The molecular mechanism of efficient transmission of plant viruses in variable virus–vector–plant interactions

Plant viruses are mainly transmitted by insect vectors in the non-persistent, semi-persistent, or persistent modes. In the non-persistent mode, plant viruses are retained in the stylets of their insect vectors. In the semi-persistent mode, plant viruses are carried to vector foreguts or salivary glands, but they cannot spread to salivary glands. In the persistent mode, plant viruses are retained in vector guts and can spread to salivary glands. In the non-persistent and semi-persistent modes, plant viruses are retained for a short time and cannot enter the hemolymph of insect vectors, whereas in the persistent mode, plant viruses are retained for a relatively long time and can be found in the hemolymph. Here, we reviewed recent studies that uncovered molecular mechanisms of how plant viruses manipulate host traits for efficient transmission by insect vectors. Normally, plants that are infected with viruses, regardless of the transmission mode, tend to release more attractive volatiles to vectors. However, plant defensive systems are regulated differently by viruses in these three modes. In the non-persistent mode, virus infections significantly induce plant defense responses, which probably trigger vectors (e.g., winged aphids) to disperse and transmit viruses in a short time. In the semi-persistent mode, virus infections frequently suppress plant defense responses, resulting in an increase of vector population and facilitating viral transmissions during vector outbreaks. In the persistent mode, virus infections reduce plant defense responses and manipulate plant traits to become suitable feeding sites in a relatively long period of time. Understanding the underlying mechanisms of virus–vector–plant interactions will lay a foundation for preventing virus transmission.