Journal Search Engine

Download PDF Export Citation Korean Bibliography
ISSN : 1225-0171(Print)
ISSN : 2287-545X(Online)
Korean Journal of Applied Entomology Vol.61 No.1(Special Issue) pp.143-154

Biochemical Adaptation of the Oriental Tobacco Budworm, Helicoverpa assulta, to Host-plant Defensive Compounds

Seung-Joon Ahn*
Department of Biochemistry, Molecular Biology, Entomology & Plant Pathology, Mississippi State University, Mississippi State, MS 39762, USA
January 29, 2022 February 9, 2022 February 14, 2022


Plant secondary metabolites play an important role in insect-plant interactions. Herbivorous insects have various strategies to cope with the plant defensive compounds. Polyphagous insects feed on a wide variety of plant species, and their detoxification mechanisms are more complex since they tend to respond to a large array of different plant-derived chemicals. Alternatively, oligophagous insects specialize on only a few related plant species and may be expected to have a more efficient form of adaptation. This adaptation could involve either the production of large quantities of enzymes to detoxify their defensive compounds or the sequestration of the compounds or their metabolites. The oriental tobacco budworm, Helicoverpa assulta, is a specialist herbivore, feeding on a few plants of Solanaceae, such as tobacco and hot pepper. Understanding its host-plant adaptation not provides an important insight on physiology, ecology and evolution of specialist herbivores, but also gives a clue to develop management strategies of the pest species such as H. assulta. This paper briefly reviews the specialist, H. assulta, focusing on its host range, larval associations with the host plants, and detoxification mechanisms to nicotine and capsaicin, two characteristic defensive compounds derived from its two major host plants, tobacco and hot pepper, respectively. It summarizes the relevant research over the last half century and provides a future perspective on this subject.

기주식물 방어물질에 대한 담배나방의 생화학적 적응

안 승준*
미국 미시시피주립대학교


식물의 이차대사산물은 곤충-식물 상호관계에서 중요한 역할을 한다. 식식성 곤충은 식물의 방어물질에 대처하는 다양한 전략을 가지고 있 다. 광식성 곤충은 넓은 범위의 다양한 식물들을 섭식하고 그 해독 기작도 보다 복잡한데, 이는 많은 종류의 식물유래 화합물에 반응하는 경향이 있 기 때문으로 보인다. 이와는 달리 협식성 곤충은 몇몇 유사한 식물에 국한되어 살아가며 보다 효율적인 적응 방식을 지니고 있을 것으로 여겨진다. 이러한 협식성 곤충의 적응은 식물의 방어물질에 대한 해독효소를 다량 생산하거나 방어물질 또는 그 대사산물을 격리하는 전략을 마련하였기 때문 으로 보인다. 담배나방은 담배와 고추 등 주로 가지과의 몇몇 식물만을 가해하는 협식성 곤충이다. 담배나방의 기주식물 적응성을 이해한다면, 이 해충에 의한 작물의 피해를 줄이는 방법을 개발하는데 도움을 줄 수 있을 뿐만 아니라, 담배나방과 같은 협식성 곤충의 생리, 생태, 진화를 연구하는 데에도 중요한 단서를 제공할 것이다. 본 종설에서는 담배나방의 기주식물 범위, 유충과 기주식물의 상호작용, 그리고 기주식물에서 특이적으로 나 오는 니코틴과 캡사이신에 대한 곤충의 반응과 해독 메카니즘을 중심으로, 지난 반세기 동안의 연구결과를 요약하고 앞으로의 전망을 제시하고자 한다.

    Plant secondary metabolites play an important role in insectplant interactions. Many of these metabolites are detrimental or toxic to herbivorous insects, therefore having defensive properties. These allelochemicals can have multiple effects on herbivores, influencing behavior as well as physiology. They can deter feeding by non-specialists or stimulate feeding by specialists which associate the chemicals with an exploitable food source. Once they are consumed, allelochemicals may influence the postingestive utilization of nutrients through various physiological and biochemical mechanisms. After being absorbed, many allelochemicals exert deleterious effects through a variety of pharmacological modes of action (Schoonhoven et al., 2005;Slansky, 1990).

    Insects feeding on the plants containing such noxious compounds, however, have strategies to cope with the plant’s defense. Therefore, the plant secondary compounds act as a driving force for specialization of herbivores on their host plants through an “evolutionary arms race” (Ehrlich and Raven, 1964). Insect herbivores confronted with a variety of noxious chemicals from the plants they consume have evolved various counter defense mechanisms to cope with their harmful effects. Among those are (1) to avoid continuous contact, (2) to excrete the unwanted compounds rapidly, (3) to modify them enzymatically, (4) to sequester them for further utilization, or (5) to develop target-site insensitivity (Brattsten, 1988;Després et al., 2007;Schoonhoven et al., 2005).

    Generalist insect herbivores feed on a wide variety of plant species, and their adaptive mechanisms are more complex than specialists since polyphagous insects tend to respond to a large array of different plant chemicals and proteins. In contrast, specialist insect herbivores specialize on only a few related plant species and might be expected to have a more efficient form of adaptation. This adaptation could involve either the production of large quantities of enzymes to detoxify their defensive compounds or the sequestration of the compounds or their metabolites (Ali and Agrawal, 2012). Most herbivorous insects feed on only one or a few genera or on a single plant family or subfamily (specialists), whereas only less than 10% of all herbivores can feed on plants in more than three different plant families (generalists) (Bernays and Graham, 1988).

    The oriental tobacco budworm, Helicoverpa assulta (Guenée) (Lepidoptera: Noctuidae) (Fig. 1), is a specialist herbivore feeding on a few plants of Solanaceae such as tobacco, hot pepper, and some Physalis species (Mitter et al., 1993). This species is widely distributed in Old World including Africa, Asia, Australasia, and the Pacific Islands (CAB International, 2020;Cunningham and Zalucki, 2014). In Korea, H. assulta has been recognized as one of the most serious pests in hot pepper and tobacco since the 1950s (An, 1976;Choi et al., 1975;Hwang et al., 1987). These early studies were mainly focused on the damage surveys and ecological characterizations of H. assulta. Between 1980 and 2010, Boo and colleagues had devoted to the H. assulta research from a wide variety of aspects, including morphology (Koh et al., 1995;Park and Boo, 1988), behavior (Cho and Boo, 1988), physiology and biochemistry (Ahn et al., 2002;Boo et al., 1990;Cho and Boo, 1990;Choi et al., 2002, 1998a, 1998b;Jung and Boo, 1992;Lee et al., 2006), pheromones and kairomones (Boo et al., 1995;Boo and Yang, 1998, 2000;Cork et al., 1992;Park et al., 2002, 1996, 1994), and plant interactions (Choi and Boo, 1989a, 1989b;Lee and Boo, 1993a, 1993b). In China, several research groups have been investigating this species since around 2000, producing a great number of noticeable publications especially by comparative studies with a congeneric generalist, Helicoverpa armigera (Cheng et al., 2017;Liu et al., 2014;Ming et al., 2007;Sun et al., 2012;Tang et al., 2006;Wang and Dong, 2001;Wang et al., 2005, 2017;Xu et al., 2016;Yang et al., 2017;Zhang et al., 2010;Zhou et al., 2022).

