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. 2025 Jun 17;33(4):1605–1617. doi: 10.1111/1744-7917.70090

Impact of TYLCV infection on host selection and feeding behavior of MED Bemisia tabaci on pepper plants

Yang Zhong 1,2,#, Jingyu Guo 2,#, Yan Li 2, Yaqi Wen 2, Jie Hu 2, Baiming Liu 3,✉, Qingjun Wu 4,✉, Xiaoguo Jiao 2,✉
PMCID: PMC13441021  PMID: 40525520

Abstract

The tomato yellow leaf curl virus (TYLCV), spread by the vector insect Bemisia tabaci, dramatically reduces worldwide tomato production and quality. Plant‐mediated interactions between TYLCV and vector whiteflies commonly occur when previous infestations induce both volatile and nonvolatile changes in the shared host. These induced changes of the shared host may differentially affect subsequent interacting species within the plant–insect–virus tripartite system. These altered volatile profiles can be perceived as airborne cues that enhance or suppress defense responses in neighboring conspecifics, a phenomenon known as “plant–plant communication.” Here, we present the first evidence that TYLCV‐infected Mediterranean (MED) B. tabaci (hereafter referred to as viruliferous MED) preferentially settles and oviposits on previously infested peppers, an alternative host for TYLCV, over those merely exposed and intact ones. Furthermore, differences in feeding behavior of viruliferous MED, assessed using an electrical penetration graph, clearly indicate that these MED whiteflies feed more effectively on previously infested and exposed peppers than on healthy ones. Our results suggest that the suppression of pepper defenses—both nonvolatile and volatile—by previous infestation and exposure to viruliferous MED promotes alternative host‐mediated mutualism between MED and TYLCV. These findings provide insight into peppers, functioning as alternative hosts, mediating the interactions between TYLCV and its vector MED whiteflies. Moreover, our results may enhance the understanding of TYLCV epidemics, particularly in the context of the rapid invasion of MED B. tabaci, thereby facilitating the development of novel management strategies for controlling this viral pathogen and its devastating whiteflies.

Keywords: Bemisia tabaci, electrical penetration graph, induced defenses, plant–insect–virus tripartite system, plant–plant communication

The tomato yellow leaf curl virus (TYLCV), spread by the vector insect Bemisia tabaci, dramatically reduces worldwide tomato production and quality. Even though the tomato crops are considered to be the major host and reservoir of TYLCV, tomato is not grown year‐round in most areas of the world, and alternate hosts, such as pepper and eggplant intercropped with tomato, could be relevant in recurring annual TYLCV epidemics. In the present study, we present the first evidence that TYLCV‐infected Mediterranean (MED) B. tabaci (hereafter referred to as viruliferous MED) preferentially settled and oviposited on previously infested peppers, an alternate host for TYLCV, over those merely exposed and intact ones. Our results suggest that the suppression of pepper defenses—both nonvolatile and volatile—by previous infestation and exposure to viruliferous MED promotes alternate host‐mediated mutualism between MED and TYLCV.

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Introduction

Plants have developed sophisticated defensive mechanisms that encompass both constitutive and inducible defense against multiple attackers (Karban & Baldwin, 1997; Schuman & Baldwin, 2016; Stahl et al., 2018; Fernández de Bobadilla et al., 2022). Constitutive defenses are considered costly, as they remain active even in undamaged plants (Wittstock & Gershenzon, 2002; Ito & Sakai, 2009). In contrast, plants under attack are more likely to enhance induced resistance, which includes the production of secondary metabolites and the emission of herbivore‐induced plant volatiles (HIPVs) (Wu & Baldwin, 2010; Hu et al., 2021). HIPVs play a critical role in both direct and indirect plant defenses, including repelling insect herbivores and attracting their natural enemies (War et al., 2011; Hu, 2022). Furthermore, these volatile compounds serve as reliable airborne cues that can be detected by neighboring plants, a phenomenon known as “plant–plant communication” (Ninkovic et al., 2021; Kessler et al., 2023). In some instances, HIPVs function as warning signals, activating various combinations of defensive traits in neighboring plants in response to impending threats (Dicke & Baldwin, 2010; Hare, 2011). Over millions of years of co‐evolution with plants, herbivores have developed numerous adaptive strategies to counter host defenses for their benefits (Howe & Jander, 2008; Huot et al., 2013). Consequently, volatile communication can be disrupted by these biotic stressors to prevent adjacent plants from priming effective defense responses, thereby enhancing the herbivores' success across a wide range of hosts (Marmolejo et al., 2021; Brosset & Blande, 2022).

