To understand how comprehensive plant defense phenotypes will respond to global change, we investigated the legacy effects of elevated CO2on the relationships between chemical resistance (constitutive and induced via mechanical damage) and regrowth tolerance in four milkweed species (
- NSF-PAR ID:
- Publisher / Repository:
- Wiley Blackwell (John Wiley & Sons)
- Date Published:
- Journal Name:
- Ecology and Evolution
- Page Range / eLocation ID:
- p. 5416-5430
- Medium: X
- Sponsoring Org:
- National Science Foundation
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null (Ed.)Background Oviposition decisions are critical to the fitness of herbivorous insects and are often impacted by the availability and condition of host plants. Monarch butterflies ( Danaus plexippus ) rely on milkweeds ( Asclepias spp.) for egg-laying and as food for larvae. Previous work has shown that monarchs prefer to oviposit on recently regrown plant tissues (after removal of above-ground biomass) while larvae grow poorly on plants previously damaged by insects. We hypothesized that these effects may depend on the life-history strategy of plants, as clonal and non-clonal milkweed species differ in resource allocation and defense strategies. Methodology/Principal Findings We first confirmed butterfly preference for regrown tissue in a field survey of paired mowed and unmowed plots of the common milkweed A. syriaca . We then experimentally studied the effects of plant damage (comparing undamaged controls to plants clipped and regrown, or damaged by insects) on oviposition choice, larval performance, and leaf quality of two closely related clonal and non-clonal species pairs: (1) A. syriaca and A. tuberosa , and (2) A. verticillata and A. incarnata . Clonal and non-clonal species displayed different responses to plant damage, impacting the proportions of eggs laid on plants. Clonal species had similar mean proportions of eggs on regrown and control plants (≈35–40% each), but fewer on insect-damaged plants (≈20%). Meanwhile non-clonal species had similar oviposition on insect-damaged and control plants (20–30% each) but more eggs on regrown plants (40–60%). Trait analyses showed reduced defenses in regrown plants and we found some evidence, although variable, for negative effects of insect damage on subsequent larval performance. Conclusions/Significance Overall, non-clonal species are more susceptible and preferred by monarch butterflies following clipping, while clonal species show tolerance to clipping and induced defense to insect herbivory. These results have implications for monarch conservation strategies that involve milkweed habitat management by mowing. More generally, plant life-history may mediate growth and defense strategies, explaining species-level variation in responses to different types of damage.more » « less
ABSTRACT Background Echium plantagineum, a native of Europe and Africa, is a noxious invasive weed in Australia forming monocultural stands in pastures and rangelands. It produces a complex mixture of bioactive secondary metabolites, including toxic pyrrolizidine alkaloids (PAs), that protect the plant from insect and livestock herbivory and naphthoquinones (NQs), which suppress competition from weeds, insects and pathogens, and also influence invasion success. However, the extent to which allelochemical production is impacted by environmental factors, thereby influencing plant defense against pests, remains unclear. Results
Following plant stress induced by drought, herbivory and high temperature, extracts of
E. plantagineumshoots and roots were subjected to metabolic profiling by UPLC‐MS‐DAD‐ QToF mass spectrometry. Abundance of NQs, especially deoxyshikonin, shikonin and dimethylacrylshikonin, rapidly increased in roots exposed to elevated temperatures. Water withholding initially increased NQ abundance, but prolonged drought resulted in reduced total PAs and NQs. Intraspecific competition elevated the production of NQs, whereas simulated herbivory had no initial effect on NQs. Following herbivory, the abundance of the PA 3′‐ O‐acetylechimidine‐ N‐oxide in seedling shoots was increased. Conclusions
Differential accumulation of defense metabolites by
E. plantagineumfollowing exposure to various stressors suggested stress‐dependent biosynthetic regulation, particularly with respect to NQ production, which was rapidly induced following drought, intraspecific competition and high temperature treatment, thereby positively impacting resistance or defense against herbivores, weeds and pathogens. We propose that trade‐offs between above‐ and below‐ground metabolism in E. plantagineummay facilitate allelochemical production in response to stress, rendering plants with an enhanced ability to defend against other neighboring plants, insects and microbes, with allelochemical production further facilitated by catabolic recycling following lengthier exposure to stress. © 2019 Society of Chemical Industry
Plants possess myriad defenses against their herbivores, including constitutive and inducible chemical compounds and regrowth strategies known as tolerance. Recent studies have shown that plant tolerance and resistance are positively associated given they are co‐localized in the same molecular pathway, the oxidative pentose phosphate pathway. However, given that both defensive strategies utilize carbon skeletons from a shared resource pool in the oxidative pentose phosphate pathway there are likely costs in maintaining both resistance‐tolerance strategies. Here we investigate fitness costs in maintaining both strategies by utilizing a double knockout of
cyp79B2and cyp79B3, key enzymes in the biosynthetic process of indole glucosinolates, which convert tryptophan to indole‐3‐acetaldoxime (IAOx) and is further used to produce indole glucosinolates. These mutant plants are devoid of any indole glucosinolates thus reducing plant resistance. Results show that knocking out indole glucosinolate production and thus one of the resistance pathways leads to an approximate 94% increase in fitness compensation shifting the undercompensating wild‐type Columbia‐0 to an overcompensating genotype following damage. We discuss the potential mechanistic basis for the observed patterns.
