Whole-body transcriptome mining for candidate effectors from Diuraphis noxia

Abstract

Background Proteins within aphid saliva play a crucial role as the molecular interface between aphids and their host plants. These salivary effectors modulate plant responses to favour aphid feeding and facilitate infestation. The identification of effectors from economically important pest species is central in understanding the molecular events during the aphid-plant interaction. The Russian wheat aphid (Diuraphis noxia, Kurdjumov) is one such pest that causes devastating losses to wheat and barley yields worldwide. Despite the severe threat to food security posed by D. noxia, the non-model nature of this pest and its host has hindered progress towards understanding this interaction. In this study, in the absence of a salivary gland transcriptome, whole-body transcriptomics data was mined to generate a candidate effector catalogue for D. noxia. Results Mining the transcriptome identified 725 transcripts encoding putatively secreted proteins amongst which were transcripts specific to D. noxia. Six of the seven examined D. noxia putative effectors, termed DnE’s (Diuraphis noxia effectors) exhibited salivary gland-specific expression. A comparative analysis between whole-body D. noxia transcriptome data versus the head and body transcriptomes from three other aphid species allowed us to define a catalogue of transcripts putatively upregulated in D. noxia head tissue. Five of these were selected for RT-qPCR confirmation, and were found to corroborate the differential expression predictions, with a further three confirmed to be highly expressed in D. noxia salivary gland tissue. Conclusions Determining a putative effector catalogue for D. noxia from whole-transcriptome data, particularly the identification of salivary-specific sequences potentially unique to D. noxia, provide the basis for future functional characterisation studies to gain further insight into this aphid-plant interaction. Furthermore, due to a lack of publicly available aphid salivary gland transcriptome data, the capacity to use comparative transcriptomics to compile a list of putative effector candidates from whole-body transcriptomics data will further the study of effectors in various aphid species.

In silico secretome prediction and expression analysis of potential effector candidates of fall armyworm (Spodoptera frugiperda)

“…For instance, SignalP and TargetP bioinformatic tools were used to predict 884 small secretory proteins from in planta transcriptome of ascomycete Colletotrichum falactum expressed during the hostpathogen interaction (Prasanth et al 2019). Similarly, a whole-body transcriptome mining approach in Russian wheat aphid, Diuraphis noxia led to the identi cation of 725 transcripts encoding putative secretary proteins including putative effector candidates of D. noxia (Nicolis et al 2022). A dual transcriptomic-proteomic approach to generate a catalogue of candidate effector proteins from the salivary gland of pea aphid, Acyrthosiphon pisum led to the identi cation of > 300 proteins harbouring secretary signal (Carolan et al, 2011).…”

“…In brown plant hopper (Nilaparvata lugens) (Stål) the transcriptome data was used to create its secretome, which ultimately led to the identi cation of multiple effector proteins (Rao et al 2019). Similarly, effector proteins were also identi ed by mining the whole-body transcriptome data of Diuraphis noxia (Russian wheat aphid) (Nicolis et al 2022). Sialotranscriptome studies, which involve the transcriptome analysis of salivary glands, have provided further impetus to the identi cation of novel effector proteins, since, salivary glands have been speculated as the factory of effector protein biosynthesis (Naalden et al 2021).…”

Estimating the Global Geographical Distribution Patterns of the Invasive Crop Pest Diuraphis noxia Kurdjumov under Current and Future Climatic Scenarios

“…Therefore, in the future climatic scenario, these countries with increased potential suitable areas, particularly, the UK, Russia, Canada, Sweden, and France, which showed a relatively large area of increase, should be alert to the import of the host plants and strengthen the warning and management system to prevent secondary invasion. Moreover, D. noxia can suck sap from the phloem of infested crops, thereby causing yield losses [ 30 , 33 ]. Major barley and wheat cultivation areas worldwide, including in Canada, Australia, and Russia, were suitable for D. noxia , thus presenting a potential threat to the global grain industry.…”

“…Wheat and barley are the main crops affected by D. noxia , and its infestation can affect crop growth and development, causing yield losses of more than 80% in severe cases [ 21 , 29 , 30 ]. Moreover, D. noxia can transmit various viruses, causing serious economic losses; within seven years of its invasion into the USA, it caused losses of USD 800 million in the western USA [ 31 , 32 , 33 , 34 ]. Owing to its potential for damaging crops and causing economic losses [ 33 , 34 ], there is an urgent need to study the potential global geographical distribution of D. noxia .…”

“…Moreover, D. noxia can transmit various viruses, causing serious economic losses; within seven years of its invasion into the USA, it caused losses of USD 800 million in the western USA [ 31 , 32 , 33 , 34 ]. Owing to its potential for damaging crops and causing economic losses [ 33 , 34 ], there is an urgent need to study the potential global geographical distribution of D. noxia . However, D. noxia potential geographical distribution patterns on a global scale remain unclear.…”