    Studies on H. assulta have been accumulated over the last half century, and its multifaceted interactions with host plants as a specialist herbivore would imply a great potential to basic and applied research in the future. This paper briefly reviews the specialist, H. assulta, focusing on its host range, larval associations with host plants, detoxification mechanisms to nicotine and capsaicin, and suppression of plant defense by herbivory, followed by a future perspective on the study of H. assulta.

    Host-plant Range

    The oriental tobacco budworm primarily feeds on a few plants of Solanaceae such as tobacco, hot pepper, Physalis, and Datura ( w ild h ost) ( Jadhav and Armes, 1 996). It was o nce recorded that H. assulta feeds five different plant families in Australia. This includes onion (Amaryllidaceae) (Matthews, 1999) and potato (Solanaceae) which have been reported as an occasional host in India, but no further reports on onion and potato have been released, indicating that they had probably been confused with a similar generalist, H. armigera (Jadhav and Armes, 1996). Tomato was also listed as a host plant of H. assulta, but the field survey and laboratory experiments showed that the tomato fruit appears the least favorable food when provided together with tobacco leaves and pepper fruits (Zhang et al., 2006). In a no-choice experiment, all the 3rd instar larvae died on the green tomato fruits before reaching to the final instar stage, probably because tomatine, a steroidal glycoalkaloid found in tomato, is toxic to H. assulta by reducing its diet ingestion (Wu et al., 2006;Xu and Qin, 1987) or eliciting aversive feeding behaviors (Sun et al., 2021). However, when tested with adults, tomato was the most favorite plant for oviposition of H. assulta, followed by tobacco and pepper (Zhang et al., 2006). Cape gooseberry (Physalis spp.) was described as a host plant seriously damaged by the H. assulta larvae in Australia (Kirkpatrick, 1961), but no further reports have been found. Devil’s trumpet (Datura spp.) was known as a wild host in India (Jadhav and Armes, 1996) and a recent study with a Datura species reported that the H. assulta larvae grow on D. stramonium as preferably as on tobacco, whereas the oviposition was not preferred on the plant surface of D. stramonium (Lim et al., 2016). Altogether, it seems that the host plants of H. assulta thus far known are tobacco, hot pepper, Physalis and Datura, whereas onion, potato, and tomato are not preferrable plants at least during their larval stage.

    On the other hand, a congeneric generalist, H. armigera, feeds on more than 60 crops including cotton, maize, sorghum, tomato, lucerne, tobacco and cowpea, across 47 plant families (Fitt, 1989;Jallow et al., 2004;Zalucki et al., 1986). Although the two closely-related species, H. armigera and H. assulta, occur in the same geographical area, they share only a few host plants, such as tobacco and produce the opposite ratios of their pheromone blends, leading to their premating isolation (Ming et al., 2007).

    Host-plant Association

    Like other specialist herbivorous insects, H. assulta is highly associated with its host plants throughout its life cycle. Female moths are more likely to lay eggs on the upper surface of hot pepper leaves or the under surface of tobacco leaves (Han et al., 1994). After hatching, the second instar larvae burrow inside the hot pepper fruits or nibble the tobacco buds. In hot pepper, the larvae spend most of the period inside the fruits, consuming nearly all the internal tissues before moving on to other fruits. They continue this process up until the moment they become 5th or sometimes 6th instar larval stage, depending on food availability, where they will burrow under the soil for pupation (Han et al., 1993). Adults usually emerge within 3 hours after sunset and copulate within 2 days after emergence. The calling and copulation behaviors usually happen between 2-6 hours after sunset (Cho and Boo, 1988), which is consistent with the diel rhythm of pheromone production in females (Choi et al., 1998b;Kamimura and Tatsuki, 1993, 1994). The calling behaviors increase when females are placed with host plants (Ahn, S.-J., unpublished observation). The peak time for oviposition is about 3 days after copulation (Cho and Boo, 1988). The number of eggs laid varies from 200 to 600 per female depending on environmental factors and host plants (Chung and Hyun, 1980;Lim et al., 2016;Wang et al., 2008).

    From a three-year field monitoring using pheromone traps in Korea, Yang et al. (2004) found that H. assulta occurs about 4 times a year from late May until early October with the highest peak starting from late August to early September in hot pepper fields. During the high season, the larvae prefer to feed on green fruits rather than red ones, causing serious yield losses directly from larvae feeding on the developing fruits.

    Biochemical Adaptation to Host-plant Defensive Compounds

    Plants defend themselves from insects with a vast array of toxic compounds, whereas insects have evolved several counter-defense mechanisms, namely behavioral, physiological, and biochemical resistance mechanisms (Brattsten, 1988). Herbivorous insects possess a variety of detoxification enzymes that allow them to deal with host toxic compounds (Heckel, 2018). Enzymatic detoxification of ingested plant allelochemicals is one of the important mechanisms by which insects can neutralize, degrade, or modify a variety of xenobiotics including plant allelochemicals (Brattsten, 1992). The most extensively studied group of detoxication enzymes is cytochrome P450s (P450s), which enables insects to convert the toxic compounds into more reactive ones by different reactions including oxidation, carbon hydroxylations, N- and O-dealkylations, or epoxidations (Feyereisen, 2012). The metabolites can be further processed by conjugating enzymes, such as glutathione S-transferases (GSTs) (Ketterman et al., 2011) or UDP-glycosyltransferases (UGTs) (Ahn et al., 2012).

    This section reviews the effects of two major host plants, tobacco and hot pepper, and their characteristic defensive compounds, nicotine and capsaicin, respectively, on the larval performance of H. assulta, and also describes the counterdefense mechanisms of H. assulta against each of them.

    Tobacco and nicotine

    A study showed that the newly hatched larvae prefer tobacco leaves rather than hot pepper or tomato (Zhang et al., 2006), but another study demonstrated some negative effects of tobacco on the larval growth and survival, and the pupal weight when compared with those reared in pepper (Capsicum frutescens) or artificial diet (Wang et al., 2008). When compared with a non-host plant (common bean), the larval growth was better in tobacco as expected, but its survivorship reached only up to 50% at day 12 after hatching (Lim et al., 2016). These contrary results indicate that tobacco, to some extent, is detrimental to H. assulta, although it is known as one of the favorite host plants. It means that the larvae struggle against the plant defensive components, such as nicotine, to adapt to tobacco just a bit more than other non-adapted herbivores. Lee and Boo (1993a) found that dietary nicotine is relatively less toxic to H. assulta when compared with another non-adapted herbivore, Spodoptera exigua. One of the earliest studies showed that nicotine has a phagostimulant effect on the H. assulta larvae (Xu and Qin, 1987).

    Nicotine is a pyridine alkaloid primarily found in the Solanaceae, especially in tobacco plants (Nicotiana spp.), which effectively reduces the herbivore’s growth by affecting the central nervous system of insects and acting as an agonist of the post-synaptic nicotinic acetylcholine receptors (Tomizawa and Casida, 2005). Nicotine toxicity to insects had been investigated early in modern history (McIndoo, 1916), but its metabolic detoxification by insects has been unveiled relatively recently. P450-catalyzed oxidative metabolism of nicotine to its common metabolites such as cotinine, and the N-oxides of nicotine and cotinine have been found in a tobacco specialist Manduca sexta from North America (Snyder et al., 1994). A recent study has proposed that the nicotine tolerance is also achieved by excretion of unmetabolized nicotine (Kumar et al., 2014). For another tobacco specialist, H. assulta from Old World, only a few have been known for its biochemical or metabolic detoxification of nicotine.

