Research
We study the interactions between plants and herbivore insects. Five major research themes include (1) the physiology of plant antiherbivore defenses, (2) the ecology of plant-insect interactions, (3) the evolution of plant-insect interactions, (4) the influence of abiotic factors on plant-insect interactions, (5) agricultural/ecological application of plant-insect interactions. We welcome students and early-career scientists interested in insect herbivores and plants to join our lab.
Publications
Lin, P. A., Paudel, S., Lai, P. C., Gc, R. K., Yang, D. H. and Felton, G. W. 2023. Integrating water and insect pest management in agriculture. Journal of Pest Science. doi: 10.1007/s10340-023-01701-w
Jones A.C., Lin P. A., Peiffer M., Felton G. W. 2023 Caterpillar Salivary Glucose Oxidase Decreases Green Leaf Volatile Emission and Increases Terpene Emission from Maize. Journal of Chemical Ecology. doi:10.1007/s10886-023-01440-3.
Escobar-Bravo R.*, Lin P. A.*, Waterman J.M.*, Erb M. 2023 Dynamic environmental interactions shaped by vegetative plant volatiles. Natural Product Reports. doi:10.1039/d2np00061j. (* co-first author)
Lin P. A., Kansman J., Chuang W.P., Robert C., Erb M., Felton G.W. 2022 Water availability and plant-herbivore interactions. Journal of Experimental Botany. doi:10.1093/jxb/erac481.
Lin P. A., Paudel S, Zainuddin N. B., Tan C. W., Helms A, Ali J. G., Felton G. W. (2022). Low water availability enhances volatile-mediated direct defenses but disturbs indirect defenses against herbivores. Journal of Ecology. doi:https://doi.org/10.1111/1365-2745.13987
Lin, P. A., Chen, Y., Ponce, G., Acevedo, F. E., Lynch, J. P., Anderson, C. T., Ali, J. G., and Felton, G. W. (2021). Stomata-mediated interactions between plants, herbivores, and the environment. Trends in Plant Science. doi:https://doi.org/10.1016/j.tplants.2021.08.017
Lin, P. A., Chen, Y., Chaverra-Rodriguez, D., Heu, C. C., Zainuddin, N. B., Sidhu, J. S., Peiffer, M., Tan, C. W., Helms, A., Kim, D., Ali, J., Rasgon, J. L., Lynch, J. P., Anderson, C. T., Felton, G. W. 2021. Silencing the alarm: An insect salivary enzyme closes plant stomata and inhibits volatile release. New Phytologist. doi: 10.1111/nph.17214
Lin, P. A., Liu, C. M., Ou, J. A., Sun, C. H., Chuang, W. P., Ho, C. K., Kinoshita, N., Felton, G. 2021. Changes in arthropod community but not plant quality benefit a specialist herbivore on plants under reduced water availability. Oecologia. doi: 10.1007/s00442-020-04845-z
Lin, P. A., Felton, G. W. 2020. Oral cues are not enough: induction of defensive proteins in Nicotiana tabacum upon feeding by caterpillars. Planta, 251(4). doi:10.1007/s00425-020-03385-3
Lin, P. A., Peiffer, M., Felton, G. W. 2020. Induction of defensive proteins in Solanaceae by salivary glucose oxidase of Helicoverpa zea caterpillars and consequences for larval performance. Arthropod-Plant Interactions, 14(3), 317-325. doi:10.1007/s11829-020-09751-y
Lin, P. A., Paudel, S., Afzal, A., Shedd, N. L., & Felton, G. W. (2020). Changes in tolerance and resistance of a plant to insect herbivores under variable water availability. Environmental and Experimental Botany, 104334. doi:10.1016/j.envexpbot.2020.104334
Paudel, S., Lin, P. A., Hoover, K., Felton, G. W., & Rajotte, E. G. (2020). Asymmetric responses to climate change: temperature differentially alters herbivore salivary elicitor and host plant responses to herbivory. Journal of Chemical Ecology. doi:10.1007/s10886-020-01201-6
Tsai, C. L., Chu, I. H., Chou, M.-H., Chareonviriyaphap, T., Chiang, M. Y., Lin, P. A., Lu, K. H., Yeh, W. B. (2020). Rapid identification of the invasive fall armyworm Spodoptera frugiperda (Lepidoptera, Noctuidae) using species-specific primers in multiplex PCR. Scientific Reports, 10(1). doi:10.1038/s41598-020-73786-7
Paudel, S., Lin, P. A., Foolad, M. R., Ali, J. G., Rajotte, E. G., & Felton, G. W. (2019). Induced plant defenses against herbivory in cultivated and wild tomato. Journal of Chemical Ecology, 45(8), 693-707. doi:10.1007/s10886-019-01090-4
1. Drought-Plant-Insect Interactions
1.1 Impact of Drought on Antiherbivore Defense Strategies of Plants
Abstract
