Down-regulation of systemin after herbivory is associated with increased root allocation and competitive ability in Solanum nigrum

After simulated herbivory, inflicted by a treatment involving wounding and the application of Manduca sexta oral secretions (OS) to mechanical wounds (OS-elicitation), transcripts of the systemin-precursor, prosystemin, are down-regulated in black nightshade (Solanum nigrum). Since S. nigrum silenced in prosystemin expression (IRSys) has unaltered herbivore resistance but produced more above-ground biomass and berries than did wild-type (WT) competitors in a pilot experiment, we examine the hypothesis that systemin helps the plant to tolerate rather than resist folivory. When plants competed, IRSys plants produced significantly more berries than did WTs. Berry production of OS-elicited and unelicited WTs did not differ, but OS-elicited WTs that were additionally treated with systemin (systemin-augmented OS-elicited WTs) produced fewer berries than did unelicited WT competitors. When root-competition was prevented by a barrier, no differences in berry production were found. Growth experiments revealed that OS-elicited WTs and IRSys plants produced more roots than did untreated WTs, whereas systemin-augmented OS-elicited WTs did not. Microarray analyses of leaves revealed that fitness differences were associated with the transcriptional regulation of sugar and spermine metabolism. We propose that down-regulation of systemin after herbivory is associated with increased root allocation which allows plants to more effectively compete with conspecifics and may allow plants to compensate for tissue losses during herbivory.