Species-specific, accession-specific, and common responses of foliar phytohormones and morphological traits to drought and herbivory

BACKGROUND: Plants are exposed to various environmental challenges. Especially with ongoing climate change, droughts and insect outbreaks are expected to become more frequent. Plant responses to these challenges are mediated by interacting phytohormonal pathways that influence plant growth, but little is known how these responses to single and combined challenges vary across different scales, within and between species. Thus, we investigated species- and accession-specific responses to two environmental challenges in three perennial plant species and compared the responses between species. Clones of several 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. After the exposure, foliar phytohormones and various morphological traits were quantified. RESULTS: Plants of T. vulgare did not respond in jasmonic acid (JA) levels, but showed an increase in abscisic acid (ABA) and a reduced aboveground biomass, particularly under the combined challenges. Plants of S. dulcamara exhibited similar responses, but JA levels were enhanced by all treatments. In contrast, P. nigra uniquely induced salicylic acid under the combined treatment, but showed no impacts on growth. Phenotypic plasticity reflected these species-specific patterns, with none of the phytohormones or morphological traits exhibiting uniform plasticity across species, but with substantial accession-specific pattern. Structural equation models further revealed distinct phytohormone-mediated pathways underlying morphological traits, potentially linking environmental challenges and accessions to specific plant responses within each species. Besides these species-specific differences, several traits responded consistently in all three species to the environmental challenges. Jasmonoyl-isoleucine was induced by herbivory and the combined treatment, 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. CONCLUSIONS: Our results indicate that plant responses to similar challenges include both species-specific and conserved components. The combined treatment elicited the strongest responses, suggesting that simultaneous challenges under climate change may have complex effects on plant performance. The intra- and interspecific differences revealed here highlight the need to further explore the mechanisms underlying this specificity and understand patterns of plant resilience.