In nature, plants often interact simultaneously with herbivorous arthropods and pathogenic microorganisms (Pieterse & Dicke, 2007). Among various pathogens, plant viruses are obligate parasites that account for nearly half of emerging infectious diseases and pose a significant threat to global crop yields (Zaitlin & Palukaitis, 2000; Jones & Naidu, 2019; Lefeuvre et al., 2019). Most phytoviruses are transmitted exclusively by insect vectors, highlighting the close relationship between these 2 detrimental agents (Gallet et al., 2018). The process of viral infection and spread involves a complex interplay among plants, insects, and viruses, as viruses rely on vectors for transmission while competing with them for plant resources (Wei et al., 2018; Noman et al., 2020). Generally, plant‐mediated interactions between insect and virus occur when insect infestations or viral infections alter phenotypic changes of the shared host plant, subsequently affecting additional attackers in distinct ways (Cory & Hoover, 2006; Chisholm et al., 2018). Consequently, such phenotypic changes related to previous attacks can modify the interactions between insect and virus, thereby reshaping their mutualism at the same trophic level (Shikano et al., 2017). Given that specific changes in volatile and nonvolatile profiles are context‐dependent, understanding these plant‐mediated interactions has important implications not only for individual organisms but also for the population dynamics of the interacting species within the plant–insect–virus tripartite system.

Tomato yellow leaf curl virus (TYLCV), a notorious virus belonging to the genus Begomovirus, originated in the Middle East–Mediterranean region and has been introduced to many other parts of the world (Prasad et al., 2020; Paris et al., 2024). In China, TYLCV has been reported in several provinces in recent years, significantly reducing tomato production and resulting in unprecedented annual economic losses (Li et al., 2022). As a whitefly‐borne phytovirus, TYLCV can directly influence vector performance in ways that enhance its transmission (Fang et al., 2013; Moreno‐Delafuente et al., 2013; Paris et al., 2024). Additionally, TYLCV usually modifies plant metabolism, increasing host attractiveness to both whitefly vectors and nonvector herbivores (Shi et al., 2013; Su et al., 2016). However, most studies on these tripartite interactions have primarily focused on tomatoes due to their status as a superior inoculum resource for TYLCV (Luan et al., 2014; Paris et al., 2024). Alternative hosts serving as inoculum resources may also play a critical role in the persistence and spread of TYLCV in agroecosystems (Polston et al., 2006; Kil et al., 2014; Cañizares et al., 2015). Although the phenomenon of plant‐mediated interactions between TYLCV and its whitefly vectors has been widely documented, the role of alternative hosts in this tripartite system remains largely unexplored.

