The majority of plant viruses are transmitted by insect vectors between hosts, and transovarial transmission of viruses from vector parents to offspring has great significance to their epidemiology. Begomoviruses are transmitted by the whitefly Bemisia tabaci in a circulative manner and are maintained through a plant–insect–plant cycle. Other routes of begomovirus transmission are not clearly known. Here, we report that transovarial transmission from female whiteflies to offspring often happens for one begomovirus, Tomato yellow leaf curl virus (TYLCV), and may have contributed significantly to its global spread. We found that TYLCV entry of the reproductive organ of its vector mainly depended on the developmental stage of the whitefly ovary, and the transovarial transmission of TYLCV to offspring increased with whitefly adult age. The specific interaction between virus coat protein (CP) and whitefly vitellogenin (Vg) was vital for virus entry into whitefly ovary. When knocking down the expression of Vg, the entry of TYLCV into ovary was inhibited and the transovarial transmission efficiency decreased. In contrast, another begomovirus, Papaya leaf curl China virus (PaLCuCNV), CP did not interact with whitefly Vg, and PaLCuCNV could not be transovarially transmitted by whiteflies. We further showed that TYLCV could be maintained for at least two generations in the absence of virus-infected plants, and the adult progenies were able to infect healthy plants in both the laboratory and field. This study reports the transovarial transmission mechanism of begomoviruses, and it may help to explain the evolution and global spread of some begomoviruses. Significance The majority of plant viruses are transmitted by insect vectors. Transovarial transmission of virus from female vectors to offspring can be very important in maintaining a source of infection and therefore has great epidemiological relevance. Identification of vector and virus components involved in transovarial transmission can lead to new strategies to combat virus spread. Here, we found that the specific interaction between viral coat protein and vector vitellogenin determines transovarial transmissibility of begomoviruses, which have caused great damage to agricultural production and are generally believed not to be transovarially transmitted by insect vectors. Our study gives valuable clues for designing strategies to block begomovirus transmission and provides insights into the evolution and global spread of begomoviruses.

Whereas most of the arthropod-borne animal viruses replicate in their vectors, this is less common for plant viruses. So far, only some plant RNA viruses have been demonstrated to replicate in insect vectors and plant hosts. How plant viruses evolved to replicate in the animal kingdom remains largely unknown. Geminiviruses comprise a large family of plant-infecting, single-stranded DNA viruses that cause serious crop losses worldwide. Here, we report evidence and insight into the replication of the geminivirus tomato yellow leaf curl virus (TYLCV) in the whitefly (Bemisia tabaci) vector and that replication is mainly in the salivary glands. We found that TYLCV induces DNA synthesis machinery, proliferating cell nuclear antigen (PCNA) and DNA polymerase δ (Polδ), to establish a replication-competent environment in whiteflies. TYLCV replication-associated protein (Rep) interacts with whitefly PCNA, which recruits DNA Polδ for virus replication. In contrast, another geminivirus, papaya leaf curl China virus (PaLCuCNV), does not replicate in the whitefly vector. PaLCuCNV does not induce DNA-synthesis machinery, and the Rep does not interact with whitefly PCNA. Our findings reveal important mechanisms by which a plant DNA virus replicates across the kingdom barrier in an insect and may help to explain the global spread of this devastating pathogen. Significance Viruses pose a great threat to animal and plant health worldwide. Whereas most plant viruses only replicate in plant hosts, some also replicate in their animal (insect) vector. A detailed knowledge of host expansion will give a better understanding of virus evolution, and identification of virus and host components involved in this process can lead to new strategies to combat virus spread. Here, we reveal that a plant DNA virus has evolved to induce and recruit insect DNA synthesis machinery to support its replication in vector salivary glands. Our study sheds light on the understanding of TYLCV–whitefly interactions and provides insights into how a plant virus may evolve to infect and replicate in an insect vector.

