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Gut-Expressed Vitellogenin Facilitates the Movement of a Plant Virus across the Midgut Wall in Its Insect Vector.

ABSTRACT: Many viral pathogens of global importance to plant and animal health are persistently transmitted by insect vectors. Midgut of insects forms the first major barrier that these viruses encounter during their entry into the vectors. However, the vector ligand(s) involved in the movement of plant viruses across the midgut barrier remains largely uncharacterized. Begomoviruses, many of which are disease agents of some major crops worldwide, are persistently transmitted by whiteflies (Bemisia tabaci). Here, in order to identify whitefly midgut proteins that interact with a devastating begomovirus, tomato yellow leaf curl virus (TYLCV), we performed midgut-specific TYLCV coat protein (CP) immunoprecipitation followed by high-throughput mass spectrometry proteomic analysis. We find that vitellogenin (Vg), a critical insect reproductive protein that has been considered to be synthesized by the fat body, is also synthesized by and interacts with TYLCV CP in the whitefly midgut. TYLCV appears to be internalized into midgut epithelial cells as a complex with Vg through endocytosis. Virus-containing vesicles then deliver the virus-Vg complexes to early endosomes for intracellular transport. Systematic silencing of Vg or midgut-specific immune blocking of Vg inhibited virus movement across the midgut wall and decreased viral acquisition and transmission by whitefly. Our findings show that a functional Vg protein is synthesized in the midgut of an insect and suggest a novel Vg mechanism that facilitates virus movement across the midgut barrier of its insect vector. IMPORTANCE An essential step in the life cycle of many viruses is transmission to a new host by insect vectors, and one critical step in the transmission of persistently transmitted viruses is overcoming the midgut barrier to enter vectors and complete their cycle. Most viruses enter vector midgut epithelial cells via specific interaction between viral structural proteins and vector cell surface receptor complexes. Tomato yellow leaf curl virus (TYLCV) is persistently transmitted by the whitefly Bemisia tabaci between host plants. Here, we find that TYLCV coat protein interacts with vitellogenin (Vg) in the whitefly midgut. This interaction is required for the movement of the virus crossing the midgut wall and thus facilitates viral acquisition and transmission by whitefly. This study reveals a novel mechanism of virus overcoming the insect midgut barrier and provides new insights into the function of Vg beyond serving as nutrition for developing embryos in insects.

SUBMITTER: He YZ

PROVIDER: S-EPMC8269243 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Autophagy plays an important role against pathogen infection in many organisms; however, little has been done with regard to vector-borne plant and animal pathogens, that sometimes replicate and cause deleterious effects in their vectors. Candidatus Liberibacter solanacearum (CLso) is a fastidious gram-negative phloem-restricted plant pathogen and vectored by the carrot psyllid, Bactericera trigonica. The plant disease caused by this bacterium is called carrot yellows and has recently gained much importance due to worldwide excessive economical losses. Here, we demonstrate that calcium ATPase, cytosolic calcium, and most importantly Beclin-1 have a role in regulating autophagy and its association with Liberibacter inside the psyllid. The presence of CLso generates reactive oxygen species and induces the expression of detoxification enzymes in the psyllid midguts, a main site for bacteria transmission. CLso also induces the expression of both sarco/endoplasmic reticulum Ca2+pump (SERCA) and 1,4,5-trisphosphate receptors (ITPR) in midguts, resulting in high levels of calcium in the cellular cytosol. Silencing these genes individually disrupted the calcium levels in the cytosol and resulted in direct effects on autophagy and subsequently on Liberibacter persistence and transmission. Inhibiting Beclin1-phosphorylation through different calcium-induced kinases altered the expression of autophagy and CLso titers and persistence. Based on our results obtained from the midgut, we suggest the existence of a direct correlation between cytosolic calcium levels, autophagy, and CLso persistence and transmission by the carrot psyllid. IMPORTANCE Plant diseases caused by vector-borne Liberibacter species are responsible for the most important economic losses in many agricultural sectors. Preventing these diseases relies mostly on chemical sprays against the insect vectors. Knowledge-based interference with the bacteria-vector interaction remains a promising approach as a sustainable solution. For unravelling how Liberibacter exploits molecular pathways in its insect vector for transmission, here, we show that the bacterium manipulates calcium levels on both sides of the endoplasmic reticulum membrane, resulting in manipulating autophagy. Silencing genes associated with these pathways disrupted the calcium levels in the cytosol and resulted in direct effects on autophagy and Liberibacter transmission. These results demonstrate major pathways that could be exploited for manipulating and controlling the disease transmission.

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Gut-Expressed Vitellogenin Facilitates the Movement of a Plant Virus across the Midgut Wall in Its Insect Vector.

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