The whitefly Bemisia tabaci (Hemiptera, Aleyrodidae) is a highly invasive pest responsible for significant crop losses due to its feeding on phloem sap and its transmitting numerous begomoviruses, including TYLCV (Adkins et al., 2011; Morin et al., 2024; Paris et al., 2024). It is widely recognized that B. tabaci represents a cryptic species complex, with the Mediterranean (MED) being the dominant invasive species contributing to severe TYLCV epidemics in many regions of China (Pan et al., 2011, 2012). Given that specific phenotypic changes can influence subsequent community assembly, we infer that the plant—particularly the alternative host—serves as a key mediator in the interactions between vector MED B. tabaci and TYLCV. Pepper (Capsicum annuum), one of the most important vegetable crops, is recognized as both an alternative host and an inoculum source for TYLCV, as well as a reservoir for its whitefly vector (Polston et al., 2006; Firdaus et al., 2011; Kil et al., 2014; Legarrea et al., 2020). Furthermore, HIPVs are known to function as airborne cues in plant–plant communication, leading us to hypothesize that volatiles emitted from damaged peppers may induce metabolic changes in neighboring conspecifics, thereby differentially influencing subsequent attackers (Riahi et al., 2021). Since pepper plants are typically grown at high densities and neighbors are often in close proximity, volatile‐mediated communication among pepper plants is anticipated to play a particularly crucial role in plant–insect–virus tripartite interactions. In addition, even though the tomato crops are considered to be the major host and reservoir of TYLCV (Adkins et al., 2011), tomato is not grown year‐round in most areas of the world, and alternative hosts, such as pepper and eggplant intercropped with tomato, could be relevant in recurring annual TYLCV epidemics (Legarrea et al., 2020).

In this study, we aimed to: (i) conduct behavioral assays to determine the settling and oviposition preferences of TYLCV‐infected MED whiteflies on differently treated pepper plants, including intact pepper plants (CK), TYLCV‐infected MED‐infested pepper plants (Infested), and noninfested plants exposed to those previously infested by TYLCV‐infected MED (Exposed); and (ii) use electrical penetration graphs (EPGs) to assess the feeding behaviors of TYLCV‐infected MED on the aforementioned treated pepper plants. With these experiments, we sought to provide new insights into the ecological implications of alternative hosts on plant–insect–virus tripartite interactions. Importantly, these results may help explain the observed concurrence of TYLCV spread and the invasion of MED B. tabaci in the landscape.

Materials and methods

Insects and host plants

The Mediterranean (MED) cryptic species of the Bemisia tabaci species complex was originally collected from poinsettia (Euphorbia pulcherrima) in 2008 in Beijing, and subsequently maintained on tomato (Solanum lycopersicum var. Zhongza 9) in separate insect‐proof screened cages (60 × 60 × 60 cm) at a laboratory‐controlled environment of 23 ± 2 °C, 60% ± 10% relative humidity (RH), and a photoperiod of 14 h light and 10 h dark (14L : 10D). The purity of the cultures was monitored every 2 to 3 generations using the random amplified polymorphic DNA‐polymerase chain reaction (RAPD‐PCR) technique (Chu et al., 2007). TYLCV‐infected tomato plants were generated via agroinoculation at the 3‐ to 4‐true‐leaf stage with Agrobacterium tumefaciens‐mediated TYLCV clones originally isolated from Shanghai, China (Wu et al., 2006). Infection was assessed visually and confirmed through PCR validation (Ghanim et al., 2007). TYLCV‐infected MED whiteflies were obtained by placing 3 TYLCV‐infected tomato plants into an insect‐proof screened cage and subsequently introducing 300 virus‐free MED adults into the cage. After 2 generations, the TYLCV‐infected MED whiteflies were used for the following experiments. Pepper plants (Capsicum annuum var. Hangjiao) were grown from seed in a greenhouse maintained at 23 ± 2 °C with natural lighting. Two weeks after sowing, seedlings were transplanted into 5‐cm‐diameter plastic pots (one seedling per pot). All tested plants were free from pests and pathogens and were treated with the same level of fertilizer. When the plants developed 6 main leaves, seedlings of similar size were selected for the subsequent experiments.

