Volatile-mediated oviposition preference for healthy over root-infested plants by the European corn borer.

The selection of oviposition sites by female moths is crucial in shaping their progeny performance and survival, and consequently in determining insect fitness. Selecting suitable plants that promote the performance of the progeny is referred to as the Preference-Performance hypothesis (or 'mother-knows-best'). While root infestation generally reduces the performance of leaf herbivores, little is known about its impact on female oviposition. We investigated whether maize root infestation by the Western corn rootworm (WCR) affects the oviposition preference and larval performance of the European corn borer (ECB). ECB females used leaf volatiles to select healthy plants over WCR-infested plants. Undecane, a compound absent from the volatile bouquet of healthy plants, was the sole compound to be upregulated upon root infestation and acted as a repellent for first oviposition. ECB larvae yet performed better on plants infested below-ground than on healthy plants, suggesting an example of 'bad motherhood'. The increased ECB performance on WCR-infested plants was mirrored by an increased leaf consumption, and no changes in the plant primary or secondary metabolism were detected. Understanding plant-mediated interactions between above- and below-ground herbivores may help to predict oviposition decisions, and ultimately, to manage pest outbreaks in the field.

Immature leaves are the dominant volatile-sensing organs of maize.

Plants perceive herbivory-induced volatiles and respond to them by upregulating their defenses. To date, the organs responsible for volatile perception remain poorly described. Here, we show that responsiveness to the herbivory-induced green leaf volatile (Z)-3-hexenyl acetate (HAC) in terms of volatile emission, transcriptional regulation, and jasmonate defense hormone activation is largely constrained to younger maize leaves. Older leaves are much less sensitive to HAC. In a given leaf, responsiveness to HAC is high at immature developmental stages and drops off rapidly during maturation. Responsiveness to the non-volatile elicitor ZmPep3 shows an opposite pattern, demonstrating that this form of hyposmia (i.e., decreased sense of smell) is not due to a general defect in jasmonate defense signaling in mature leaves. Neither stomatal conductance nor leaf cuticle composition explains the unresponsiveness of older leaves to HAC, suggesting perception mechanisms upstream of jasmonate signaling as driving factors. Finally, we show that hyposmia in older leaves is not restricted to HAC and extends to the full blend of herbivory-induced volatiles. In conclusion, our work identifies immature maize leaves as dominant stress volatile-sensing organs. The tight spatiotemporal control of volatile perception may facilitate within plant defense signaling to protect young leaves and may allow plants with complex architectures to explore the dynamic odor landscapes at the outer periphery of their shoots.

Dynamic environmental interactions shaped by vegetative plant volatiles.

Covering: up to November 2022Plants shape terrestrial ecosystems through physical and chemical interactions. Plant-derived volatile organic compounds in particular influence the behavior and performance of other organisms. In this review, we discuss how vegetative plant volatiles derived from leaves, stems and roots are produced and released into the environment, how their production and release is modified by abiotic and biotic factors, and how they influence other organisms. Vegetative plant volatiles are derived from different biosynthesis and degradation pathways and are released via distinct routes. Both biosynthesis and release are regulated by other organisms as well as abiotic factors. In turn, vegetative plant volatiles modify the physiology and the behavior of a wide range of organisms, from microbes to mammals. Several concepts and frameworks can help to explain and predict the evolution and ecology of vegetative plant volatile emission patterns of specific pathways: multifunctionality of specialized metabolites, chemical communication displays and the information arms race, and volatile physiochemistry. We discuss how these frameworks can be leveraged to understand the evolution and expression patterns of vegetative plant volatiles. The multifaceted roles of vegetative plant volatiles provide fertile grounds to understand ecosystem dynamics and harness their power for sustainable agriculture.

Elevated atmospheric CO2 changes defence allocation in wheat but herbivore resistance persists.

Predicting how plants allocate to different anti-herbivore defences in response to elevated carbon dioxide (CO2) concentrations is important for understanding future patterns of crop susceptibility to herbivory. Theories of defence allocation, especially in the context of environmental change, largely overlook the role of silicon (Si), despite it being the major anti-herbivore defence in the Poaceae. We demonstrated that elevated levels of atmospheric CO2 (e[CO2]) promoted plant growth by 33% and caused wheat (Triticum aestivum) to switch from Si (-19%) to phenolic (+44%) defences. Despite the lower levels of Si under e[CO2], resistance to the global pest Helicoverpa armigera persisted; relative growth rates (RGRs) were reduced by at least 33% on Si-supplied plants, irrespective of CO2 levels. RGR was negatively correlated with leaf Si concentrations. Mandible wear was c. 30% higher when feeding on Si-supplemented plants compared to those feeding on plants with no Si supply. We conclude that higher carbon availability under e[CO2] reduces silicification and causes wheat to increase concentrations of phenolics. However, Si supply, at all levels, suppressed the growth of H. armigera under both CO2 regimes, suggesting that shifts in defence allocation under future climate change may not compromise herbivore resistance in wheat.

Short-term exposure to silicon rapidly enhances plant resistance to herbivory.

