while Landsberg erecta and the RIL both undercompensated and significantly down-regulated secondary defense pathways. The genotypes’ different compensatory performances are thus positively correlated with their differential investments into secondary metabolism following tissue loss. This study identifies differential post-damage gene regulation of growth, developmental signaling, and environmental response pathways in A. thaliana, and provides the first transcriptomic evidence counter to the presumed tradeoff between tolerance and defense in plant-herbivore interactions.