Transcriptome of the maize leafhopper (Dalbulus maidis) and its transcriptional response to maize rayado fino virus (MRFV), which it transmits in a persistent, propagative manner

Authors: XU, JUNHUAN - The Ohio State University; Willman, Matthew; Todd, Jane; KIM, KWANG-HO - Rural Development Administration - Korea; REDINBAUGH, MARGARET - The Ohio State University; Stewart, Lucy

Submitted to: Microbiology Spectrum
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/11/2021
Publication Date: 11/24/2021
Citation: Xu, J., Willman, M., Todd, J., Kim, K., Redinbaugh, M.G., Stewart, L.R. 2021. Transcriptome of the maize leafhopper (Dalbulus maidis) and its transcriptional response to maize rayado fino virus (MRFV), which it transmits in a persistent, propagative manner. Microbiology Spectrum. 9:e0061221. https://doi.org/10.1128/Spectrum.00612-21.
DOI: https://doi.org/10.1128/Spectrum.00612-21

Interpretive Summary: The corn leafhopper (Dalbulus maidis) is an important insect pest of corn in the southern United States and central and south America, and also transmits maize rayado fino virus (MRFV), which causes disease in corn. The interaction of the virus and leafhopper that enables virus transmission is highly specific, and MRFV infects the corn leafhopper as well as corn. However, little is known about the molecular biology including genetic sequences of the corn leafhopper, and how exposure to virus alters gene expression, which is important to understand how virus infection and transmission occur. In this work, we developed the first sequence set of expressed genes in the corn leafhopper (the leafhopper's transcriptome) of 56,116 sequences, and identified leafhopper genes that were responsive to MRFV exposure. We identified immunity pathway and other genes in the corn leafhopper, and compared MRFV-responsive genes in the corn leafhopper to genes other viruses regulate in the leafhopper or planthopper species that transmit those viruses. Together, these data provide a scientific groundwork to understand and potentially block the transmission of MRFV by the corn leafhopper, including the sequenced set of expressed genes for the corn leafhopper, and a list of candidate leafhopper genes involved in the MRFV-leafhopper interaction.

Technical Abstract: The corn leafhopper (Dalbulus maidis) is an important vector of maize rayado fino virus (MRFV), a +ssRNA marafivirus which it transmits in a persistent propagative manner. The interaction of D. maidis with MRFV, including infection of the insect and subsequent transmission to new plants, is not well understood at the molecular level. To examine the leafhopper-virus interaction, a D. maidis transcriptome was assembled and differences in transcript abundance between virus-exposed and naïve D. maidis were examined at two time points (4 h and 7 days) post exposure to MRFV. The D. maidis transcriptome contained 56,116 transcripts generated from 1,727,369,026 100 nt paired-end reads from whole adult insects. The transcriptome of D. maidis shared highest identity and most orthologs with the leafhopper, Graminella nigrifrons (65% of transcripts had matches with E-values <10-5) versus planthoppers Sogatella furcifera (with 23% of transcript matches below the E-value cutoff) and Peregrinus maidis (with 21% transcript matches below the E-value cutoff), as expected based on taxonomy. D. maidis expressed genes in the Toll, Imd, and Jak/Stat insect immune signaling pathways, RNAi pathway genes, prophenoloxidase activating system pathways, and immune recognition protein-encoding genes such as peptidoglycan recognition proteins (PGRPs), antimicrobial peptides, and other effectors. Genes expected to be favorable for virus propagation, such as protein synthesis-related genes and genes encoding superoxide dismutase, were significantly upregulated after MRFV exposure. Genes encoding splicing factor, small nuclear ribonucleoprotein and ribosomal proteins were also significantly upregulated in response to MRFV exposure in D. maidis. IMPORTANCE: The transcriptome of the corn leafhopper, D. maidis revealed conserved biochemical pathways for immunity and discovered transcripts responsive to MRFV-infected plants at two time points, providing a basis for functional identification genes that either limit or promote the virus-vector interaction. Compared to other hopper species and the propagative plant viruses they transmit, D. maidis shared responsive transcripts with S. furcifera (to southern rice black-streaked dwarf virus, SRBSDV) and to G nigrifrons (to maize fine streak virus, MFSV), and one with P. maidis (to maize mosaic virus, MMV), but no virus-responsive transcripts identified were shared among all four hopper vector species