Silicon (Si) can adversely affect insect herbivores, particularly in plants that evolved the ability to accumulate large quantities of Si. Very rapid herbivore-induced accumulation of Si has recently been demonstrated, but the level of protection against herbivory this affords plants remains unknown. Brachypodium distachyon, a model Si hyperaccumulating grass, was exposed to the chewing herbivore, Helicoverpa armigera, and grown under three conditions: supplied Si over 34 d (+Si), not supplied Si (-Si), or supplied Si once herbivory began (-Si → +Si). We evaluated the effectiveness of each Si treatment at reducing herbivore performance and measured Si-based defenses and phenolics (another form of defense often reduced by Si). Although Si concentrations remained lower, within 72 h of exposure to Si, -Si → +Si plants were as resistant to herbivory as +Si plants. Both +Si and -Si → +Si treatments reduced herbivore damage and growth, and increased mandible wear compared to -Si. After 6 h, herbivory increased filled Si cell density in -Si → +Si plants, and within 24 h, -Si → +Si plants reached similar filled Si cell densities to +Si plants, although decreased phenolics only occurred in +Si plants. We demonstrate that plants with short-term Si exposure can rapidly accumulate Si-based antiherbivore defenses as effectively as plants with long-term exposure.

Author Correction: Increased insect herbivore performance under elevated CO2 is associated with lower plant defence signalling and minimal declines in nutritional quality.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Increased insect herbivore performance under elevated CO2 is associated with lower plant defence signalling and minimal declines in nutritional quality.

Changes in insect herbivore performance under elevated atmosphere carbon dioxide concentrations e[CO2] are often driven by changes in the nutritional and defensive chemistry of their host plants. Studies addressing how the prolific pest cotton bollworm (Helicoverpa armigera) responds to e[CO2] show that performance usually declines, often associated with lower nutritional (e.g. nitrogen (N) concentrations) quality of host plants under e[CO2]. We investigated the impacts of e[CO2] on nutritional quality and anti-herbivore (jasmonate) defensive signalling in lucerne (Medicago sativa) when challenged by H. armigera. While foliar N decreased under e[CO2], other aspects of nutritional quality (soluble protein, amino acids, foliar C:N) were largely unaffected, potentially due to increased root nodulation under e[CO2]. In contrast, e[CO2] greatly reduced jasmonate signalling in M. sativa following H. armigera attack; jasmonic acid concentrations were ca. 56% lower in attacked plants grown under e[CO2]. Concurrent with this, relative growth rates of H. armigera were ca. 66% higher when feeding on e[CO2]-grown plants. In contrast with previous reports, which we meta-analytically summarise, we provide the first evidence that H. armigera performance can increase under e[CO2]. This may occur in plants, such as M. sativa, where e[CO2] has limited impacts on nutritional quality yet reduces jasmonate defence signalling.

Silicon Alters Leaf Surface Morphology and Suppresses Insect Herbivory in a Model Grass Species.

Grasses accumulate large amounts of silicon (Si) which is deposited in trichomes, specialised silica cells and cell walls. This may increase leaf toughness and reduce cell rupture, palatability and digestion. Few studies have measured leaf mechanical traits in response to Si, thus the effect of Si on herbivores can be difficult to disentangle from Si-induced changes in leaf surface morphology. We assessed the effects of Si on Brachypodium distachyon mechanical traits (specific leaf area (SLA), thickness, leaf dry matter content (LDMC), relative electrolyte leakage (REL)) and leaf surface morphology (macrohairs, prickle, silica and epidermal cells) and determined the effects of Si on the growth of two generalist insect herbivores (Helicoverpa armigera and Acheta domesticus). Si had no effect on leaf mechanical traits; however, Si changed leaf surface morphology: silica and prickle cells were on average 127% and 36% larger in Si supplemented plants, respectively. Prickle cell density was significantly reduced by Si, while macrohair density remained unchanged. Caterpillars were more negatively affected by Si compared to crickets, possibly due to the latter having a thicker and thus more protective gut lining. Our data show that Si acts as a direct defence against leaf-chewing insects by changing the morphology of specialised defence structures without altering leaf mechanical traits.

The Role of Silicon in Antiherbivore Phytohormonal Signalling.

The role of plant silicon (Si) in the alleviation of abiotic and biotic stress is now widely recognised and researched. Amongst the biotic stresses, Si is known to increase resistance to herbivores through biomechanical and chemical mechanisms, although the latter are indirect and remain poorly characterised. Chemical defences are principally regulated by several antiherbivore phytohormones. The jasmonic acid (JA) signalling pathway is particularly important and has been linked to Si supplementation, albeit with some contradictory findings. In this Perspectives article, we summarise existing knowledge of how Si affects JA in the context of herbivory and present a conceptual model for the interactions between Si and JA signalling in wounded plants. Further, we use novel information from the model grass Brachypodium distachyon to underpin aspects of this model. We show that Si reduces JA concentrations in plants subjected to chemical induction (methyl jasmonate) and herbivory (Helicoverpa armigera) by 34% and 32%, respectively. Moreover, +Si plants had 13% more leaf macrohairs than -Si plants. From this study and previous work, our model proposes that Si acts as a physical stimulus in the plant, which causes a small, transient increase in JA. When +Si plants are subsequently attacked by herbivores, they potentially show a faster induction of JA due to this priming. +Si plants that have already invested in biomechanical defences (e.g. macrohairs), however, have less utility for JA-induced defences and show lower levels of JA induction overall.

Simulated Herbivory: The Key to Disentangling Plant Defence Responses.

Plants are subjected to a multitude of stimuli during insect herbivory, resulting in a complex and cumulative defence response. Breaking down the components of herbivory into specific stimuli and identifying the mechanisms of defence associated with them has thus far been challenging. Advances in our understanding of responses to inconspicuous stimuli, such as those induced by microbial symbionts in herbivore secretions and mechanical stimulation caused by insects, have illuminated the intricacies of herbivory. Here, we provide a synthesis of the interacting impacts of herbivory on plants and the consequential complexities associated with uncoupling defence responses. We propose that simulated herbivory should be used to complement true herbivory to decipher the mechanisms of insect herbivore-induced plant defence responses.