Abstract
BackgroundInfestation 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.ResultsS. 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.ConclusionsS. 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.
Highlights
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
Damage symptoms and changes in the chlorophyll content of wheat leaves after S. avenae and S. graminum feeding As shown in Fig. 1a-c, no obvious damage symptoms were detected in leaves 48 h after S. avenae infestation compared with leaves without aphid infestation, whereas S. graminum feeding caused severe chlorosis in wheat leaves
We found that more than 20,000 genes were significantly regulated in wheat infested with S. graminum, but only 1700 genes were significantly modulated after 48 h of S. avenae feeding, which indicated that the physiological changes induced by S. graminum are notably different from those induced by S. avenae and that various metabolic pathways are involved in the development of damage caused by S. graminum feeding
Summary
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. 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. Plants can perceive damage-associated molecular patterns (DAMPs) or herbivory-associated molecular patterns (HAMPs) in insect oral secretions and subsequently induce direct and indirect plant defence responses [1, 2]. Leaf-eating beetles (Coleoptera) or caterpillars (Lepidoptera) cause extensive tissue damage during herbivory, which usually activates the jasmonic acid (JA)mediated defence pathway in plants [9, 10]. Different from leaf chewing insects, hemipterans, such as aphids and whiteflies, have highly modified piecing-sucking mouthparts (stylets) that can penetrate the extracellular pathway and feed on the nutrients from phloem sap provided by sieve elements (SEs). Many studies have demonstrated that hemipteran feeding results in the induction of the salicylic acid (SA)-dependent defence pathway in plants [12, 13]
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