Transcriptome analysis reveals rapid defence responses in wheat induced by phytotoxic aphid Schizaphis graminum feeding

Abstract

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 (9,761 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 (H 2 O 2 ) accumulation at the feeding sites at 2 hpi, and increased H 2 O 2 production was detected with the increases in aphid feeding time. Pretreatment with diphenylene iodonium, an NADPH oxidase inhibitor, repressed the H 2 O 2 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 H 2 O 2 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.

Transcriptomic and Metabolomic Responses of Rice Plants to Cnaphalocrocis medinalis Caterpillar Infestation

“…Our transcriptomic analysis provided molecular evidence that the downregulated genes induced by C. medinalis feeding were significantly enriched in photosynthesis-related GO terms, such as “photosynthesis”, “photosynthesis, light reaction”, “photosynthesis, light harvesting”, and “response to light stimulus”, and also in KEGG terms, including “photosynthesis” and “photosynthesis-antenna proteins”. Similar results also were reported in wheat, in which genes involved in photosynthesis, such as asribulose-1,5-bisphosphate carboxylase and chlorophyll A-B binding protein, were significantly downregulated by feeding of the greenbug Schizaphis graminum [ 48 ]. In plants, the downregulation of the photosynthetic apparatus could protect them from oxidative damage [ 49 ].…”

Transcriptional profiling reveals a critical role of GmFT2a in soybean staygreen syndrome caused by the pest Riptortus pedestris

“…Phytohormones, especially JA and SA pathways, are important signaling molecules in response to insect attack (Li et al ., 2006; Yates & Michel, 2018). The expression of SA‐ and JA‐related defense genes, such as LOX , FAD , PAL , and PR1 , is significantly induced when piercing–sucking insects, such as aphids and bugs, feed (Reddy et al ., 2013; Zhang et al ., 2020; H. Zhang et al ., 2022; Y. Zhang et al ., 2022). In addition, WRKY TFs, as important components in MAPK signaling pathways, are also significantly upregulated in response to insect feeding (Li et al ., 2012; Zhang et al ., 2020).…”

“…The expression of SA‐ and JA‐related defense genes, such as LOX , FAD , PAL , and PR1 , is significantly induced when piercing–sucking insects, such as aphids and bugs, feed (Reddy et al ., 2013; Zhang et al ., 2020; H. Zhang et al ., 2022; Y. Zhang et al ., 2022). In addition, WRKY TFs, as important components in MAPK signaling pathways, are also significantly upregulated in response to insect feeding (Li et al ., 2012; Zhang et al ., 2020). Similarly, insects have developed various strategies to adapt to their host plants.…”

The salivary effector protein Sg2204 in the greenbug Schizaphis graminum suppresses wheat defence and is essential for enabling aphid feeding on host plants

“…In addition, the plant defence hormones JA and SA are important signalling molecules conferring plant resistance against aphids (Li et al ., 2006; Yates and Michel, 2018; Züst and Agrawal, 2016). The expression levels of genes involved in both the JA‐ and SA‐dependent defence pathways of wheat, such as LOX , FAD , PAL and PR1 , are significantly up‐regulated in response to S. graminum infestation (Reddy et al ., 2013; Zhang et al ., 2020; Zhu‐Salzman et al ., 2004). Exogenous application of SA and JA on Arabidopsis , wheat, tomato and Brassica plants had negative effects on aphid population growth (Ali et al ., 2021; Boughton et al ., 2006; Bruce et al ., 2003; Feng et al ., 2021).…”

“…In contrast to most other aphid species, S. graminum is a phytotoxic aphid, and its feeding can rapidly induce obvious leaf chlorosis in susceptible plants, resulting in the deterioration of plant quality and even plant death (Al‐Mousawi et al ., 1983; Blackman and Eastop, 2000; Nicholson and Puterka, 2014; Zhang et al ., 2019). A previous study showed that induced hydrogen peroxide accumulation is predicted to be involved in the induction of chlorosis symptoms by S. graminum feeding (Zhang et al ., 2020). As global warming continues, the potential risk of S. graminum infestation will increase, especially in the Northern Hemisphere, which could increase global food insecurity and poverty by invading economically important crops (Aljaryian and Kumar, 2016).…”