Settling and oviposition preference of TYLCV‐infected MED on intact, infested, and exposed pepper plants

The host choice experiment assessing the settling and oviposition preferences of viruliferous MED whiteflies was conducted as described by Jiao et al. (2013, 2012, 2014). The host choice experiments were carried out in the laboratory under controlled conditions of 25 ± 2 °C, 75% ± 5% RH, and a photoperiod of 14 L: 10 D. The experiments included 3 treatments: intact pepper plants (CK), viruliferous MED‐infested pepper plants (Infested), and noninfested plants exposed to viruliferous MED‐infested plants (Exposed). The infested plants were prepared by attaching 1 clip cage per plant, each containing 50 viruliferous MED whiteflies. The exposed plants were positioned within 10 cm of the infested plants but did not come into direct contact. To eliminate potential effects of clip cage attachment, intact and exposed pepper plants were also fitted with 1 clip cage without adding whiteflies. After 72 h, the pepper plants were utilized for the host choice experiment. One plant from each treatment (CK, Infested, and Exposed) was placed in a screened cage (60 × 60 × 60 cm). The 3 pepper plants in each cage were arranged in an equilateral triangle with 20 cm sides to prevent leaf contact. Approximately 150 viruliferous MED whiteflies were collected between 07:00 and 08:00 hours and released from an aspirator into the center of the screened cage above the plant canopy. The aspirator, containing the whiteflies in a sampling bottle, was held inside a clear plastic tumbler suspended 30 cm above the canopy. The whiteflies moved to the open top of the sampling bottle and flew away to approach the plants from above. The number of whiteflies that settled on each plant was counted after 12, 24, 36, 48, 60, 72, 84, 96, 108, and 120 h. To minimize movement among leaves and plants during counting, the whiteflies were counted under dim light just before 07:00 hours and just after 19:00 hours. After the settling assay, all leaves from each pepper plant were removed, and the number of eggs laid (an indicator of oviposition preference) on each plant within each treatment was assessed under a dissecting microscope. The settling and oviposition preferences of viruliferous MED whiteflies were replicated 7 times.

EPG feeding behaviors of TYLCV‐infected MED on intact, infested, and exposed pepper plants

Waveform patterns of EPG feeding by viruliferous MED whiteflies were classified according to Liu et al. (2012). Specifically, we identified 5 distinct waveforms: nonprobing (“NP”), pathway (“C”), potential drop (“pd”), phloem salivation (“E(pd)1”), and phloem sap ingestion (“E(pd)2”). Two rare waveforms, F (indicating presumed penetration difficulties) and G (related to xylem sap ingestion), were grouped under waveform C. Data on the start and end times of each waveform were used to calculate 6 nonphloem parameters (number of probes, total duration of probes, total duration of NP, total duration of C, time from 1st probe before 1st E(pd), and number of probes before 1st E(pd)) and 8 phloem parameters (total duration of E(pd)1, number of E(pd)1, mean duration of E(pd)1, total duration of E(pd)2, number of E(pd)2, mean duration of E(pd)2, potential E(pd)2 index, and percentage of phloem phases reaching E(pd)2). The phloem and nonphloem parameters assess various aspects of whitefly feeding, corresponding to whether the insect stylet is inserted into the phloem or not. Each parameter was calculated for all 30 replicates; mean values and standard errors were computed for each parameter across the 3 treatments.

Statistical analysis

Statistical analysis was conducted using SPSS (version 13.0; SPSS Inc., Chicago, IL, USA). Before performing analysis of variance (ANOVA), we applied the Levene test and the Shapiro–Wilk test to assess homogeneity of variance and normality, respectively. Differences in settling preferences of TYLCV‐infected MED whiteflies among the 3 treatments were evaluated using repeated‐measures ANOVA (RMANOVA). Female oviposition preferences of TYLCV‐infected MED whiteflies among the 3 treatments were analyzed with one‐way ANOVA. Similarly, feeding parameters of TYLCV‐infected MED based on EPG data were compared among the 3 treatments using one‐way ANOVA. Tukey's test was employed to separate treatment means when the main effect was statistically significant. The data for the percentage of MED whiteflies reaching E(pd)2 among the 3 treatments (CK, Infested, and Exposed) were compared using a Chi‐square test.

Results

Settling and oviposition of TYLCV‐infected MED on intact, infested, and exposed pepper plants

Viruliferous MED whiteflies exhibited a significant preference for settling on the previously infested plants, followed by the exposed plants, and least on the intact plants (F 2,18 = 930.094, P < 0.001; Fig. 1). Similarly, viruliferous MED whiteflies demonstrated a preference for ovipositing on the previously infested plants compared to the exposed and the intact plants (F 2,18 = 14.161, P < 0.001; Fig. 2).