    It was suggested that the nicotine tolerance of H. assulta is probably associated with an elevated induction of midgut P450 enzymes in H. assulta larvae reared on tobacco leaves and an efficient excretion of nicotine in H. assulta compared to S. exigua (Lee and Boo, 1993a, 1993b). Another study showed that the dietary nicotine more strongly induces the midgut GST activity in H. assulta than H. armigera (Dong et al., 2002). According to an electrophysiological study on the maxillary sensilla styloconica, which represents almost 70% of the total number of larval sensilla on the mouthparts (Park and Boo, 1988), nicotine does less likely inhibit the sugar-evoking stimulation on the lateral sensillum styloconicum in H. assulta than H. armigera (Tang et al., 2000). Recently, Sun et al. (2021) compared behaviors and electrophysiological responses of both species to gossypol, tomatine, nicotine and capsaicin, showing that nicotine as well as capsaicin drives appetitive feeding behaviors on the specialist and elicits different responses of the single sensillum recordings (SSR) on the maxillary sensilla styloconica of larvae, of which patterns are consistent with the difference of feeding preferences to these compounds (Sun et al., 2021). These studies suggest that the nicotine-associated host adaptation might happen not only by metabolic detoxification, but also in a sensory level of the H. assulta larvae.

    Hot pepper and capsaicin

    Capsaicin (8-methyl-N-vanillyl-6-nonenamide) is the predominant form among more than ten capsaicinoids found in Capsicum fruits (Mazourek et al., 2009). Capsaicin is responsible for the burning sensation experienced by mammals via transient receptor potential vanilloid subtype 1, TRPV1 (Caterina et al., 1997), but not sensed by avian animals due to their insensitive receptor orthologs (Jordt and Julius, 2002;Tewksbury and Nabhan, 2001). In insects, capsaicin is known to deter oviposition in the onion fly (Cowles et al., 1989), inhibit feeding in the ladybird beetle (Hori et al., 2011), and impede larval growth in the spiny bollworm (Weissenberg et al., 1986). Capsicum extracts also have larvicidal activities against two mosquitoes species (Madhumathy et al., 2007). When treated with an organophosphate, capsaicin showed a synergistic insecticidal effect against Colorado potato beetle (Maliszewska and Tȩgowska, 2012).

    As H. assulta larvae preferably feed on Capsicum fruits (Choi and Boo, 1989a), it is a reasonable inference that the larvae might have a defense mechanism to cope with the signature compound, capsaicin, from the hot pepper fruit. Ahn et al. (2011a) systematically compared the capsaicin toxicity among six Noctuidae species, including H. assulta, H. armigera, H. zea, Heliothis virescens, Heliothis subflexa, and Spodoptera frugiperda, by measuring their larval development, survival rate, food consumption, and utilization using capsaicinspiked artificial diet. The study showed that the host-plant specialist H. assulta has a greater tolerance to capsaicin than the other insects tested. Interestingly, the larval growth of H. assulta was even enhanced to some extent in the capsaicinsupplemented diet with a low dosage, indicating that H. assulta probably has a mechanism to utilize capsaicin for a feeding stimulus or metabolic benefit (Ahn et al., 2011a). The three Helicoverpa species were further challenged by injecting a series of higher doses of capsaicin into their larval hemolymph to bypass the gut for acute toxicity. It demonstrated that capsaicin is less toxic to H. assulta when it is present in the circulatory system, which is a similar result with the feeding experiments (Ahn et al., 2011a). Taken together, it seems that H. assulta can cope with capsaicin not just by detoxification, but also by utilization for its own benefit, probably explaining its successful feeding on hot pepper fruits in the field.

    Zhu et al. (2020) traced the metabolites of capsaicin and dihydrocapsaicin (the second major form of capsaicinoids) after in vitro enzymatic reactions with the crude extracts from fat body, midgut and Malpighian tubules from H. assulta. The study identified five metabolites and their chemical structures by LC-MS/MS. This study proposed that both capsaicin and dihydrocapsaicin are transformed by macrocylization, alkyl hydroxylation, alkyl dehydrogenation, or dimerization. The same metabolites were detected in H. armigera without any species-specific metabolites formed in H. assulta. However, it is noteworthy that the specialist H. assulta exhibited an overall greater capacity to metabolize the capsaicinoids compared to the generalist H. armigera and the midgut was the most significant contributor to this metabolism (Zhu et al., 2020). It was proposed earlier that such metabolites are produced via P450- catalyzed biotransformations in H. armigera, where four P450 enzymes, CYP6B6, CYP9A12, CYP9A14 and CYP9A17, are involved (Tian et al., 2019), suggesting that orthologous enzymes are most likely to be involved in H. assulta as well, but not tested yet.

    Ahn et al. (2011b) examined a metabolic fate of capsaicin in three Helicoverpa species, H. assulta, H. armigera, and H. zea, after feeding on capsaicin-laced diet. It exhibited that unmetabolized capsaicin is excreted into feces at a greater rate in two generalists, H. armigera (32%) and H. zea (39%), but only at a smaller rate in the specialist H. assulta (5%). The same study identified a glucose conjugate of capsaicin excreted in the feces of three Helicoverpa species as a metabolite, but the glucosylation efficacy was higher in the two generalists H. armi gera (7%) and H. zea (8%) than in the specialist H. assulta (2%). It demonstrates that H. assulta does not take a strategy to quickly excrete capsaicin as a form of either an intact capsaicin or a glucoside. This suggests that the specialist might have an alternative pathway for dealing with capsaicin, such as metabolic conversion and/or sequestration, but more studies are required for this to be confirmed (Ahn et al., 2011b). Enzymatic experiments on the capsaicin glucosylation among different tissues showed that fat body has the highest activity in the three species, indicating that the capsaicin glucosylation most likely happens after capsaicin passes the gut into the hemolymph. The enzymes responsible for the capsaicin glucosylation are not yet known.

    The electrophysiological study, like shown in the nicotine section above, demonstrated that capsaicin is less likely to inhibit the sugar-evoking stimulation on the lateral sensillum styloconicum in H. assulta than H. armigera (Tang et al., 2000). Recently, Sun et al. (2021) compared the behavioral and electrophysiological responses of both species to gossypol, tomatine, nicotine and capsaicin, showing that capsaicin as well as nicotine triggers appetitive feeding behaviors on the specialist and induces different SSR responses on the maxillary sensilla styloconica of larvae, of which patterns are consistent with the difference of feeding preferences to these compounds (Sun et al., 2021). These studies suggest that the capsaicinassociated host adaptation might happen, not only by metabolic detoxification, but might also occur in a sensory level of the H. assulta larvae.

