Drought stress drives sex-specific differences in plant resistance against herbivores between male and female poplars through changes in transcriptional and metabolic profiles

Drought stress poses adverse influence on plant growth and further alters plant-herbivore interactions. Such effect is enhanced as drought occurrence is reported to increase due to global warming. Although dioecious plant species have shown sex-specific response to drought stress through the changes in growth performance and stress tolerance, whether such changes will drive sex-specific differences in defense against herbivores between male and female plant conspecifics is barely studied. In the current study, female and male poplar full-siblings were submitted to moderate (75 % field water capacity) and severe drought (50 % field water capacity) stresses, followed by herbivore growth and feeding bioassays to test the effect of plant gender on herbivore growth and feeding performance of two specialist and two generalist leaf herbivores. The results showed that although the growth of both plant sexes was inhibited by the two drought levels, male plants performed better than female conspecifics. In the paired-choice bioassays, the specialist herbivores preferred female plants while the generalist herbivores fed more on the male plants without drought stress. Both the moderate and severe drought stresses reversed such preferences. In the triple-choice bioassays, the specialist herbivores preferred female control plants while the generalist herbivores fed more on female plants under severe drought. In addition, the specialist herbivores fed on female plants from severe drought stress grew the worst while the generalist herbivores gained the highest fresh weight. The transcriptomic and metabolomic profiling revealed that female plant leaves contained higher levels of flavonoids than males under control condition while severe drought stress remarkably reduced the levels of defensive metabolites such as flavonoids, isoflavonoids, neoflavonoids and alkaloids in female but not in male plant leaves.