Background: Plant metabolites play vital roles in regulating the behavior of herbivore insects. Virus infection can universally alter plant metabolites to manipulate the orientation and feeding behaviors of insect vector, to favor the transmission of virus. Thus, determining the differentially accumulated metabolites of plant upon virus infection could provide insights into understanding how the triple interactions among plant, virus and insect vector happens. Our previous studies have found that vector whitefly Bemisia tabaci (Gennadius, Hemiptera: Aleyrodidae) showed different orientation behavior and performance on CCYV-infected and healthy cucumber plants. Cucurbit chlorotic yellows virus (CCYV) is exclusively transmitted by B. tabaci in a semi-persistent mode. In this study, we take the CCYV, B. tabaci and cucumber as a research system to explore the functions of phyto-metabolites in the triple interactions. Results: A total of 612 metabolites changed upon CCYV infection were monitored. Metabolites mainly enriched in flavonoids, lipids, nucleotides and their derivatives. At 7 days post CCYV inoculation (dpi), the contents of lipids, terpenoids and flavonoids remarkably decreased, while amino acids, nucleotides and their derivatives notably up-accumulated. At 15 dpi, the accumulation of flavonoids were still significantly reduced upon CCYV infection, while lipids, amino acids, nucleotides and derivatives were remarkably enhanced. Most of significantly increased metabolites were lipids (lysophosphatidylethanolamine, LPE; lysophosphatidylcholine, LPC and their isomers). Also, the number of significantly changed metabolites increased with the infection period. However, only a few organic acids and phenolic acids showed difference between CCYV-infected and healthy cucumber plants. Conclusions: CCYV infection repressed the defensive flavonoids, terpeneoids metabolism but triggered the lipids, amino acids and nucleotides metabolism with the inoculation period. This result suggests that CCYV-infection makes cucumber plants more susceptible for whiteflies attack and CCYV infection. The reduction of defensive comounds and the increase of amino acids may be partially responsible for enhancing feeding preference of whiteflies to CCYV-infected hosts. CCYV may hijacked lipid metabolism for virus replication and assembly.

The bean bug, Riptortus pedestris (Hemiptera: Heteroptera), poses a significant threat to soybean production, resulting in substantial crop losses. Throughout the soybean cultivation period, these insects probe and suck on various parts of plants, including leaves, pods, and beans. However, the specific mechanisms by which they adapt to different food resources remain unknown. In this study, we conducted gut transcriptomic analyses of R. pedestris fed with soybean leaves, pods, and beans. A total of 798, 690, and 548 differently expressed genes (DEGs) were monitored in G—pod vs. G—leaf (comparison of insect feeding on pods and leaves), G—bean vs. G—leaf (comparison of insect feeding on beans and leaves), and G—pod vs. G—bean (comparison of insect feeding on pods and beans), respectively. When fed on pods and beans, there was a significant increase in the expression of digestive enzymes, particularly cathepsins, serine proteases, and lipases. Conversely, when soybean leaves were consumed, detoxification enzymes, such as ABC transporters and 4-coumarate-CoA ligase, exhibited higher expression. Our findings indicate that R. pedestris dynamically regulates different metabolic pathways to cope with varying food resources, which may contribute to the development of effective strategies for managing this pest.

Cucurbit chlorotic yellows virus (CCYV) has caused serious damage to melon crops in many countries in recent years. It is exclusively transmitted by the notorious pest Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) in a semi-persistent manner. Previous studies have shown that both persistently and non-persistently transmitted viruses can manipulate orientation and performance of vector insects through changing host phenotype to facilitate virus spread. However, as a semi-persistently transmitted virus, how CCYV affect vector B. tabaci in locating host plants by altering physiological traits of host plants is still unknown. In this study, we investigated B. tabaci visual and olfactory preference between healthy and CCYV-infected host plant Cucumis sativus. Volatile profiles of healthy and CCYV-infected C. sativus plants were analyzed by using gas chromatography-mass spectrometry (GC-MS). Initially, it was found that vector insects preferred to settle down CCYV-infected Cucumis sativus seedlings in free choice. The concentrations of total volatiles and terpenes in cucumber plants were notably decreased after CCYV infection, and especially, the concentrations of α-pinene, β-ocimene, α-farnesene, and nonanal, responsible for olfactory attraction of B. tabaci, dramatically reduced in CCYV-infected plants. Subsequently, we investigated the visual preference of B. tabaci to CCYV-infected and healthy host, and found that B. tabaci adults showed significant preference to CCYV-infected host. CCYV induced yellowing symptoms in host leaves may explain the visual preference of B. tabaci adults to infected hosts. This study indicated that visual cues could play a vital role in vector insects locating virus-infected host plants.