    Other defensive compounds

    Choi and Boo (1989b) examined the larval development of H. assulta on the tobacco leaves sprayed with different extracts of several wild plants and showed that each extract from Rhamnus davurica (Rhamnaceae), Persicaria hydropiper (Polygonaceae), Forsythia koreana (Oleaceae), Trifolium repens (Fabaceae), Styrax japonicus (Styracaceae), Ginkgo biloba (Ginkgoaceae), and Vitis amurensis (Vitaceae) causes larval death due to antifeeding effects on the first and second instar larvae. Tannic acid, when provided in artificial diet, reduced the larval growth and lowered the food digestibility in H. assulta (Xu and Qin, 1987). The midgut proteases were inhibited by dietary tannic acid as well as protease inhibitors (Xu and Qin, 1994). Strychnine, a terpene indole alkaloid found in the seeds of the Strychnos nux-vomica tree, strongly deterred the feeding behavior of H. assulta larvae, but the larvae displayed habituation to strychnine after a shorter time (48 hr) than the generalist H. armigera (72 hr) (Zhou et al., 2022). Electrophysiological tests revealed that a deterrent-sensitive neuron in the medial sensillum styloconicum of both species displayed significantly reduced sensitivity to strychnine that correlated with the onset of habituation (Zhou et al., 2022). Gossypol and tomatine elicited aversive feeding behaviors as well as electrophysiological responses in H. assulta larvae, which are mediated via gustatory receptor neuros (Sun et al., 2021).

    Suppression of Plant Defense by Herbivory

    Glucose oxidase (GOX) is the principal salivary enzyme in H. zea (Eichenseer et al., 1999), and is responsible for suppression of the nicotine production in host plant (Musser et al., 2002). In H. armigera or H. assulta, lower levels of nicotine were induced in the damaged leaves by larval feeding than by mechanical wounding, and the GOX activity from the salivary glands plays an important role in suppressing the nicotine production in the plants (Zong and Wang, 2004). Interestingly, the salivary GOX activity was significantly higher in H. armigera than H. assulta (Zong and Wang, 2004), and two enzymes responsible for the plant's oxidative responses, polyphenoloxidase (PPO) and peroxidase (POD), were differently induced between the two species (Zong and Wang, 2007). These results demonstrate that the specialist H. assulta might be more tolerant to nicotine or at least have different counter-adaptation mechanisms compared to the generalist H. armigera. A survey of the salivary GOX activities in 85 lepidopteran species across 23 different families showed a significant correlation between polyphagy and high levels of GOX, compared to the species with a more limited host range, suggesting that generalists have higher GOX activities than specialists (Eichenseer et al., 2010). Another comparative study also showed that GOX activities are consistently higher in the generalist (H. armigera) than the specialist (H. assulta) throughout all the time points of the final instar larvae, and all the treatments of host plants, protein-carbohydrate ratios and 11 allelochemical challenges including nicotine and capsaicin (Yang et al., 2017). However, the expression levels of GOX transcripts were not as high as the corresponding enzyme activities and the transcript levels were even lower in H. armigera in some cases (different allelochemicals and different P:C ratio), indicating that the greater GOX activity in generalist herbivores is not achieved only by greater transcription rate, but by higher transcript stability, greater translation rate, better enzyme stability and/or their combinations (Yang et al., 2017).

    Fatty acid-amino acid conjugates (FACs) from larval secretions play a beneficial role in nitrogen assimilation of lepidopteran herbivores (Yoshinaga et al., 2008), whereas they provide detrimental effects on herbivores by eliciting direct and indirect defenses in plants (Bonaventure et al., 2011). It is critical for the FAC-producing insect herbivores to regulate the amount of FACs. The FAC hydrolysis enzyme has been identified as Lepidopteran aminoacylase 1 in both H. assulta and H. armigera with different regulatory regimes in different diets, suggesting that FACs are utilized mainly for removal of excessive nitrogen in generalists, while for nitrogen assimilation in specialists (Cheng et al., 2017).

    Conclusion and Perspectives

    This review has mainly focused on two major host plants, tobacco and hot pepper and their characteristic allelochemicals, nicotine and capsaicin, respectively. The detoxification mechanisms of H. assulta described above are not crystal clear yet, but more investigations are required to understand in detail especially from biochemical and molecular perspectives. Not only by metabolic detoxification, however, there could be many other factors affecting the performances of H. assulta, for instance primary nutritional substances and other secondary compounds from the host plants. Also, the capability of digestion, assimilation and other corresponding digestive enzymes could contribute to its overall performance. Host selection by adults mostly for oviposition could be another important biotic factor. On the other hand, abiotic factors include temperature, humidity, photoperiod, seasons, and geographical locality, affecting its development, survival and fecundity in its host plants (Han et al., 1993;Kamimura and Tatsuki, 1994;Lee and Han, 1998;Xie et al., 1998). Further research on the physiology and biochemistry of H. assulta feeding on different host plants will no doubt be informative in this regard. Over the last five decades, we have come to understand, to some extent, how different diets or host plants affect the larval growth rates, mortality, and adult fecundity and survival in H. assulta, but the biochemical and molecular mechanisms remain largely unknown and deserve further research.

    Both tobacco and hot pepper are native to Central America, and they were introduced to East Asia at around the 15th century, whereas H. assulta seems to have been indigenous in Old World before these two new crops were introduced. Over the last 500 years or so, H. assulta has successfully dominated these newly introduced plants. In general, introduced plants acquire herbivorous insects from the local fauna and the recruitment takes about 500 - 10,000 years for specialists, while about 100 years for generalists (Bernays and Graham, 1988). It suggests the notion that H. assulta has probably expanded its host plant to tobacco and hot pepper recently. Along with many other factors, novel detoxification machinery has probably enabled the herbivore to cope with the new defensive compounds, like nicotine and capsaicin, from the new host plants. What plants had H. assulta been feeding on before it expanded its host range? It would be worthwhile searching for the native host plants of H. assulta, which could provide an insight as to how its host-plant shift or expansion evolved. Datura spp. (devil’s trumpet, Solanaceae) is known as a wild host of H. assulta in India, but no experimental or field evidence has been demonstrated (Jadhav and Armes, 1996). In 2016, however, Ahn and colleagues examined a Datura species (D. stramonium) for the feeding and oviposition performances of H. assulta, and demonstrated that the larval survival and growth on D. stramonium was similarly preferred as to tobacco, while the oviposition was not preferred on the plant surface of D. stramonium (Lim et al., 2016). More field investigations on wild hosts would shed some light on how this specialist has evolved to adapt the novel host plants.

    As shown in the different activities for capsaicin glucosylation between H. assulta and two congeneric generalists (Ahn et al., 2011b), the host-associated performance of H. assulta, as a specialist, could be distinguished especially when it is compared with that of the generalists. Since H. armigera overlappingly occurs in the most geographical areas where H. assulta appears, a set of these two closely-related species have been used as a good model system to study many different topics in the frame of specialists and generalists, including host-plant adaptation (Dong et al., 2002;Tang et al., 2000;Wang et al., 2004, 2017;Zong and Wang, 2007), chemical communication (Cheng et al., 2017;Liu et al., 2014;Sun et al., 2012;Wang et al., 2005;Xu et al., 2016;Zhang et al., 2010), genetics (Ming et al., 2007;Tang et al., 2006;Wang and Dong, 2001), and many others.

