Disentangling the influence of water limitation and simultaneous above and belowground herbivory on plant tolerance and resistance to stress

Abstract

Plants face multiple biotic and abiotic stressors simultaneously. Many species can tolerate and resist stress, but countermeasures differ between roots and leaves. Since herbivores and environmental conditions modulate costs and benefits of plant defence traits, stress responses are context‐dependent. We examined whole‐plant tolerance and resistance responses to individual and combined effects of above and belowground herbivory under variable water conditions. We manipulated water availability and access by two common herbivores (Spodoptera exigua caterpillars and Meloidogyne incognita nematodes) to Solanum lycocarpum. Plants were either watered based on historical regional averages or the 30% reduction predicted by IPCC studies. Herbivory treatments included isolated above (AG) and belowground (BG) attacks, simultaneous (AGBG) attacks and no‐herbivory controls. We then parameterized generalized linear mixed‐effects models with data on plant survival, leaf and root biomass accumulation, root complexity and terpenoid concentration. Foliar herbivory increased terpenoid concentrations in roots relative to no‐herbivory plants under control water but decreased concentrations in both roots and leaves under drought. Similarly, root feeders increased concentrations of terpenoids in leaves under control water but decreased concentrations only in roots under drought. Plants challenged with AGBG herbivory had greater whole‐plant biomass (i.e. tolerance) and lower total concentrations of defensive compounds (i.e. resistance) than plants exposed to no‐herbivore controls, regardless of water conditions. Importantly, the capacity of plants to grow or produce terpenoids changes when herbivory level is considered. In plants exposed to AGBG herbivory, greater nematode infection was related to decreases in whole‐plant biomass and marginal increases in total terpenoid concentration. Ultimately, accounting only for individual AG and BG responses would have led to different conclusions and underestimated the magnitude of S. lycocarpum's compensatory responses. A ‘whole‐plant’ approach revealed that belowground herbivory is the primary driver of tolerance in plants surviving moderate water stress. Synthesis. Whole‐plant responses to stress in variable environments are complex, and their comprehensive understanding requires accounting for belowground herbivores and root responses.

Tolerance Mitigates Gall Effects When Susceptible Plants Fail to Elicit Induced Defense

“…This can be explained by a reduction in photosynthetic plant tissue as well as the high cost of defenses [ 56 ]. In this way, resistant genotypes could be favored in high herbivory damage scenarios, having a high cost associated with resistance and, therefore, a disadvantage in low herbivory damage scenarios [ 59 , 67 , 68 ]. Thus, considering that the susceptible plants of B. brevipes showed similar performance in comparison with the resistant plants, our results suggest that these plants invest more resources in defense.…”

“…All plants were sampled from a relatively small area with homogeneous soil characteristics, which may explain the low variation in nutrient concentrations in both plant groups. In addition, soil nutritional intake is low in savannah plant species [ 68 ], which may lead to similarities in nutritional concentrations between resistant and susceptible plants.…”

Water availability and plant–herbivore interactions

“…For instance, SA (Khan et al, 2019) and JA (Sheteiwy et al, 2018) applications enhance drought resistance. In addition to phytohormones, other secondary metabolites have also been shown to play critical roles in both drought resistance and direct antiherbivore defenses, for instance, glucosinolates (Bennett and Wallsgrove, 1994;Salehin et al, 2019), terpenoids (Mundim et al, 2021;Peñuelas and Staudt, 2010;Zhou and Jander, 2022), flavonoids (Hernández et al, 2006;Li et al, 2022b), and protease inhibitors (Fan et al, 2019;Lin et al, 2021b;Nguyen et al, 2016a;Zhang et al, 2008). Contrary to the speculated synergism between drought resistance and antiherbivore defenses, a negative correlation between percentage biomass loss under herbivory and water deficit across accessions of Arabidopsis has been reported, suggesting a lack of synergisms (Davila Olivas et al, 2017).…”

Biosynthesis and the Transcriptional Regulation of Terpenoids in Tea Plants (Camellia sinensis)

“…Monoterpenes (linalool, limonene, myrcene, and trans-β-ocimene) and some sesquiterpenes (farnesene, nerolidol, and caryophyllene) are common constituents of floral scents [ 4 , 15 , 16 , 17 ]. In addition, these terpenoid substances might serve as important signals mediating interactions between plants and herbivores, and they have potential applications in the pharmaceutical, food, and cosmetic industries [ 6 , 18 , 19 , 20 , 21 ].…”