The cryptic species Middle East-Asia Minor 1 (MEAM1), formerly referred to as ‘B biotype’, of the whitefly Bemisia tabaci complex entered China in the mid 1990s, and the Mediterranean (MED) cryptic species, formerly referred to as ‘Q biotype’, of the same whitefly complex entered China around 2003. Field surveys in China after 2003 indicate that in many regions MED has been replacing the earlier invader MEAM1. The factors underlying this displacement are unclear. We conducted laboratory experiments and field sampling to examine the effects of insecticide application on the competitive interactions between MEAM1 and MED. In the laboratory, on cotton, a plant showing similar levels of suitability to both whitefly species, MEAM1 displaced MED in five generations when initial populations of the two species were equal and no insecticide was applied. In contrast, MED displaced MEAM1 in seven and two generations, respectively, when 12.5 and 50.0 mg l⁻¹ imidacloprid was applied to the plants via soil drench. Field sampling indicated that in a single season MED displaced MEAM1 on crops heavily sprayed with neonicotinoid insecticides but the relative abundance of the two species changed little on crops without insecticide spray. We also examined the effects of host plants on the competitive interactions between the two species in the laboratory. When cohorts with equal abundance of MEAM1 and MED were set up on different host plants, MEAM1 displaced MED on cabbage and tomato in five and seven generations, respectively, but MED displaced MEAM1 on pepper in two generations. As field populations of MED have lower susceptibility than those of MEAM1 to nearly all commonly used insecticides including imidacloprid, insecticide application seems to have played a major role in shifting the species competitive interaction effects in favour of MED in the field across China. Host plants may also shape competition between the two species depending on the relative levels of plant suitability.

Begomoviruses are transmitted by cryptic species of the whitefly Bemisia tabaci complex, often in a species-specific manner. Papaya leaf curl China virus (PaLCuCNV) has been recorded to infect several crops including papaya, tomato and tobacco in China. To help assess the risks of spread of this virus, we compared the acquisition, retention and transmission of PaLCuCNV among four species of whiteflies, Middle East-Asia Minor 1 (MEAM1), Mediterranean (MED), Asia 1 and Asia II 7. All four species of whiteflies are able to acquire, retain and transmit the virus, but with different levels of efficiency. Transmission tests using tomato as the host plant showed that MEAM1 transmitted PaLCuCNV with substantially higher efficiency than did MED, Asia 1 and Asia II 7. Furthermore, accumulation of PaLCuCNV in the whiteflies was positively associated with its efficiency of transmitting the virus. Altogether, these findings indicate that MEAM1 is the most efficient vector for PaLCuCNV in the four species of whiteflies and suggest that risks of PaLCuCNV pandemics are high in regions where MEAM1 occurs.

Summary: Herbivore attack induces plants to mobilize chemical defences, including the release of volatiles that attract natural enemies of the herbivore. This commonly involves the jasmonic acid (JA) pathway. However, phloem‐feeding whiteflies specifically trigger salicylic acid (SA)‐signalling, thereby suppressing JA‐based defences and enhancing host plant suitability. Here, we show with Arabidopsis thaliana plants that the whitefly parasitoid Encarsia formosa outsmarts this apparent host plant manipulation by exploiting the SA‐triggered emission of β‐myrcene. Assays with various Arabidopsis mutants and phytohormone and gene‐expression analyses reveal that the whiteflies induce the accumulation of endogenous SA, thereby enhancing the expression of SA‐regulated genes, one of which encodes ocimene/myrcene synthase, which resulted in the recruitment of parasitoids under greenhouse conditions. Performance assays confirmed that whiteflies directly benefit from suppressing JA‐based defences. Taken together, we conclude that by activating SA‐signalling whitefly feeding suppresses direct, JA‐based defences, but that parasitoids can adapt to this by exploiting specific, SA‐induced volatile emissions for host location. Our work further confirms that herbivory contributes to selective pressure governing the evolution of inducible volatile signals as indirect plant defences.