    Genome sequences of both H. zea and H. armigera have recently been released with their corresponding publication (Pearce et al., 2017). Overall analysis revealed that the extreme polyphagy of these two major pests from Old and New Worlds, respectively, is associated with extensive gene duplications in detoxification genes and versatile transcriptional responses on different host plants. However, no genome has been sequenced from H. assulta yet, as of February 2022. The H. assulta genome would be not just an additional genome, but an important reference to compare the specialist and generalist genomes. The comparative genomics would pave a new avenue for understanding the persistent adaptability and host specificity of H. assulta from a molecular level, and also provide a deeper insight on the wide adaptability of the congenic generalists. Recently, a transcriptome analysis of larval antennae and mouthparts identified 27 odorant binding proteins and 20 cuticle specific proteins from H. assulta, providing useful information for functional studies of the genes involved in larval foraging (Chang et al., 2017). More “omics” studies along with the multifarious biochemical, physiological and ecological investigations are required to better understand H. assulta, one of the most important agricultural pest species in Korea and other countries.


    The author would like to express special appreciation to the late Prof. Kyung Saeng Boo for his dedication to the development of insect physiology and chemical ecology in Korea. This manuscript is based upon work supported by the National Institute of Food and Agriculture, USDA, Hatch-Multistate project (MIS-311360) and by the Mississippi Agricultural and Forestry Experiment Station (MAFES) Special Research Initiative (SRI) grant.


    The oriental tobacco budworm, Helicoverpa assulta. (A) adult male, (B) adult female, (C) 4th instar larva boring a hole into the hot pepper fruit, and (D) 5th instar larva feeding the flesh inside the pepper fruit (© Seung-Joon Ahn).


