Common, species-specific, and accession-specific responses of foliar phytohormones and morphological traits to drought and herbivory

Background: Plants are exposed to various environmental challenges. With ongoing climate change, droughts and insect outbreaks are expected to become more frequent. Thus, a better understanding is needed of how different plant species respond to such single and combined challenges. This study investigated common versus species-specific responses to environmental challenges in three perennial plant species of different growth forms and whether responses differ intraspecifically among accessions. Clones of different accessions of the herbaceous species Tanacetum vulgare, the woody vine Solanum dulcamara, and the tree Populus nigra were subjected to similar control, herbivory, drought, and combined (drought and herbivory) treatments for the same periods. After the exposure, concentrations of foliar phytohormones and various morphological traits were measured. Results: Across all species, several foliar phytohormones and one of ten morphological traits responded consistently to the environmental challenges. Jasmonoyl-isoleucine was induced by herbivory and the combined treatment, abscisic acid (ABA) by drought and the combined treatment, and indole acetic acid by the combined treatment in all species. Root mass remained unchanged in all species. However, structural equation models (SEMs) revealed a shared regulatory pathway across species in which ABA connected treatment and root mass, indicating a common hormonal response potentially linking challenges to growth responses. Despite these common patterns, species-specific responses were pronounced. In P. nigra, a unique induction of salicylic acid was found under the combined treatment, while aboveground mass and root-shoot ratio remained unaffected by any treatment, in contrast to the other two species. Species-specific SEMs further indicated distinct phytohormone-mediated pathways underlying morphological variation. Phenotypic plasticity reflected these species-specific patterns, with none of the phytohormones or morphological traits exhibiting uniform plasticity across species. Intraspecific variation further shaped responses, as phytohormone and morphological trait plasticity depended on accession, indicating substantial accession-specific plant responses. Conclusions: Our results indicate that some responses to comparable challenges may be conserved across species, while others are species-specific. The combined treatment elicited the most pronounced responses, and such complex responses may become more frequent under current global change. Our study highlights that comprehensive understanding of plant responses requires systematic comparisons at both interspecific and intraspecific scales.