Fig. 1.

Fig. 1

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Host choices (as indicated by settling on whole plants) of tomato yellow leaf curl virus (TYLCV)‐infected Mediterranean (MED) whiteflies on the intact (CK), infested, and exposed pepper plants. Clip cages were used on the infested plants with TYLCV‐infected MED. Values are means ± standard error. Means with different letters are significantly different (P < 0.05).

Fig. 2.

Fig. 2

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Egg‐laying choices of tomato yellow leaf curl virus (TYLCV)‐infected Mediterranean (MED) whiteflies on the intact (CK), infested, and exposed pepper plants. Clip cages were used on the infested plants with TYLCV‐infected MED. Values are means + standard error. Means with different letters are significantly different (P < 0.05).

EPG feeding behaviors of TYLCV‐infected MED on the intact, infested, and exposed pepper plants

Among the 6 nonphloem parameters, there were no significant differences in the total number of probes (Fig. 3A, F 2,86 = 1.382, P = 0.256), total duration of probes (Fig. 3B, F 2,86 = 3.046, P = 0.053), total duration of NP (Fig. 3C, F 2,86 = 3.046, P = 0.053), total duration of pathway (C) (Fig. 3D, F 2,86 = 1.893, P = 0.157), and number of probes before the 1st potential drop (E(pd)) (Fig. 3F, F 2,86 = 2.172, P = 0.120) across the 3 treatments. In contrast, the time from the 1st probe to the 1st E(pd) (Fig. 3E, F 2,86 = 3.805, P = 0.026) during viruliferous MED feeding on the infested and the exposed plants was significantly shorter compared to intact plants, with no significant difference observed between the infested and the exposed pepper plants.

Fig. 3.

Fig. 3

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Nonphloem electrical penetration graph (EPG) parameters A to F of tomato yellow leaf curl virus (TYLCV)‐infected Mediterranean (MED) whiteflies feeding on different pepper plants (CK: Intact plant; Infested: pre‐infested plant by TYLCV‐infected MED whiteflies; Exposed: pepper plants exposed to the plant pre‐infested by TYLCV‐infected MED). Values are means + standard error. Different letters show significant differences among the 3 treatments.

Among the 8 phloem parameters, the feeding efficiencies of viruliferous MED on the infested and exposed plants were significantly higher in total duration of E(pd)1 (Fig. 4A, F 2,86 = 5.640, P = 0.005), number of E(pd)1 (Fig. 4B, F 2,86 = 4.718, P = 0.011), mean duration of E(pd)1 (Fig. 4C, F 2,86 = 7.704, P = 0.001), and number of E(pd)2 (Fig. 4E, F 2,86 = 5.676, P = 0.012), while no significant difference was found between the infested and exposed pepper plants. However, there were no significant differences in total duration of E(pd)2 (Fig. 4D, F 2,86 = 1.269, P = 0.286), mean duration of E(pd)2 (Fig. 4F, F 2,86 = 0.478, P = 0.622), and potential E(pd)2 index (Fig. 5A, F 2,86 = 1.194, P = 0.308) among the 3 treatments. Furthermore, the percentage of phloem phases reaching E(pd)2 during viruliferous MED feeding on the infested and exposed plants was significantly higher than that on intact plants (Fig. 5B, χ 2 = 10.369, P = 0.005), with no significant difference observed between the infested and exposed pepper plants.

Fig. 4.

Fig. 4

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Phloem electrical penetration graph (EPG) parameters A to F of tomato yellow leaf curl virus (TYLCV)‐infected Mediterranean (MED) whiteflies feeding on different pepper plants (CK: Intact plant; Infested: pre‐infested plant by TYLCV‐infected MED whiteflies; Exposed: pepper plants exposed to the plant pre‐infested by TYLCV‐infected MED). Values are means + standard error. Different letters show significant differences among the 3 treatments.