    1. Ahn, S.-J. , Badenes-Pérez, F.R. , Heckel, D.G. ,2011a. A host-plant specialist, Helicoverpa assulta, is more tolerant to capsaicin from Capsicum annuum than other noctuid species. J. Insect Physiol. 57, 1212-1219.
    2. Ahn, S.-J. , Badenes-Pérez, F.R. , Reichelt, M. , Svatoš, A. , Schneider, B. , Gershenzon, J. , Heckel, D.G. ,2011b. Metabolic detoxification of capsaicin by UDP-glycosyltransferase in three Helicoverpa species. Arch. Insect Biochem. Physiol. 78, 104-118.
    3. Ahn, S.-J. , Choi, M.-Y. , Boo, K.S. ,2002. Mating effect on sex pheromone production of the oriental tobacco budworm, Helicoverpa assulta. J. Asia-Pacific Entomol. 5, 43-48.
    4. Ahn, S.-J. , Vogel, H. , Heckel, D.G. ,2012. Comparative analysis of the UDP-glycosyltransferase multigene family in insects. Insect Biochem. Mol. Biol. 42, 133-147.
    5. Ali, J.G. , Agrawal, A.A. ,2012. Specialist versus generalist insect herbivores and plant defense. Trends Plant Sci. 17, 293-302.
    6. An, C.H. ,1976. Study on the ecological characteristics of oriental tobacco budworm. Study Tob. Leaves 3, 15-20.
    7. Bernays, E. , Graham, M. ,1988. On the evolution of host specificity in phytophagous arthropods. Ecology 69, 886-892.
    8. Bonaventure, G. , VanDoorn, A. , Baldwin, I.T. ,2011. Herbivoreassociated elicitors: FAC signaling and metabolism. Trends Plant Sci. 16, 294-299.
    9. Boo, K.S. , Park, K.C. , Hall, D.R. , Cork, A. , Berg, B.G. , Mustaparta, H. ,1995. (Z)-9-tetradecenal: a potent inhibitor of pheromone- mediated communication in the oriental tobacco budworm moth, Helicoverpa assulta. J. Comp. Physiol. A 177, 695-699.
    10. Boo, K.S. , Shin, H.C. , Han, M.W. , Lee, M.H. ,1990. Initiation and termination of pupal diapause in the oriental tobacco budworm (Heliothis assulta). Korean J. Appl. Entomol. 29, 277-285.
    11. Boo, K.S. , Yang, J.P. ,1998. Olfactory response of Trichogramma chilonis to Capsicum annuum. J. Asia-Pacific Entomol. 1, 123-129.
    12. Boo, K.S. , Yang, J.P. ,2000. Kairomones used by Trichogramma chilonis to find Helicoverpa assulta eggs. J. Chem. Ecol. 26, 359- 375.
    13. Brattsten, L.B. ,1988. Enzymic adaptations in leaf-feeding insects to host-plant allelochemicals. J. Chem. Ecol. 14, 1919-1939.
    14. Brattsten, L.B. ,1992. Metabolic defenses against plant allelochemicals, Vol II: Ecological and evolutionary processes, in: Rosenthal, G.A., Berenbaum, M.R. (Eds.), Herbivores: Their interactions with secondary plant metabolites. Academic Press, pp. 175-242.
    15. CAB International,2020. Distribution map of Helicoverpa assulta (Oriental tobacco budworm) [WWW Document]. (accessed on 28 January, 2022).
    16. Caterina, M.J. , Schumacher, M.A. , Tominaga, M. , Rosen, T.A. , Levine, J.D. , Julius, D. ,1997. The capsaicin receptor: A heatactivated ion channel in the pain pathway. Nature 389, 816-824.
    17. Chang, H. , Ai, D. , Zhang, J. , Dong, S. , Liu, Y. , Wang, G. ,2017. Candidate odorant binding proteins and chemosensory proteins in the larval chemosensory tissues of two closely related noctuidae moths, Helicoverpa armigera and H. assulta. PLoS ONE 12, e0179243.
    18. Cheng, Q. , Gu, S. , Liu, Z. , Wang, C.-Z. , Li, X. ,2017. Expressional divergence of the fatty acid-amino acid conjugate-hydrolyzing aminoacylase 1 (L-ACY-1) in Helicoverpa armigera and Helicoverpa assulta. Sci. Rep. 7, 8721.
    19. Cho, J.R. , Boo, K.S. ,1988. Behavior and circadian rhythm of emergence, copulation and oviposition in the oriental tobacco budworm, Heliothis assulta Guenée. Korean J. Appl. Entomol. 27, 103-110.
    20. Cho, K.H. , Boo, K.S. ,1990. Change in protein and carbohydrate contents in diapausing and non-diapausing pupae of the oriental tobacco budworm, Heliothis assulta Guenée. Korean J. Appl. Entomol. 29, 286-293.
    21. Choi, K.M. , Cho, E.H. , So, J.S. , Hwang, C.Y. ,1975. Studies on the seasonal occurrences of the tobacco budworm, Heliothis assulta H. (Lepidoptera: Noctuidae), and the parasitism ratio of Trichogramma spp. on the eggs. Korean J. Plant Prot. 14, 137-140.
    22. Choi, K.S. , Boo, K.S. ,1989a. Food attractancy of the oriental tobacco budworm, Heliothis assulta, larvae. Korean J. Appl. Entomol. 28, 88-92.
    23. Choi, K.S. , Boo, K.S. ,1989b. Effects of extracts from some selected wild plant species on larval development and adult oviposition in Heliothis assulta. Korean J. Appl. Entomol. 28, 113-119.
    24. Choi, M.Y. , Han, K.S. , Boo, K.S. , Jurenka, R.A. ,2002. Pheromone biosynthetic pathways in the moths Helicoverpa zea and Helicoverpa assulta. Insect Biochem. Mol. Biol. 32, 1353-1359.
    25. Choi, M.Y. , Tanaka, M. , Kataoka, H. , Boo, K.S. , Tatsuki, S. ,1998a. Isolation and identification of the cDNA encoding the pheromone biosynthesis activating neuropeptide and additional neuropeptides in the oriental tobacco budworm, Helicoverpa assulta (Lepidoptera: Noctuidae). Insect Biochem. Mol. Biol. 28, 759-766.
    26. Choi, M.Y. , Tatsuki, S. , Boo, K.S. ,1998b. Regulation of sex pheromone biosynthesis in the oriental tobacco budworm, Helicoverpa assulta (Lepidoptera: Noctuidae). J. Insect Physiol. 44, 653-658.
    27. Chung, C.S. , Hyun, J.S. ,1980. The effects of temperatures on the development of oriental tobacco budmoth, Heliothis assulta Guenée, and control effects of Thuricide HP®. Korean J. Plant Prot. 19, 57-65.
    28. Cork, A. , Boo, K.S. , Dunkelblum, E. , Hall, D.R. , Jee-Rajunga, K. , Kehat, M. , Kong Jie, E. , Park, K.C. , Tepgidagarn, P. , Xun, L. ,1992. Female sex pheromone of oriental tobacco budworm, Helicoverpa assulta (Guenée) (Lepidoptera: Noctuidae): Identification and field testing. J. Chem. Ecol. 18, 403-418.
    29. Cowles, R.S. , Keller, J.E. , Miller, J.R. ,1989. Pungent spices, ground red pepper, and synthetic capsaicin as onion fly ovipositional deterrents. J. Chem. Ecol. 15, 719-730.
    30. Cunningham, J.P. , Zalucki, M.P. ,2014. Understanding Heliothine (Lepidoptera: Heliothinae) pests: What is a host plant. J. Econ. Entomol. 107, 881-896.
    31. Després, L. , David, J.P. , Gallet, C. ,2007. The evolutionary ecology of insect resistance to plant chemicals. Trends Ecol. Evol. 22, 298- 307.
    32. Dong, J.-F. , Zhang, J.-H. , Wang, C.-Z. ,2002. Effects of plant allelochemicals on nutritional utilization and detoxication enzyme activities in two Helicoverpa species. Acta Entomol. Sin. 45, 296- 300.
    33. Ehrlich, P.R. , Raven, P.H. ,1964. Butterflies and plants: A study in coevolution. Evolution. 18, 586-608.
    34. Eichenseer, H. , Mathews, M.C. , Bi, J.L. , Murphy, J.B. , Felton, G.W. ,1999. Salivary glucose oxidase: Multifunctional roles for Helicoverpa zea? Arch. Insect Biochem. Physiol. 42, 99-109.
    35. Eichenseer, H. , Mathews, M.C. , Powell, J.S. , Felton, G.W. ,2010. Survey of a salivary effector in caterpillars: Glucose oxidase variation and correlation with host range. J. Chem. Ecol. 36, 885- 897.
    36. Feyereisen, R. ,2012. Insect CYP genes and P450 enzymes, in: Insect Molecular Biology and Biochemistry. Elsevier, pp. 236-316.
    37. Fitt, G.P. ,1989. The ecology of Heliothis species in relation to agroecosystems. Annu. Rev. Entomol. 34, 17-53.
