Dataset Information

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

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, wheat genotype 94M370). Gene ontology enrichments, k-means analysis and KEGG pathway analysis indicated that 94M370 plants containing the Dn7 D. noxia resistance 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 94M370 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 94M370 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 of cross resistance.

SUBMITTER: Rojas LA

PROVIDER: S-EPMC7313535 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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

Rojas Lina Aguirre LA Scully Erin E Enders Laramy L Timm Alicia A Sinha Deepak D Smith Charles Michael CM

PloS one 20200522 5

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 phlo ...[more]

PMID: 32442185

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Project description:BACKGROUND:Schizaphis graminum is one of the most important and devastating cereal aphids worldwide, and its feeding can cause chlorosis and necrosis in wheat. However, little information is available on the wheat defence responses triggered by S. graminum feeding at the molecular level. RESULTS:Here, we collected and analysed transcriptome sequencing data from leaf tissues of wheat infested with S. graminum at 2, 6, 12, 24 and 48?hpi (hours post infestation). A total of 44,835 genes were either up- or downregulated and differed significantly in response to aphid feeding. The expression levels of a number of genes (9761 genes) were significantly altered within 2 hpi and continued to change during the entire 48?h experiment. Gene Ontology analysis showed that the downregulated DEGs were mainly enriched in photosynthesis and light harvesting, and the total chlorophyll content in wheat leaves was also significantly reduced after S. graminum infestation at 24 and 48?hpi. However, a number of related genes of the salicylic acid (SA)-mediated defence signalling pathway and MAPK-WRKY pathway were significantly upregulated at early feeding time points (2 and 6 hpi). In addition, the gene expression and activity of antioxidant enzymes, such as peroxidase and superoxide dismutase, were rapidly increased at 2, 6 and 12 hpi. DAB staining results showed that S. graminum feeding induced hydrogen peroxide (H2O2) accumulation at the feeding sites at 2 hpi, and increased H2O2 production was detected with the increases in aphid feeding time. Pretreatment with diphenylene iodonium, an NADPH oxidase inhibitor, repressed the H2O2 accumulation and expression levels of SA-associated defence genes in wheat. CONCLUSIONS:Our transcriptomic analysis revealed that defence-related pathways and oxidative stress in wheat were rapidly induced within hours after the initiation of aphid feeding. Additionally, NADPH oxidase plays an important role in aphid-induced defence responses and H2O2 accumulation in wheat. These results provide valuable insight into the dynamic transcriptomic responses of wheat leaves to phytotoxic aphid feeding and the molecular mechanisms of aphid-plant interactions.

Project description:BACKGROUND:Infestation of the phytotoxic aphid Schizaphis graminum can rapidly induce leaf chlorosis in susceptible plants, but this effect is not observed with the nonphytotoxic aphid Sitobion avenae. However, few studies have attempted to identify the different defence responses induced in wheat by S. graminum and S. avenae feeding and the mechanisms underlying the activation of chlorosis by S. graminum feeding. RESULTS:S. graminum feeding significantly reduced the chlorophyll content of wheat leaves, and these effects were not observed with S. avenae. A transcriptomic analysis showed that the expression levels of genes involved in the salicylic acid, jasmonic acid and ethylene signalling defence pathways were significantly upregulated by both S. avenae and S. graminum feeding; however, more plant defence genes were activated by S. graminum feeding than S. avenae feeding. The transcript levels of genes encoding cell wall-modifying proteins were significantly increased after S. graminum feeding, but only a few of these genes were induced by S. avenae. Furthermore, various reactive oxygen species-scavenging genes, such as 66 peroxidase (POD) and 8 ascorbate peroxidase (APx) genes, were significantly upregulated after S. graminum feeding, whereas only 15 POD and one APx genes were induced by S. avenae feeding. The activity of four antioxidant enzymes was also significantly upregulated by S. graminum feeding. Cytological examination showed that S. graminum feeding induced substantial hydrogen peroxide (H2O2) accumulation in wheat leaves. The chlorosis symptoms and the loss of chlorophyll observed in wheat leaves after S. graminum feeding were reduced and inhibited by the scavenging of H2O2 by dimethylthiourea, which indicated that H2O2 plays important role in the induction of chlorosis by S. graminum feeding. CONCLUSIONS:S. graminum and S. avenae feeding induces the JA, SA and ET signalling pathways, but S. graminum activated stronger plant defence responses than S. avenae. S. graminum feeding triggers strong ROS-scavenging activity and massive H2O2 production in wheat leaves, and the accumulation of H2O2 induced by S. graminum feeding is involved in the activation of chlorosis in wheat leaves. These results enhance our understanding of mechanisms underlying aphid-wheat interactions and provide clues for the development of aphid-resistant wheat varieties.

Project description:BackgroundThe Russian wheat aphid, Diuraphis noxia Kurdjumov, is one of the most important pests of small grains throughout the temperate regions of the world. This phytotoxic aphid causes severe systemic damage symptoms in wheat, barley, and other small grains as a direct result of the salivary proteins it injects into the plant while feeding.ResultsWe sequenced and de novo assembled the genome of D. noxia Biotype 2, the strain most virulent to resistance genes in wheat. The assembled genomic scaffolds span 393 MB, equivalent to 93% of its 421 MB genome, and contains 19,097 genes. D. noxia has the most AT-rich insect genome sequenced to date (70.9%), with a bimodal CpG(O/E) distribution and a complete set of methylation related genes. The D. noxia genome displays a widespread, extensive reduction in the number of genes per ortholog group, including defensive, detoxification, chemosensory, and sugar transporter groups in comparison to the Acyrthosiphon pisum genome, including a 65% reduction in chemoreceptor genes. Thirty of 34 known D. noxia salivary genes were found in this assembly. These genes exhibited less homology with those salivary genes commonly expressed in insect saliva, such as glucose dehydrogenase and trehalase, yet greater conservation among genes that are expressed in D. noxia saliva but not detected in the saliva of other insects. Genes involved in insecticide activity and endosymbiont-derived genes were also found, as well as genes involved in virus transmission, although D. noxia is not a viral vector.ConclusionsThis genome is the second sequenced aphid genome, and the first of a phytotoxic insect. D. noxia's reduced gene content of may reflect the influence of phytotoxic feeding in shaping the D. noxia genome, and in turn in broadening its host range. The presence of methylation-related genes, including cytosine methylation, is consistent with other parthenogenetic and polyphenic insects. The D. noxia genome will provide an important contrast to the A. pisum genome and advance functional and comparative genomics of insects and other organisms.

Dataset Information

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

Publications

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

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