Plants maintain microbial associations whose functions remain largely unknown. For the past 15 y, we have planted the annual postfire tobacco Nicotiana attenuata into an experimental field plot in the plant’s native habitat, and for the last 8 y the number of plants dying from a sudden wilt disease has increased, leading to crop failure. Inadvertently we had recapitulated the common agricultural dilemma of pathogen buildup associated with continuous cropping for this native plant. Plants suffered sudden tissue collapse and black roots, symptoms similar to a Fusarium–Alternaria disease complex, recently characterized in a nearby native population and developed into an in vitro pathosystem for N. attenuata. With this in vitro disease system, different protection strategies (fungicide and inoculations with native root-associated bacterial and fungal isolates), together with a biochar soil amendment, were tested further in the field. A field trial with more than 900 plants in two field plots revealed that inoculation with a mixture of native bacterial isolates significantly reduced disease incidence and mortality in the infected field plot without influencing growth, herbivore resistance, or 32 defense and signaling metabolites known to mediate resistance against native herbivores. Tests in a subsequent year revealed that a core consortium of five bacteria was essential for disease reduction. This consortium, but not individual members of the root-associated bacteria community which this plant normally recruits during germination from native seed banks, provides enduring resistance against fungal diseases, demonstrating that native plants develop opportunistic mutualisms with prokaryotes that solve context-dependent ecological problems.
Abstract1. Plants emit volatile blends specific to particular herbivore interactions, which predators and parasitoids learn to associate with prey, increasing herbivore mortality and thereby plant fitness in a phenomenon termed indirect defence.2. Herbivore-induced plant volatile blends commonly include both rapid, transient green leaf volatiles (GLVs) and delayed, enduring sesquiterpenes. A few laboratory studies indicate that insects can use plant volatiles to time behaviour, but it is not known whether and how the temporal dynamics of plant volatile blends influence their function in indirect defence.3. We characterized the activity of the native herbivores Manduca sexta and Tupiocoris notatus and their predators, Geocoris spp., on their host plant Nicotiana attenuata in their natural habitat. Diurnal predator activity only partially overlapped with variable herbivore activity, and herbivore attack at the beginning or end of the photophase elicited plant volatile blends with distinct GLV and sesquiterpene profiles.4. In field trials, day-active Geocoris spp. predators preferred morning-over eveningtypical GLV blends. Using plants genetically transformed so as to be unable to produce specific volatiles, we found that GLVs increased predation after dawn elicitations, whereas sesquiterpenes increased predation after dusk elicitations in field trials.5. We conclude that predators respond to temporal differences in plant volatile blends, and that the different dynamics of specific volatiles permit effective indirect defence despite variable herbivore activity in nature. K E Y W O R D SGeocoris sp., green leaf volatiles, herbivore-induced plant volatiles, Manduca sexta, Nicotiana attenuata, sesquiterpenes, temporal dynamics, Tupiocoris notatus | INTRODUCTIONFlowering plants (angiosperms) and the insect herbivores that attack them are among the most diverse groups of multicellular life on Earth.Perhaps it is not surprising that plants can induce defences with great specificity in response to attack by particular insect herbivores (reviewed in Schuman & Baldwin, 2016), as exemplified by the specificity of herbivore-induced plant volatiles (HIPVs, reviewed e.g. in Howe & Jander, 2008). Much work on plant-insect interactions is done under controlled conditions required to dissect intricate mechanisms of specificity in elicitation and response. However, to be useful for wild plants, responses must keep functioning in the face of environmental disturbances: they must be robust (Kitano, 2004). Most plant and insect communities in nature are unevenly distributed over space andtime (Agrawal, Lau, & Hambäck, 2006) and changes in spatiotemporal co-occurrence may alter the course of plant-insect interactions (Brown, 2003;Kolasa & Rollo, 1991;López-Carretero, Díaz-Castelazo, Boege, & Rico-Gray, 2014). Thus it is important to ask how robust are plant defences when faced with the variable herbivore communities that characterize natural interactions.Plant indirect defences are perhaps more susceptible to disturbance by shifts in t...