    38. Han, M.-W. , Lee, J.-H. , Lee, M.-H. ,1993. Effect of temperature on development of oriental tobacco budworm, Helicoverpa assulta Guenée. Korean J. Appl. Entomol. 32, 236-244.
    39. Han, M.-W. , Lee, J.-H. , Son, J.-S. ,1994. Intra- and inter-plant distribution of Helicoverpa assulta (Lepioprera: Noctuidae) eggs in red pepper and tobacco fields. Korean J. Appl. Entomol. 33, 6-11.
    40. Heckel, D.G. ,2018. Insect detoxification and sequestration strategies, in: Annual Plant Reviews Online. John Wiley & Sons, Ltd, Chichester, UK, pp. 77-114.
    41. Hori, M. , Nakamura, H. , Fujii, Y. , Suzuki, Y. , Matsuda, K. ,2011. Chemicals affecting the feeding preference of the Solanaceaefeeding lady beetle Henosepilachna vigintioctomaculata (Coleoptera: Coccinellidae). J. Appl. Entomol. 135, 121-131.
    42. Hwang, C.Y. , Choi, K.M. , Park, J.S. ,1987. Studies on bionomics of the oriental tobacco budworm, Heliothis assulta Guenée. Res. Rep. RDA 29, 95-113.
    43. Jadhav, D.R. , Armes, N.J. ,1996. Comparative status of insecticide resistance in the Helicoverpa and Heliothis species (Lepidoptera: Noctuidae) of south India. Bull. Entomol. Res. 86, 525-531.
    44. Jallow, M.F.A. , Paul Cunningham, J. , Zalucki, M.P. ,2004. Intraspecific variation for host plant use in Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae): Implications for management. Crop Prot. 23, 955-964.
    45. Jordt, S.E. , Julius, D. ,2002. Molecular basis for species-specific sensitivity to “hot” chili peppers. Cell 108, 421-430.
    46. Jung, J.K. , Boo, K.S. ,1992. Lipid and carbohydrate contents in the adult hemolymph during flight of the oriental tobacco budworm (Helicoverpa assulta (Guenée)). Korean J. Appl. Entomol. 31, 329- 337.
    47. Kamimura, M. , Tatsuki, S. ,1993. Diel rhythms of calling behavior and pheromone production of oriental tobacco budworm moth, Helicoverpa assulta (Lepidoptera: Noctuidae). J. Chem. Ecol. 19, 2953-2963.
    48. Kamimura, M. , Tatsuki, S. ,1994. Effects of photoperiodic changes on calling behavior and pheromone production in the Oriental tobacco budworm moth, Helicoverpa assulta (Lepidoptera: Noctuidae). J. Insect Physiol. 40, 731-734.
    49. Ketterman, A.J. , Saisawang, C. , Wongsantichon, J. ,2011. Insect glutathione transferases. Drug Metab. Rev. 43, 253-265.
    50. Kirkpatrick, T.H. ,1961. Comparative morphological studies of Heliothis species (Lepidoptera: Noctuidae) in Queensland. Queensl. J. Agric. Sci. 18, 179-194.
    51. Koh, Y.H. , Park, K.C. , Boo, K.S. ,1995. Antennal sensilla in adult Helicoverpa assulta (Lepidoptera: Noctuidae): Morphology, distribution, and ultrastructure. Ann. Entomol. Soc. Am. 88, 519-530.
    52. Kumar, P. , Pandit, S.S. , Steppuhn, A. , Baldwin, I.T. ,2014. Natural history-driven, plant-mediated RNAi-based study reveals CYP- 6B46’s role in a nicotine-mediated antipredator herbivore defense. Proc. Natl. Acad. Sci. U. S. A. 111, 1245-1252.
    53. Lee, D.W. , Kim, S.S. , Shin, S.W. , Kim, W.T. , Boo, K.S. ,2006. Molecular characterization of two acetylcholinesterase genes from the oriental tobacco budworm, Helicoverpa assulta (Guenée). Biochim. Biophys. Acta 1760, 125-133.
    54. Lee, J.H. , Boo, K.S. ,1993a. Comparative effects of nicotine and diazinon on larval mortality and activity of cytochrome P-450 monooxygenases in Helicoverpa assulta and Spodoptera exigua. Korean J. Appl. Entomol. 32, 225-235.
    55. Lee, J.H. , Boo, K.S. ,1993b. Activity of mixed function oxidase in a few insect species in relation to their food source. Korean J. Appl. Entomol. 32, 291-299.
    56. Lee, J.-H. , Han, M.-W. ,1998. Survival and development of overwintering pupae of the oriental tobacco budworm, Helicoverpa assulta, from different locality. Korean J. Appl. Entomol. 37, 127- 135.
    57. Lim, H.-J. , Kang, T.J. , Kim, H.H. , Yang, C.Y. , Kim, I. , Kim, D.H. , Ahn, S.-J. ,2016. Effect of a non-host plant Phaseolus vulgaris on larval performance and oviposition of the oriental tobacco budworm Helicoverpa assulta (Lepidoptera: Noctuidae). Entomol. Res. 46, 170-175.
    58. Liu, Y.-L. , Guo, H. , Huang, L.-Q. , Pelosi, P. , Wang, C.-Z. ,2014. Unique function of a chemosensory protein in the proboscis of two Helicoverpa species. J. Exp. Biol. 217, 1821-1826.
    59. Madhumathy, A.P. , Aivazi, A.A. , Vijayan, V.A. ,2007. Larvicidal efficacy of Capsicum annum against Anopheles stephensi and Culex quinquefasciatus. J. Vector Borne Dis. 44, 223-226.
    60. Maliszewska, J. , Tȩgowska, E. ,2012. Capsaicin as an organophosphate synergist against Colorado potato beetle (Leptinotarsa decemlineata Say). J. Plant Prot. Res. 52, 28-34.
    61. Matthews, M. ,1999. Heliothine moths of Australia. A guide to pest bollworms and related noctuid groups. CSIRO Publishing, Collingwood, Australia.
    62. Mazourek, M. , Pujar, A. , Borovsky, Y. , Paran, I. , Mueller, L. , Jahn, M.M. ,2009. A dynamic interface for capsaicinoid systems biology. Plant Physiol. 150, 1806-1821.
    63. McIndoo, N.E. ,1916. Effects of nicotine as an insecticide. J. Agric. Res. Dep. Agric. 7, 89-122.
    64. Ming, Q.-L. , Yan, Y.-H. , Wang, C.-Z. ,2007. Mechanisms of premating isolation between Helicoverpa armigera (Hübner) and Helicoverpa assulta (Guenée) (Lepidoptera: Noctuidae). J. Insect Physiol. 53, 170-178.
    65. Mitter, C. , Poole, R.W. , Matthews, M. ,1993. Biosystematics of the Heliothinae (Lepidoptera: Noctuidae). Annu. Rev. Entomol. 38, 207-225.
    66. Musser, R.O. , Hum-Musser, S.M. , Eichenseer, H. , Peiffer, M. , Ervin, G. , Murphy, J.B. , Felton, G.W. ,2002. Caterpillar saliva beats plant defences. Nature 416, 599-600.
    67. Park, K.C. , Boo, K.S. , Cork, A. , Hall, D.R. ,2002. Monitoring Helicoverpa assulta (Guenée) (Lepidoptera: Noctuidae) with synthetic sex pheromone and small scale disruption trial with controlledrelease PVC resin formulation. Chem. Pharm. Bull. 34, 19-22.
    68. Park, K.C. , Boo, K.S. , Hall, D.R. , Cork, A. ,1994. Biological activity of female sex pheromone of the oriental tobacco budworm, Helicoverpa assulta (Guenée) (Lepidoptera: Noctuidae). Korean J. Appl. Entomol. 33, 26-32.
    69. Park, K.C. , Cork, A. , Boo, K.S. ,1996. Intrapopulational changes in sex pheromone composition during scotophase in oriental tobacco budworm, Helicoverpa assulta (Guenée) (Lepidoptera: Noctuidae). J. Chem. Ecol. 22, 1201-1210.
    70. Park, S.S. , Boo, K.S. ,1988. Structure of sensilla on the antenna and mouthparts of the oriental tobacco budworm (Heliothis assulta Guenée) larvae. Korean J. Appl. Entomol. 27, 94-102.
    71. Pearce, S.L. , Clarke, D.F. , East, P.D. , Elfekih, S. , Gordon, K.H.J. , Jermiin, L.S. , McGaughran, A. , Oakeshott, J.G. , Papanikolaou, A. , Perera, O.P. , Rane, R. V. , Richards, S. , Tay, W.T. , Walsh, T.K. , Anderson, A. , Anderson, C.J. , Asgari, S. , Board, P.G. , Bretschneider, A. , Campbell, P.M. , Chertemps, T. , Christeller, J.T. , Coppin, C.W. , Downes, S.J. , Duan, G. , Farnsworth, C.A. , Good, R.T. , Han, L.B. , Han, Y.C. , Hatje, K. , Horne, I. , Huang, Y.P. , Hughes, D.S.T. , Jacquin-Joly, E. , James, W. , Jhangiani, S. , Kollmar, M. , Kuwar, S.S. , Li, S. , Liu, N.Y. , Maibeche, M.T. , Miller, J.R. , Montagne, N. , Perry, T. , Qu, J. , Song, S. V. , Sutton, G.G. , Vogel, H. , Walenz, B.P. , Xu, W. , Zhang, H.J. , Zou, Z. , Batterham, P. , Edwards, O.R. , Feyereisen, R. , Gibbs, R.A. , Heckel, D.G. , McGrath, A. , Robin, C. , Scherer, S.E. , Worley, K.C. , Wu, Y.D. ,2017. Genomic innovations, transcriptional plasticity and gene loss underlying the evolution and divergence of two highly polyphagous and invasive Helicoverpa pest species. BMC Biol. 15, 63.