Fig. 5.

Fig. 5

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Electrical penetration graph (EPG) parameters A to B of tomato yellow leaf curl virus (TYLCV)‐infected Mediterranean (MED) whiteflies feeding on different pepper plants (CK: Intact plant; Infested: pre‐infested plant by TYLCV‐infected MED whiteflies; Exposed: pepper plants exposed to the plant pre‐infested by TYLCV‐infected MED). Values are means + standard error. Different letters show significant differences among the 3 treatments.

Discussion

The simultaneous presence of multiple intruders, such as herbivores and pathogens, sharing a plant is common in nature, resulting in complex interactions among plants, insects, and viruses (Dietzgen et al., 2016; Paris et al., 2024). Generally, plant mediation of interactions between insect and virus occurs when specific attacks induce volatile and/or nonvolatile changes that differentially affect subsequent attackers (Stout et al., 2006). Understanding these plant‐mediated indirect effects has ecological implications for both host defenses and the epidemiology of viral diseases in conjunction with pest invasions. In this study, we investigated for the first time the role of pepper (Capsicum annuum var. Hangjiao) as an alternative host that modifies the interactions between TYLCV and its vector, MED B. tabaci, under laboratory conditions. With behavioral assays and EPG experiments, we demonstrated that the preference and feeding performance of TYLCV‐infected MED were significantly enhanced on the infested and exposed pepper plants. Thus, the increased susceptibility in the alternative host indicates a pepper‐mediated mutualistic relationship between TYLCV and vector MED B. tabaci.

Plants often respond defensively to herbivory by establishing physical and chemical barriers through the activation of phytohormonal signaling networks (Berens et al., 2017). Although increased resistance typically deters aggregative feeding, some herbivores enhance plant susceptibility by manipulating host defenses, facilitating subsequent community assembly (Hancock et al., 2015). For instance, the invasive spider mite Tetranychus evansi reduces defensive profiles mediated by salicylic acid (SA) and jasmonic acid (JA) in tomato plants, particularly suppressing proteinase inhibitors and favoring heterospecific native mites (Sarmento et al., 2011). Similar findings by Su et al. (2018) showed that MED B. tabaci significantly suppressed terpenoid and flavonoid levels, thereby promoting conspecific colonization on tomato plants. In this study, viruliferous MED exhibited a strong preference for and increased oviposition on conspecific‐infested peppers, suggesting that this whitefly species can enhance plant susceptibility to subsequent herbivores. These findings align with observations made by Colvin et al. (2006), who reported that viruliferous B. tabaci feeding on TYLCV‐infected tomato plants experienced greater population increases than those feeding on healthy controls. The Begomovirus‐infected whitefly typically feeds in large aggregations on plant leaves, manipulating host defenses. For example, the JA‐related defenses of tobacco plants were impaired by Middle East‐Asia Minor 1 (MEAM1) B. tabaci carrying the bipartite Begomovirus tomato yellow leaf curl China virus (TYLCCNV), thus promoting subsequent whitefly development (Zhang et al., 2012). TYLCV‐infected MED whiteflies also significantly suppressed JA‐related defenses in tomato, potentially accelerating the increase of the MED population (Shi et al., 2018, 2014). Furthermore, TYLCCNV‐infected MEAM1 notably attenuated terpene biosynthesis in tobacco by inhibiting the JA‐associated transcription factor MYC2, leading to reduced plant resistance and enhanced performance of whitefly vectors (Luan et al., 2013; Li et al., 2014). The increased susceptibility observed in our study suggests that TYLCV‐infected MED manipulates defensive mechanisms, rendering the infested peppers more favorable to subsequently colonizing conspecifics. However, how plant defenses influence this interaction remains poorly understood. Our previous studies demonstrated that phenolic‐dependent defensive traits are significantly reduced in nonviruliferous MED‐infested peppers, while effective SA and JA pathways remained unaltered (Hu et al., 2023). Considering that plant defense responses to colonizing herbivores are species‐specific and highly context‐dependent, further research is required to determine how viruliferous MED affects pepper defense profiles, which may modify the behavior of subsequently colonizing conspecifics in this context.

