Silencing the alarm: an insect salivary enzyme closes plant stomata and inhibits volatile release

Lin, Po An; Chen, Yintong; Chaverra-Rodríguez, Duverney; Heu, Chan C.; Zainuddin, Nursyafiqi Bin; Sidhu, Jagdeep Singh; Peiffer, Michelle; Tan, Ching Wen; Helms, Anjel M.; Kim, Dong-Hun; Ali, Jared G.; Rasgon, Jason L.; Lynch, Jonathan P.; Anderson, Charles T.; Felton, Gary W.

doi:10.1111/nph.17214

Cited by 47 publications

(58 citation statements)

References 50 publications

(75 reference statements)

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“…In contrast, two Athetis insects with low GOX activity can induce the highest amounts of volatiles. These results were consistent with other studies that GOX activity was negatively correlated with plant defence 55,56 …”

Section: Discussionsupporting

confidence: 94%

Differential Levels of Fatty Acid‐Amino Acid Conjugates in the Oral Secretions of Lepidopteran Larvae Account for the Different Profiles of Volatiles

Ling

Tian

et al. 2021

Pest Management Science

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BACKGROUND Plants have evolved sophisticated defense responses to insect herbivore attack, which often involve elicitors in the insects' oral secretions. The major eliciting compounds in insect oral secretions across different species and their potency in inducing volatile emissions have not yet been fully characterized and compared. RESULTS Seven lepidopteran insects with variable duration of association with maize were selected, five species known as pests for a long time (Ostrinia furnacalis, Spodoptera exigua, Spodoptera litura, Mythimna separata, and Helicoverpa armigera) and two newly emerging pests (Athetis lepigone and Athetis dissimilis). Oral secretions of the newly emerging pests have the highest total contents of Fatty Acid‐Amino Acid Conjugates (FACs), and their relative composition was well separated from that of the other five species in principal compound analysis. Redundancy analyses suggested that higher quantity of FACs was mainly responsible for the increases in maize volatiles, of which (E)‐3,8‐dimethyl‐1,4,7‐nonatriene (DMNT) and (E, E)‐4,8,12‐trimethyltrideca‐1,3,7,11‐tetraene (TMTT) were the most strongly inducible compounds. Adding FACs to the oral secretion of S. litura larvae significantly increased the emissions of TMTT and DMNT, confirming the key role of FACs in inducing volatile emissions in maize plants. Additional experiments with artificial diet spiked with linolenic acid suggested that variation in FACs is due to differences in internal FAC degradation and fatty acid excretion. CONCLUSION Compared with two newly emerging pests A. lepigone and A. dissimilis, the long‐term pests could diminish the volatile emission by maize through reducing the FAC content in their oral secretions, which may lower the risk of attracting natural enemies.

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Section: Discussionsupporting

confidence: 94%

Differential Levels of Fatty Acid‐Amino Acid Conjugates in the Oral Secretions of Lepidopteran Larvae Account for the Different Profiles of Volatiles

Ling

Tian

et al. 2021

Pest Management Science

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“…We tested if the day/night patterns of volatile emission were controlled by changes in stomatal resistance, which might influence the release of volatiles from plant tissues (Fig. 3 A, [ 32 , 33 ]). We used ABA treatments to increase the stomatal resistance of leaves of empty vector control (EV) and ir MPK4 plants, which, as previously described [ 34 ], have stomata that are largely in the open state and are not responsive to ABA treatments (Fig.…”

Section: Resultsmentioning

confidence: 99%

Light dominates the diurnal emissions of herbivore-induced volatiles in wild tobacco

