Citrus yellow vein clearing virus infection in lemon influences host preference of the citrus whitefly by affecting the host metabolite composition

Authors: Sun, Yongduo; Wallis, Christopher; Krugner, Rodrigo; Yokomi, Raymond

Submitted to: Plants
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/16/2025
Publication Date: 1/20/2025
Citation: Sun, Y., Wallis, C.M., Krugner, R., Yokomi, R.K. 2025. Citrus yellow vein clearing virus infection in lemon influences host preference of the citrus whitefly by affecting the host metabolite composition. Plants. 14(2). Article 288. https://doi.org/10.3390/plants14020288.
DOI: https://doi.org/10.3390/plants14020288

Interpretive Summary: Citrus yellow vein clearing virus (CYVCV) is an emerging threat to the citrus industry in California. The virus is known to be transmitted by the citrus whitefly and aphid vectors, but knowledge of plant metabolic changes due to infection and its effects on insect vector settling behaviors is unknown. Experiments showed that CYVCV infection in lemons influenced vector host attraction. Citrus whiteflies preferred to settle on CYVCV-infected lemon plants versus healthy control plants and significantly more citrus whiteflies oriented toward volatile chemical compounds from infected leaves than healthy leaves. Analysis of the chemical composition of plants showed that the amounts of carbohydrates were similar in healthy and CYVCV-infected lemon, while several amino acids and non-volatile phenolic compounds in infected plants differed drastically from healthy plants. In addition, volatile organic compounds known to repel whiteflies decreased significantly in virus-infected plants. Therefore, preference of citrus whiteflies for CYVCV-infected lemon may be due to a reduction of repellent volatile organic compounds. These findings provide valuable insights into the complex behavior of CYVCV vectors that may be useful for developing future management strategies to reduce the spread of CYVCV.

Technical Abstract: Citrus yellow vein clearing virus (CYVCV) is an emerging threat to the citrus industry in California. CYVCV has been reported to be transmitted by citrus whiteflies and aphids. Other plant viruses have been known to alter host metabolites that influence attraction of insect vectors, therefore, we investigated whether CYVCV infection influences vector attractiveness, focusing on the citrus whitefly, Dialeurodes citri. Free choice assays showed that citrus whiteflies exhibited a preference for settling on CYVCV-infected lemon plants versus healthy control plants. Using chromatography techniques, levels of carbohydrates were found to be similar in leaves and stems of both plant groups, while several amino acids in leaf or stem samples and non-volatile phenolic compounds in leaf samples of CYVCV-infected and healthy plants differed drastically. In addition, volatile terpenes/terpenoids decreased significantly in virus-infected plants compared to healthy control. Several of the identified volatile compounds such as a-phellandrene, a-terpinolene, p-cymene, linalool, and citral, show whitefly repellent properties. Y-tube olfactometer bioassays revealed that emissions of volatile organic compounds (VOCs) from infected plants attracted more citrus whiteflies (Dialeurodes citri) than those from healthy plant. In contrast, the CYVCV-induced VOCs changes in lemon trees had no impact on the olfactory response of alate spirea aphids, Aphis spiraecola, suggesting the VOCs released from CYVCV-infected lemon plants may specifically affect citrus whiteflies. Therefore, we suggest that, in addition to the visual cue of yellow vein symptoms, preference of citrus whiteflies settlement on CYVCV-infected lemon plants may also be attributed to a reduction of levels of repellent volatile compounds. These findings provide valuable insights into vector control management strategies aimed at reducing the spread of CYVCV. More research effort is needed to understand the precise role of these compounds in affecting whitefly vector behavior.