The EPG has been extensively used to measure specific probing and feeding behaviors of phloem‐feeders, including whiteflies (Liu et al., 2013; Jiao et al., 2018; Walker et al., 2024). EPG parameters, such as frequency, duration, and waveform sequence, serve as reliable indicators of plant suitability (Lu et al., 2021). For example, in our previous work, we observed that the mean duration of the pd waveform, which indicates an intracellular puncture, was significantly different, suggesting that exposure to toxic hydrolysates of glucosinolate and myrosinase was greater for MED B. tabaci than for MEAM1, which may explain why MED performs relatively poorly on cabbage plants (Hu et al., 2020). In this study, phloem phase parameters such as the total duration of E(pd)1, number of E(pd)1, mean duration of E(pd)1, and number of E(pd)2 were significantly higher on conspecific‐infested peppers than on intact controls, indicating that viruliferous MED‐infested peppers are highly suitable for subsequent feeding by conspecifics. Indeed, viruses can directly enhance the performance of their vectors to maximize transmission (Ng & Falk, 2006). This is especially true for persistently transmitted viruses, including TYLCV, which require prolonged feeding by whitefly vectors for acquisition and transmission of the virus (Hogenhout et al., 2008). As phloem phase behaviors are closely related to viral infection, EPG is frequently employed to study the transmissibility of TYLCV by whiteflies, focusing on specific activities such as penetration through intercellular spaces and the establishment of feeding sites in phloem sieve elements (Fereres & Moreno, 2009; Tan et al., 2017). Previous research has demonstrated that TYLCV‐infected MED whiteflies feed more frequently from phloem sieve elements and make a larger number of phloem contacts in tomato, which likely increases TYLCV transmission (Moreno‐Delafuente et al., 2013). Although the feeding behavior documented here reflects a pepper‐mediated mutualistic relationship between vector MED B. tabaci and TYLCV, the capacity of whiteflies to acquire and transmit this Begomovirus remains largely unknown. Given the limited combination of results studied thus far, it is essential to gain a deeper understanding of our system, particularly the positively direct effects of TYLCV on whitefly vectors feeding on peppers.

All plants within natural ecosystems interact with one another (Brooker, 2006). The HIPVs, one kind of communication among plants, serve as warning signals to neighboring plants in anticipation of imminent threats, thereby enhancing their anti‐herbivore defenses in advance (Ninkovic et al., 2019). For example, maize plants exposed to neighbors infested with Spodoptera littoralis exhibited increased resistance and negatively affected the development of this lepidopteran pest (Ton et al., 2007). Similarly, Peng et al. (2011) found that cabbage plants activated several defense‐related genes and became more resistant when exposed to volatiles emitted from neighbors infested by Pieris brassicae. However, herbivorous arthropods have developed various adaptive strategies to interfere with volatile‐mediated plant communication for their own benefit (Li et al., 2017; Ye et al., 2018; Zhang et al., 2019; De Lange et al., 2020; Lin et al., 2021). In these cases, HIPVs can act as suppressors of resistance or induce “incorrect” defense responses in neighboring plants (Erb, 2018). The phloem‐feeding whitefly, for instance, is well‐known for its ability to disrupt volatile communication, thereby preventing neighboring plants from priming effective defenses and enhancing its success across a wide range of hosts (Walling, 2008; Zhang et al., 2009). In the present study, the preference and feeding performance of viruliferous MED were significantly enhanced on exposed pepper plants, suggesting that pepper volatiles induced by this whitefly species may lead to increased susceptibility in neighboring plants, ultimately favoring subsequent conspecifics. Further studies should clarify the key volatile compounds induced by TYLCV‐infected MED B. tabaci and elucidate the molecular mechanisms underlying the suppression of host defenses in neighboring plants within our system. This may add a new dimension to the role of HIPVs as mediators of plant communication within the pepper community.