Water availability is an important factor that influences plant-insect interactions. While the influence of water limitation on plant resistance traits has received much attention, how water availability affects plant tolerance to herbivory is rarely tested. Here we show that lower water availability reduced tolerance capacity of tomato plants as measured by above ground regrowth and flower development after herbivory. In contrast to a reduced ability to tolerate herbivory, lower water availability increased the constitutive and induced levels of two defensive proteins, trypsin protease inhibitor and polyphenol oxidase, indicative of an increased investment on resistance under water limitation. The increase in defense proteins was paralleled with lower performance of a specialist caterpillar, Manduca sexta, and lower consumption of plant tissues. Although the performance of generalist, Helicoverpa zea, was unaffected by water availability, we observed a high mortality of H. zea that suggests strong resistance of tomato against H. zea. The findings revealed an unexpected case where water limitation decreases tolerance but increases resistance of a plant, suggesting a potential tradeoff between these strategies. This plasticity may benefit herbaceous plants by balancing growth and defense under variable water availability.
1.2 Impact of Drought on Species Interactions
Caterpillars face more predators as well as competitors on plants that are growing under high soil water availability compared to plants that are growing under water limitation. Caterpillars of cabbage white butterfly (Pieris rapae) attacked by predatory ants (Monomorium chinense) on their host plant (Rorippa indica) in Taiwan.
Abstract
Plants grow under reduced water availability can have divergent effects on insect herbivores, in some instances producing benefits to them. However, the forces mediating these positive impacts remain mostly unclear. We conducted a manipulative field study using a specialist herbivore Pieris rapae, and its host plant, Rorippa indica, in two populations to identify how water availability impacts overall plant quality and multitrophic interactions. We observed that R. indica growing under low water availability led to higher survival of P. rapae larvae. The increase in survival of eggs and larvae was related to the reduced abundance of other herbivores and natural enemies. Water availability had differential impacts on members of the herbivore community through changes in plant quality. Low water availability decreased the quality of R. indica to most herbivores as indicated by reduced abundance in the field and decreased relative growth rate in feeding assays. In contrast, the performance of P. rapae larvae were not affected by differences in sympatric R. indica grown under different water availability. These results indicate that local P. rapae possess some physiological adaptation to overcome fluctuations in host quality. Our findings illustrate that reduced water availability is beneficial to a specialist herbivore, but detrimental to most other herbivores. Our work highlights the complex roles of the arthropod communities associated with plants in determining the impacts of water availability on insect herbivores.
1.3 Drought-Like Responses of Plants Induced by Herbivores
Abstract
Herbivore-induced plant volatiles (HIPVs) are widely recognized as an ecologically important defensive response of plants against herbivory. Although the induction of this “cry for help” has been well-documented, only a few studies has investigated the inhibition of HIPVs by herbivores, and little is known about whether herbivores have evolved mechanisms to inhibit the release of HIPVs. To examine the role of herbivore effectors in modulating HIPVs and stomatal dynamics, we conducted series of experiments combining pharmacological, surgical, genetic (CRISPR-Cas9) and chemical (GC-MS analysis) approaches. We show that the salivary enzyme, glucose oxidase (GOX), secreted by the caterpillar Helicoverpa zea on leaves, causes stomatal closure in tomato (Solanum lycopersicum) within 5 min, and in both tomato and soybean (Glycine max) for at least 48 h. GOX also inhibits the emission of several HIPVs during feeding by H. zea, including (Z)-3-hexenol, (Z)-jasmone, and (Z)-3-hexenyl acetate, which are important airborne signals in plant defenses. Our findings highlight a potential adaptive strategy where an insect herbivore inhibits plant airborne defenses during feeding by exploiting the association between stomatal dynamics and HIPV emission.
