Comparative transcriptomics of Diuraphis noxia and Schizaphis graminum fed wheat plants containing different aphid-resistance genes

Authors: ROJAS, LINA AGUIRRE - Kansas State University; Scully, Erin; ENDERS, LARAMY - Purdue University; TIMM, ALICIA - Colorado State University; SINHA, DEEPAK - Sage University; SMITH, C. MICHAEL - Kansas State University

Submitted to: PLOS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/11/2020
Publication Date: 5/22/2020
Citation: Rojas, L., Scully, E.D., Enders, L., Timm, A.E., Sinha, D.K., Smith, C. 2020. Comparative transcriptomics of Diuraphis noxia and Schizaphis graminum fed wheat plants containing different aphid-resistance genes. PLoS One. 15(5):e0233077. https://doi.org/10.1371/journal.pone.0233077.
DOI: https://doi.org/10.1371/journal.pone.0233077

Interpretive Summary: The mechanisms by which aphids overcome plant resistance is not known in many cases. Bread wheat (Triticum aestivum) L. is routinely attacked by several aphid pests, including greenbug (Schizaphis graminum; GB) and Russian wheat aphid (Diuraphis noxia; RWA); however, wheat plants containing the Dn4 gene have resistance against some populations of RWA, but no resistance to GB, while wheat containing the Dn7 gene has resistance to both aphid species. The purposes of this study were to study changes in gene expression in GB and RWA in response to feeding on wheat plants containing no resistance genes (Dn0), resistance against RWA (Dn4), or resistance against both aphids (Dn7). Feeding on Dn4 had few effects on gene expression in GB, but upregulation of numerous detoxification genes was observed in RWA suggesting that plant defensive chemicals produced by Dn4 plants might be responsible for its resistance to RWA and that GB may have evolved mechanisms to detoxify these compounds. In contrast, feeding on Dn7 had extensive effects on gene expression of both aphid species with GB upregulating genes for DNA and protein repair and RWA upregulating genes for detoxification and nutrient acquisition. This finding indicates that even though a single locus translocated from rye into wheat is responsible for resistance to both GB and RWA in Dn7 plants, the mechanisms of resistance to GB and RWA are likely different and are probably encoded by different rye genes. Overall, this study shows that, in some wheat cultivars, cross-resistance to multiple insect pests may be due to different genes and that care should be taken to screen for resistance to multiple aphid species when Dn7 is used in wheat breeding programs.

Technical Abstract: The molecular bases of aphid virulence to aphid crop plant resistance genes are poorly understood. The Russian wheat aphid, Diuraphis noxia, (Kurdjumov), and the greenbug, Schizaphis graminum Rondani, are global pest of cereal crops. Each species damages barley, oat, rye and wheat, but S. graminum includes fescue, maize, rice and sorghum in its host range. This study was conducted to compare and contrast the transcriptomes of S. graminum biotype I and D. noxia biotype 1 when each ingested phloem from leaves of varieties of bread wheat, Triticum aestivum L., containing no aphid resistance (Dn0), resistance to D. noxia biotype 1 (Dn4), or resistance to both D. noxia biotype 1 and S. graminum biotype I (Dn7). Gene ontology enrichments, k-means analysis and KEGG pathway analysis indicated that plants containing the Dn7 gene from rye had stronger effects on the global transcriptional profiles of S. graminum and D. noxia relative to those fed Dn4 plants. S. graminum responds to ingestion of phloem sap from Dn7 plants by expression of unigenes coding for proteins involved in DNA and RNA repair, and delayed tissue and structural development. In contrast, D. noxia displays a completely different transcriptome after ingesting phloem sap from Dn4 or Dn7 plants, consisting of unigenes involved primarily in detoxification, nutrient acquisition and structural development. These variations in transcriptional responses of D. noxia and S. graminum suggest that the underlying evolutionary mechanism(s) of virulence in these aphids are likely species specific, even in cases where the Dn7 gene exhibits some level of cross resistance.