Abstract
BackgroundInsects are the most important epidemiological factors for plant virus disease spread, with >75% of viruses being dependent on insects for transmission to new hosts. The black-faced leafhopper (Graminella nigrifrons Forbes) transmits two viruses that use different strategies for transmission: Maize chlorotic dwarf virus (MCDV) which is semi-persistently transmitted and Maize fine streak virus (MFSV) which is persistently and propagatively transmitted. To date, little is known regarding the molecular and cellular mechanisms in insects that regulate the process and efficiency of transmission, or how these mechanisms differ based on virus transmission strategy.ResultsRNA-Seq was used to examine transcript changes in leafhoppers after feeding on MCDV-infected, MFSV-infected and healthy maize for 4 h and 7 d. After sequencing cDNA libraries constructed from whole individuals using Illumina next generation sequencing, the Rnnotator pipeline in Galaxy was used to reassemble the G. nigrifrons transcriptome. Using differential expression analyses, we identified significant changes in transcript abundance in G. nigrifrons. In particular, transcripts implicated in the innate immune response and energy production were more highly expressed in insects fed on virus-infected maize. Leafhoppers fed on MFSV-infected maize also showed an induction of transcripts involved in hemocoel and cell-membrane linked immune responses within four hours of feeding. Patterns of transcript expression were validated for a subset of transcripts by quantitative real-time reverse transcription polymerase chain reaction using RNA samples collected from insects fed on healthy or virus-infected maize for between a 4 h and seven week period.ConclusionsWe expected, and found, changes in transcript expression in G. nigrifrons feeding of maize infected with a virus (MFSV) that also infects the leafhopper, including induction of immune responses in the hemocoel and at the cell membrane. The significant induction of the innate immune system in G. nigrifrons fed on a foregut-borne virus (MCDV) that does not infect leafhoppers was less expected. The changes in transcript accumulation that occur independent of the mode of pathogen transmission could be key for identifying insect factors that disrupt vector-mediated plant virus transmission.
Highlights
Insects are the most important epidemiological factors for plant virus disease spread, with >75% of viruses being dependent on insects for transmission to new hosts
The most economically significant insect vectors of plant viruses are restricted to a few hemipteran families, including leafhoppers (Cicadellidae) [51]
Comparison of the responses of the leafhopper, G. nigrifrons, to feeding on maize infected with two different viruses uncovered similarities as well as clear differences in the transcriptional responses in the vector that may provide some mechanistic insight
Summary
Insects are the most important epidemiological factors for plant virus disease spread, with >75% of viruses being dependent on insects for transmission to new hosts. Non-persistentlytransmitted and semi-persistently-transmitted viruses do not breach the gut barrier in the insect vector; rather they are retained in the insect stylet or foregut prior to transmission. Because of their location outside of insect cells and the few barriers they must cross prior to introduction into a new plant host, these viruses can be transmitted within seconds to hours after acquisition. Transmitted viruses are divided into two categories: circulative viruses that are able to cross the gut barriers and circulate in the insect hemolymph, but do not replicate in the insect vector; and, propagative viruses that circulate in and replicate in the vector Because these viruses must cross several molecular and physical barriers in the insect and require a latency period between acquisition and transmission, their transmission requires days to weeks. Because non- and semi-persistently transmitted viruses interact only briefly with the vector, and do not cross vector membranes, we hypothesized that the genetic and molecular responses of the vector to these viruses are likely to be substantially different and perhaps less diverse than those of the vector to persistently transmitted plant viruses
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