Negative frequency-dependent selection (NFDS) has been shown to maintain polymorphism in a diverse array of traits. The actionof NFDS has been confirmed through modeling, experimental approaches, and genetic analyses. In this study, we investigated NFDS in the wild using morph-frequency changes spanning a 20-year period from over 30 dimorphic populations of Datura wrightii. In these populations, plants either possess glandular (sticky) or non-glandular (velvety) trichomes, and the ratio of these morphs varies substantially among populations. Our method provided evidence that NFDS, rather than drift or migration, is the primary force maintaining this dimorphism. Most populations that were initially dimorphic remained dimorphic, and the overall mean and variance in morph frequency did not change over time. Furthermore, morph-frequency differences were not related to geographic distances. Together, these results indicate that neither directional selection, drift, or migration played a substantial role in determining morph frequencies. However, as predicted by negative frequency-dependent selection, we found that the rare morph tended to increase in frequency, leading to a negative relationship between the change in the frequency of the sticky morph and its initial frequency. In addition, we found that morph-frequency change over time was significantly correlated with the damage inflicted by two herbivores: Lema daturaphila and Tupiochoris notatus. The latter is a specialist on the sticky morph and damage by this herbivore was greatest when the sticky morph was common. The reverse was true for L. daturaphila, such that damage increased with the frequency of the velvety morph. These findings suggest that these herbivores contribute to balancing selection on the observed trichome dimorphism. K E Y W O R D S : balanced polymorphism, Datura wrightii, glandular trichomes, plant-herbivore interactions. Impact SummaryWe present a long-term observational study of morph frequency changes in naturally dimorphic populations of Datura wrightii. We were able to determine that negative frequency-dependent selection-rather than drift, migration, or directional selection-is the main contributor to the main-tenance of this dimorphism over the past 20 years. We also sampled herbivory across our sample of populations and found evidence suggesting that the damage inflicted by two species of specialist herbivores may underlie this selective regime.Negative frequency-dependent selection (NFDS)-a selective regime in which rare morphs are favored over common 8 3
Animal signals evolve by striking a balance between the need to convey information through particular habitats and the limitations of what types of signals can most easily be produced and perceived. Here, we present new results from field measures of undisturbed behavior and biochemical analyses of scent marks from 12 species of Sceloporus lizards to explore whether evolutionary changes in chemical composition are better predicted by measures of species behavior, particularly those associated with visual displays, chemoreception, and locomotion, or by measures of habitat climate (precipitation and temperature). We found that more active lizard species used fewer compounds in their volatile scent marks, perhaps conveying less specific information about individual and species identity. Scent marks from more active lizard species also had higher proportions of saturated fatty acids, and the evolution of these compounds has been tracking the phylogeny closely as we would expect for a metabolic byproduct. In contrast, the proportions of unsaturated fatty acids were better explained by evolutionary shifts in habitat temperature (and not precipitation), with species in warmer climates using almost no volatile unsaturated fatty acids. The proportion of aldehydes was explained by both behavior and environment, decreasing with behavioral activity and increasing with habitat temperature. Our results highlight the evolutionary flexibility of complex chemical signals, with different chemical compounds responding to different elements of the selective landscape over evolutionary time.
The timing of plant volatile emissions is important for a robust indirect defense response. Green leaf volatiles (GLVs) are emitted by plants upon damage but can be suppressed by herbivore-associated elicitors, and the abundance and composition of GLVs vary depending on the timing of herbivore attack. We show that the GLV biosynthetic enzyme HYDROPEROXIDE LYASE (HPL) is transcriptionally regulated by the circadian clock in Nicotiana attenuata. In accordance with transcript abundance of NaHPL, GLV aldehyde pools in intact leaves peaked at night and at subjective night under diurnal and continuous light conditions, respectively. Moreover, although the basal abundance of NaHPL transcripts is upregulated by jasmonate (JA) signaling, JA does not regulate the reduction of NaHPL transcript abundance in damaged leaves by simulated herbivore treatment. Unexpectedly, the plant circadian clock was strongly altered when Manduca sexta larvae fed on N. attenuata, and this was also independent of JA signaling. Lastly, the temporal dynamics of NaHPL transcripts and total GLV emissions were strongly altered by M. sexta larval feeding. Our data suggest that the temporal dynamics of emitted GLV blends result from a combination of damage, JA signaling, herbivore-associated elicitors, and the plant circadian clock.
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