Abstract
Rice stripe virus (RSV, genus Tenuivirus, family Phenuiviridae) is the causal agent of rice stripe disease transmitted by the small brown planthopper (SBPH, Laodelphax striatellus) in a persistent propagative manner. The midgut and salivary glands of SBPH are the first and last barriers to the viral circulation and transmission processes, respectively; however, the precise mechanisms used by RSV to cross these organs and transmit to rice plants have not been fully elucidated. We obtained the full-length cDNA sequence of L. striatellus α-tubulin 2 (LsTUB) and found that RSV infection increased the level of LsTUB in vivo. Furthermore, LsTUB was shown to co-localize with RSV nonstructural protein 3 (NS3) in vivo and bound NS3 at positions 74–76 and 80–82 in vitro. Transient gene silencing of LsTUB expression caused a significant reduction in detectable RSV loads and viral NS3 expression levels, but had no effect on NS3 silencing suppressor activity and viral replication in insect cells. However, suppression of LsTUB attenuated viral spread in the bodies of SBPHs and decreased RSV transmission rates to rice plants. Electrical penetration graphs (EPG) showed that LsTUB knockdown by RNAi did not impact SBPH feeding; therefore, the reduction in RSV transmission rates was likely caused by a decrease in viral loads inside the planthopper. These findings suggest that LsTUB mediates the passage of RSV through midgut and salivary glands and leads to successful horizontal transmission.
Highlights
The survival of plant viruses is largely dependent on the efficient transmission to plant hosts by virus-specific vectors [1, 2]
Over 70% of all known plant viruses are transmitted by specific arthropods, mainly including planthoppers, leafhoppers, aphids and whiteflies
Plant viruses with persistent relationships must overcome multiple barriers
Summary
The survival of plant viruses is largely dependent on the efficient transmission to plant hosts by virus-specific vectors [1, 2]. Over 70% of all known plant viruses are transmitted by insects, and approximately 55% are vectored by Hemipteran insects (e.g. leafhoppers, planthoppers, aphids and whiteflies) [3]. These insects have distinctive piercing-sucking mouthparts with needle-like stylet bundles that are comprised of two maxillary and two mandibular stylets, making insect more suitable for virus transmission [3,4,5]. Barriers to the persistent transmission of plant viruses in insect vectors include the following: (i) midgut infection barriers; (ii) dissemination barriers, including midgut escape and salivary gland infection barriers; (iii) salivary gland escape barriers; and (iv) transovarial transmission barriers [8, 9]. A deeper understanding of the mechanistic basis of virus transmission through these four barriers will facilitate the development of novel methods to control the systemic spread of plant viruses
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