Halitschke

Schuman

et al. 2021

BMC Plant Biol

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Background Timing is everything when it comes to the fitness outcome of a plant’s ecological interactions, and accurate timing is particularly relevant for interactions with herbivores or mutualists that are based on ephemeral emissions of volatile organic compounds. Previous studies of the wild tobacco N. attenuata have found associations between the diurnal timing of volatile emissions, and daytime predation of herbivores by their natural enemies. Results Here, we investigated the role of light in regulating two biosynthetic groups of volatiles, terpenoids and green leaf volatiles (GLVs), which dominate the herbivore-induced bouquet of N. attenuata. Light deprivation strongly suppressed terpenoid emissions while enhancing GLV emissions, albeit with a time lag. Silencing the expression of photoreceptor genes did not alter terpenoid emission rhythms, but silencing expression of the phytochrome gene, NaPhyB1, disordered the emission of the GLV (Z)-3-hexenyl acetate. External abscisic acid (ABA) treatments increased stomatal resistance, but did not truncate the emission of terpenoid volatiles (recovered in the headspace). However, ABA treatment enhanced GLV emissions and leaf internal pools (recovered from tissue), and reduced internal linalool pools. In contrast to the pattern of diurnal terpenoid emissions and nocturnal GLV emissions, transcripts of herbivore-induced plant volatile (HIPV) biosynthetic genes peaked during the day. The promotor regions of these genes were populated with various cis-acting regulatory elements involved in light-, stress-, phytohormone- and circadian regulation. Conclusions This research provides insights into the complexity of the mechanisms involved in the regulation of HIPV bouquets, a mechanistic complexity which rivals the functional complexity of HIPVs, which includes repelling herbivores, calling for body guards, and attracting pollinators.

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“…Notably, another generalist caterpillar species ( Helicoverpa zea ) suppresses HIPV production when feeding on tomato plants. An effector molecule, glucose oxidase (GOX), in the caterpillar saliva induces stomatal closure that limits the release of HIPVs (Lin et al 2021 ). Future research should characterize the presence and activity of effector molecules in saltmarsh caterpillar oral secretions to determine their role in modulating HIPVs and interplant communication (Felton and Tumlinson 2008 ; Acevedo et al 2019 ).…”

Section: Discussionmentioning

confidence: 99%

Defense Suppression through Interplant Communication Depends on the Attacking Herbivore Species

2021

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In response to herbivory, plants emit volatile compounds that play important roles in plant defense. Herbivore-induced plant volatiles (HIPVs) can deter herbivores, recruit natural enemies, and warn other plants of possible herbivore attack. Following HIPV detection, neighboring plants often respond by enhancing their anti-herbivore defenses, but a recent study found that herbivores can manipulate HIPV-interplant communication for their own benefit and suppress defenses in neighboring plants. Herbivores induce species-specific blends of HIPVs and how these different blends affect the specificity of plant defense responses remains unclear. Here we assessed how HIPVs from zucchini plants (Cucurbita pepo) challenged with different herbivore species affect resistance in neighboring plants. Volatile “emitter” plants were damaged by one of three herbivore species: saltmarsh caterpillars (Estigmene acrea), squash bugs (Anasa tristis), or striped cucumber beetles (Acalymma vittatum), or were left as undamaged controls. Neighboring “receiver” plants were exposed to HIPVs or control volatiles and then challenged by the associated herbivore species. As measures of plant resistance, we quantified herbivore feeding damage and defense-related phytohormones in receivers. We found that the three herbivore species induced different HIPV blends from squash plants. HIPVs induced by saltmarsh caterpillars suppressed defenses in receivers, leading to greater herbivory and lower defense induction compared to controls. In contrast, HIPVs induced by cucumber beetles and squash bugs did not affect plant resistance to subsequent herbivory in receivers. Our study shows that herbivore species identity affects volatile-mediated interplant communication in zucchini, revealing a new example of herbivore defense suppression through volatile cues.

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Silencing the alarm: an insect salivary enzyme closes plant stomata and inhibits volatile release

Cited by 47 publications

References 50 publications

Differential Levels of Fatty Acid‐Amino Acid Conjugates in the Oral Secretions of Lepidopteran Larvae Account for the Different Profiles of Volatiles

Differential Levels of Fatty Acid‐Amino Acid Conjugates in the Oral Secretions of Lepidopteran Larvae Account for the Different Profiles of Volatiles

Light dominates the diurnal emissions of herbivore-induced volatiles in wild tobacco

Defense Suppression through Interplant Communication Depends on the Attacking Herbivore Species

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