In recent years, a growing number of studies examining the plant‐mediated interactions between TYLCV and whitefly have primarily focused on tomato, while a limited number have investigated the role of alternative hosts in this tripartite system. However, tomatoes are not cultivated year‐round; therefore, alternative hosts that act as inoculum sources during growing seasons, especially in crop‐free periods, could play a significant role in TYLCV epidemics (Duffus, 1971; Smith et al., 2015; Legarrea et al., 2020). One pertinent example is pepper, which is recognized as a controversial host of TYLCV in the landscape (Legarrea et al., 2020). Given that specific phenotypic changes can influence subsequent community structures, we infer that plants, particularly alternative hosts, may serve as key mediators of interactions between TYLCV and MED whiteflies. Through behavioral assays and EPG experiments, we documented an intriguing phenomenon: pepper plants infested by TYLCV‐infected MED exhibited enhanced susceptibility to subsequent conspecifics. It should be noted that it is uncertain whether the increased susceptibility arises from MED whitefly infestation or TYLCV infection. Indeed, phytoviruses not only directly enhance vector performance but also indirectly manipulate plant defenses to maximize their transmission (Wu & Ye, 2020). For instance, TYLCV not only enriches the nutritional content of leaf tissue and phloem sap but also suppresses herbivore‐induced production of plant defensive enzymes and callose deposition, both of which benefit MED whiteflies (Su et al., 2015). Similarly, potato leaf roll virus (PLRV) and barley yellow dwarf virus (BYDV) mediate changes in the odor characteristics of their host plants, making virus‐infected plants more attractive to aphids than healthy plants (Ingwell et al., 2012). It should be noted that we previously proposed that phenolic‐dependent defensive traits are significantly impaired in MED‐infested pepper plants (Hu et al., 2023). Therefore, it is necessary and needs more convincing evidence to clarify whether viral copies of TYLCV can replicate at high levels in pepper plants, enabling the manipulation of plant defense.

TYLCV, a significant threat to global tomato production, is transmitted exclusively by the whitefly B. tabaci in a persistent and circulative manner. Given that TYLCV epidemics are associated with the invasion of MED B. tabaci in China, a comprehensive understanding of this plant–insect–virus tripartite system is crucial. In the present experiments, we aimed to provide new insights into the role of alternative hosts in the plant‐mediated interactions between TYLCV and its vector, MED B. tabaci. Notably, we found that the host choice preference and feeding performance of TYLCV‐infected MED were significantly enhanced on the infested and exposed pepper plants compared to those on the intact controls. Specifically, viruliferous MED can interfere with volatile‐mediated communication in pepper plants, which may explain this species' success as an invasive pest. To our knowledge, this is the first study to demonstrate the ability of TYLCV‐infected MED whiteflies to manipulate both volatile and nonvolatile defense profiles in a contentious alternative host. Understanding insect–virus interactions mediated by alternative hosts may not only elucidate the emergence of TYLCV alongside the rapid invasion of MED B. tabaci but also inform effective strategies for controlling this viral disease and whitefly pest within pepper management schemes.

Author contributions

XGJ, BML, and QJW designed the experiment. YZ, JYG, YL, YQW, JH, and YQW performed the experiment. XGJ and YL analyzed the data. YZ, XGJ, JH, and BML wrote the paper. All authors read and approved the manuscript.

Disclosure

The authors declare no conflict of interest.

Ethics statement

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. This article does not contain any studies with human participants performed by any of the authors.

Acknowledgments

We thank Jie Hu and Yaqi Wen for their devotion on the manuscript and providing pepper plants for the experiments. This study was funded by the National Key R & D Program of China (2022YFD1401200) and the National Natural Science Foundation of China (32272552, 32272544, 31371941).

Contributor Information

Baiming Liu, Email: baimingliu@126.com.

Qingjun Wu, Email: wuqingjun@caas.cn.

Xiaoguo Jiao, Email: jiaoxg@hubu.edu.cn.

Data availability statement

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

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