(https://doi.org/10.1111/nph.17214)
1.4 Drought influences on plant volatile defenses
Abstract
1. Interactions between plants and natural enemies of insect herbivores influence plant productivity and survival by reducing herbivory. Plants attract natural enemies via herbivore-induced plant volatiles (HIPVs), but how water availability (WA) influences HIPV-mediated defenses is unclear.
2. We use tomato (Solanum lycopersicum), tomato fruitworm (Helicoverpa zea), and two natural enemies, the parasitoid wasp (Microplitis croceipes) and the predator spined soldier bug (Podisus maculiventris), to investigate the effect of WA on HIPV emission dynamics and associated plant defense.
3. We show that low WA initially increases total HIPV emission by tomato on the first day of herbivore exposure and, in contrast, reduces HIPV emission on the second day. Low WA enhances HIPVs that are mostly found in tomato trichomes. Notably, some volatiles inhibited by low WA are known attractants of natural enemies. Evidence from Y-tube and in-cage behavioral assays indicates that changes in HIPV emissions by low WA compromise the ability of tomato plants to attract natural enemies.
4. Synthesis: Based on our results, we propose a hypothesis where plants respond to low WA by enhancing repellent HIPV emissions and reducing the emission of HIPVs that attract natural enemies, which disrupts natural enemy-mediated plant indirect defenses, but enhances plant direct defense against herbivores.
2. Plant Defense and Insect Feeding Behavior
2.1 Semi-Circle Feeding Behavior and its Role in Plant Defense Induction
Abstract
Many leaf-feeding caterpillars share similar feeding behaviors involving repeated removal of previously wounded leaf tissue (semicircle feeding pattern). We hypothesized that this behavior is a strategy to attenuate plant-induced defenses by removing both the oral cues and tissues that detect it. Using tobacco (Nicotiana tabacum) and the tobacco hornworm (Manduca sexta), we found that tobacco increased defensive responses during herbivory compared to mechanical wounding at moderate damage levels (30%). However, tobacco did not differentiate between mechanical wounding and herbivory when the level of leaf tissue loss was either small (4%) or severe (100%, whole leaf removal). Higher amounts of oral cues did not induce higher defenses when damage was small. Severe damage led to the highest level of systemic defense proteins compared to other levels of leaf tissue loss with or without oral cues. In conclusion, we did not find clear evidence that semicircle feeding behavior compromises plant defense induction. In addition, the level of leaf tissue loss and oral cues interact to determine the level of induced defensive responses in tobacco. Although oral cues play an important role in inducing defensive proteins, the level of induction depends more on the level of leaf tissue loss in tobacco. (https://doi.org/10.1007/s00425-020-03385-3)
3. Light and Plant-Insect Interactions
3.1 The Salient Aroma Hypothesis
Abstract
Host plant specialization by moths and butterflies has been a primary research focus in the field of coevolution and ecological specialization. However, factors underlying the evolution of host specificity remain largely unclear despite decades of research. Here, we demonstrate that host plant specialization is closely linked to diurnality in the Lepidoptera: diurnal butterflies and moths tend to specialize in their range of host choices, whereas nocturnal moths tend to be relative generalists. We further show that plants, on average, release larger amounts of volatile organic compounds (VOC) during the day than at night. Given that plant VOCs are important chemical cues for host searching in herbivores, we propose the ‘Salient Aroma Hypothesis (SAH)’. Under SAH, herbivores that are active during the period when plant VOCs are more available are better able to discriminate between potential host species and therefore have more specialized diet breadth. Conversely, those active at night, when VOCs are not released as much, are more likely to have wider diet breadth. Antennae are the primary organs used to perceive VOCs. Differences in their morphologies also support predictions from the SAH: Diurnal females have larger antennae relative to their body sizes than nocturnal females. Our study underscores the importance of plant VOCs in Lepidoptera evolution, suggesting a possible evolutionary pathway for host specialization in herbivorous insects.