The effects of climate change on plants and ecosystems are mediated by plant hydraulic traits, including interspecific and intraspecific variability of trait phenotypes. Yet, integrative and realistic studies of hydraulic traits and climate change are rare. In a semiarid grassland, we assessed the response of several plant hydraulic traits to elevated CO2(+200 ppm) and warming (+1.5 to 3°C; day to night). For leaves of five dominant species (three graminoids and two forbs), and in replicated plots exposed to 7 years of elevated CO2, warming, or ambient climate, we measured: stomatal density and size, xylem vessel size, turgor loss point, and water potential (pre‐dawn). Interspecific differences in hydraulic traits were larger than intraspecific shifts induced by elevated CO2and/or warming. Effects of elevated CO2were greater than effects of warming, and interactions between treatments were weak or not detected. The forbs showed little phenotypic plasticity. The graminoids had leaf water potentials and turgor loss points that were 10% to 50% less negative under elevated CO2; thus, climate change might cause these species to adjust their drought resistance strategy away from tolerance and toward avoidance. The C4 grass also reduced allocation of leaf area to stomata under elevated CO2, which helps explain observations of higher soil moisture. The shifts in hydraulic traits under elevated CO2were not, however, simply due to higher soil moisture. Integration of our results with others' indicates that common species in this grassland are more likely to adjust stomatal aperture in response to near‐term climate change, rather than anatomical traits; this contrasts with apparent effects of changing CO2on plant anatomy over evolutionary time. Future studies should assess how plant responses to drought may be constrained by the apparent shift from tolerance (via low turgor loss point) to avoidance (via stomatal regulation and/or access to deeper soil moisture).
Animals rely on a balance of endogenous and exogenous sources of immunity to mitigate parasite attack. Understanding how environmental context affects that balance is increasingly urgent under rapid environmental change. In herbivores, immunity is determined, in part, by phytochemistry which is plastic in response to environmental conditions. Monarch butterflies
Danaus plexippus, consistently experience infection by a virulent parasite Ophryocystis elektroscirrha, and some medicinal milkweed ( Asclepias) species, with high concentrations of toxic steroids (cardenolides), provide a potent source of exogenous immunity.
We investigated plant‐mediated influences of elevated CO2(eCO2) on endogenous immune responses of monarch larvae to infection by
O. elektroscirrha. Recently, transcriptomics have revealed that infection by O. elektroscirrhadoes not alter monarch immune gene regulation in larvae, corroborating that monarchs rely more on exogenous than endogenous immunity. However, monarchs feeding on medicinal milkweed grown under eCO2lose tolerance to the parasite, associated with changes in phytochemistry. Whether changes in milkweed phytochemistry induced by eCO2alter the balance between exogenous and endogenous sources of immunity remains unknown.
We fed monarchs two species of milkweed;
A. curassavica(medicinal) and A. incarnata(non‐medicinal) grown under ambient CO2(aCO2) or eCO2. We then measured endogenous immune responses (phenoloxidase activity, haemocyte concentration and melanization strength), along with foliar chemistry, to assess mechanisms of monarch immunity under future atmospheric conditions.
The melanization response of late‐instar larvae was reduced on medicinal milkweed in comparison to non‐medicinal milkweed. Moreover, the endogenous immune responses of early‐instar larvae to infection by
O. elektroscirrhawere generally lower in larvae reared on foliage from aCO2plants and higher in larvae reared on foliage from eCO2plants. When grown under eCO2, milkweed plants exhibited lower cardenolide concentrations, lower phytochemical diversity and lower nutritional quality (higher C:N ratios). Together, these results suggest that the loss of exogenous immunity from foliage under eCO2results in increased endogenous immune function.
Animal populations face multiple threats induced by anthropogenic environmental change. Our results suggest that shifts in the balance between exogenous and endogenous sources of immunity to parasite attack may represent an underappreciated consequence of environmental change.