    72. Schoonhoven, L.M. , van Loon, J.J.A. , Dicke, M. ,2005. Insectplant biology, Second. ed. Oxford University Press, New York.
    73. Slansky, F. ,1990. Insect nutritional ecology as a basis for studying host plant resistance. Florida Entomol. 73, 359-378.
    74. Snyder, M.J. , Walding, J.K. , Feyereisen, R. ,1994. Metabolic fate of the allelochemical nicotine in the tobacco hornworm Manduca sexta. Insect Biochem. Mol. Biol. 24, 837-846.
    75. Sun, L. , Hou, W. , Zhang, J. , Dang, Y. , Yang, Q. , Zhao, X. , Ma, Y. , Tang, Q. ,2021. Plant metabolites drive different responses in caterpillars of two closely related Helicoverpa species. Front. Physiol. 12, 662978.
    76. Sun, Y.-L. , Huang, L.-Q. , Pelosi, P. , Wang, C.-Z. ,2012. Expression in antennae and reproductive organs suggests a dual role of an odorant-binding protein in two sibling Helicoverpa species. PLoS ONE 7, e30040.
    77. Tang, D. , Wang, C. , Luo, L. , Qin, J. ,2000. Comparative study on the responses of maxillary sensilla styloconica of cotton bollworm Helicoverpa armigera and Oriental tobacco budworm H. assulta larvae to phytochemicals. Sci. China Ser. C Life Sci. 43, 606-612.
    78. Tang, Q.-B. , Jiang, J.-W. , Yan, Y.-H. , van Loon, J.J.A. , Wang, C.-Z. ,2006. Genetic analysis of larval host-plant preference in two sibling species of Helicoverpa. Entomol. Exp. Appl. 118, 221- 228.
    79. Tewksbury, J.J. , Nabhan, G.P. ,2001. Seed dispersal: Directed deterrence by capsaicin in chillies. Nature 412, 403-404.
    80. Tian, K. , Zhu, J. , Li, M. , Qiu, X. ,2019. Capsaicin is efficiently transformed by multiple cytochrome P450s from Capsicum fruit-feeding Helicoverpa armigera. Pestic. Biochem. Physiol. 156, 145-151.
    81. Tomizawa, M. , Casida, J.E. ,2005. Neonicotinoid insecticide toxicology: Mechanisms of selective action. Annu. Rev. Pharmacol. Toxicol. 45, 247-268.
    82. Wang, C. , Dong, J. ,2001. Interspecific hybridization of Helicoverpa armigera and H. assulta (Lepidoptera: Noctuidae). Chinese Sci. Bull. 46, 489-491.
    83. Wang, C. , Dong, J. , Tang, D. , Zhang, J. , Li, W. , Qin, J. ,2004. Host selection of Helicoverpa armigera and H. assulta and its inheritance. Prog. Nat. Sci. 14, 880-884.
    84. Wang, H.-L. , Zhao, C.-H. , Wang, C.-Z. ,2005. Comparative study of sex pheromone composition and biosynthesis in Helicoverpa armigera, H. assulta and their hybrid. Insect Biochem. Mol. Biol. 35, 575-583.
    85. Wang, K.-Y. , Zhang, Y. , Wang, H.-Y. , Xia, X.-M. , Liu, T.-X. ,2008. Biology and life table studies of the oriental tobacco budworm, Helicoverpa assulta (Lepidoptera: Noctuidae), influenced by different larval diets. Insect Sci. 15, 569-576.
    86. Wang, Y. , Ma, Y. , Zhou, D.-S. , Gao, S.-X. , Zhao, X.-C. , Tang, Q.-B. , Wang, C.-Z. , van Loon, J.J.A. ,2017. Higher plasticity in feeding preference of a generalist than a specialist: Experiments with two closely related Helicoverpa species. Sci. Rep. 7, 17876.
    87. Weissenberg, M. , Klein, M. , Meisner, J. , Ascher, K.R.S. ,1986. Larval growth inhibition of the spiny bollworm, Earias insulana, by some steroidal secondary plant compounds. Entomol. Exp. Appl. 42, 213-217.
    88. Wu, K.J. , Gong, P.Y. , Ruan, Y.M. ,2006. Is tomato plant the host of the oriental tobacco budworm, Helicoverpa assulta (Guenée)? Acta Entomol. Sin. 49, 421-427.
    89. Xie, L. , Jiang, M. , Zhang, X. ,1998. Effect of temperature and humidity on laboratory population of Helicoverpa assulta. Acta Entomol. Sin. 41, 61-69.
    90. Xu, G. , Qin, J. ,1994. Extraction and characterization of midgut proteases from Heliothis armigera and H. assulta (Lepidoptera: Noctuidae) and their inhibition by tannic acid. J. Econ. Entomol. 87, 334-338.
    91. Xu, G. , Qin, J.-D. ,1987. Responses of two Heliothis species to plant secondary substances: the influence of host secondary substances on larval growth and food utilization. Acta Entomol. Sin. 30, 359- 366.
    92. Xu, M. , Guo, H. , Hou, C. , Wu, H. , Huang, L.-Q. , Wang, C.-Z. ,2016. Olfactory perception and behavioral effects of sex pheromone gland components in Helicoverpa armigera and Helicoverpa assulta. Sci. Rep. 6, 22998.
    93. Yang, C.-Y. , Jen, H.-Y. , Cho, M.-R. , Kim, D.-S. , and Yiem, M.-S. ,2004. Seasonal occurrence of oriental tobacco budworm (Lepidoptera: Noctuidae) male and cohemical control at red pepper fields. Korean J. Appl. Entomol. 43, 49-54.
    94. Yang, L. , Wang, X. , Bai, S. , Li, Xin, Gu, S. , Wang, C.-Z. , Li, Xianchun ,2017. Expressional divergence of insect GOX genes: From specialist to generalist glucose oxidase. J. Insect Physiol. 100, 21- 27.
    95. Yoshinaga, N. , Aboshi, T. , Abe, H. , Nishida, R. , Alborn, H.T. , Tumlinson, J.H. , Mori, N. ,2008. Active role of fatty acid amino acid conjugates in nitrogen metabolism in Spodoptera litura larvae. Proc. Natl. Acad. Sci. U. S. A. 105, 18058-18063.
    96. Zalucki, M.P. , Daglish, G. , Firempong, S. , Twine, P. ,1986. The biology and ecology of Heliothis armigera (Hübner) and Heliothis punctigera Wallengren (Lepidoptera, Noctuidae) in Australia - What do we know. Aust. J. Zool. 34, 779-814.
    97. Zhang, D.-D. , Zhu, K.Y. , Wang, C.-Z. ,2010. Sequencing and characterization of six cDNAs putatively encoding three pairs of pheromone receptors in two sibling species, Helicoverpa armigera and Helicoverpa assulta. J. Insect Physiol. 56, 586-593.
    98. Zhang, Y. , Wang, K.Y. , Wang, G. , Guo, Q.L. , Fan, K. , Yuan, X.L. , Wu, C.Z. ,2006. Preference and adaptability of oriental tobacco budworm, Helicoverpa assulta, to three food plants. Chinese Bull. Entomol. 43, 781-784.
    99. Zhou, D.-S. , Wang, C.-Z. , van Loon, J.J.A. ,2022. Habituation to a deterrent plant alkaloid develops faster in the specialist herbivore Helicoverpa assulta than in its generalist congener Helicoverpa armigera and coincides with taste neuron desensitisation. Insects 13, 21.
    100. Zhu, J. , Tian, K. , Reilly, C.A. , Qiu, X. ,2020. Capsaicinoid metabolism by the generalist Helicoverpa armigera and specialist H. assulta: Species and tissue differences. Pestic. Biochem. Physiol. 163, 164-174.
    101. Zong, N. , Wang, C.-Z. ,2004. Induction of nicotine in tobacco by herbivory and its relation to glucose oxidase activity in the labial gland of three noctuid caterpillars. Chinese Sci. Bull. 49, 1596-1601.
    102. Zong, N. , Wang, C.-Z. ,2007. Larval feeding induced defensive responses in tobacco: Comparison of two sibling species of Helicoverpa with different diet breadths. Planta 226, 215-224.

    Vol. 40 No. 4 (2022.12)

    Journal Abbreviation Korean J. Appl. Entomol.
    Frequency Quarterly
    Doi Prefix 10.5656/KSAE
    Year of Launching 1962
    Publisher Korean Society of Applied Entomology
    Indexed/Tracked/Covered By