Abstract
BackgroundThe brown planthopper (BPH), Nilaparvata lugens (Stål), a destructive rice pest in Asia, can quickly overcome rice resistance by evolving new virulent populations. Herbivore saliva plays an important role in plant–herbivore interactions, including in plant defense and herbivore virulence. However, thus far little is known about BPH saliva at the molecular level, especially its role in virulence and BPH–rice interaction.Methodology/Principal FindingsUsing cDNA amplification in combination with Illumina short-read sequencing technology, we sequenced the salivary-gland transcriptomes of two BPH populations with different virulence; the populations were derived from rice variety TN1 (TN1 population) and Mudgo (M population). In total, 37,666 and 38,451 unigenes were generated from the salivary glands of these populations, respectively. When combined, a total of 43,312 unigenes were obtained, about 18 times more than the number of expressed sequence tags previously identified from these glands. Gene ontology annotations and KEGG orthology classifications indicated that genes related to metabolism, binding and transport were significantly active in the salivary glands. A total of 352 genes were predicted to encode secretory proteins, and some might play important roles in BPH feeding and BPH–rice interactions. Comparative analysis of the transcriptomes of the two populations revealed that the genes related to ‘metabolism,’ ‘digestion and absorption,’ and ‘salivary secretion’ might be associated with virulence. Moreover, 67 genes encoding putative secreted proteins were differentially expressed between the two populations, suggesting these genes may contribute to the change in virulence.Conclusions/SignificanceThis study was the first to compare the salivary-gland transcriptomes of two BPH populations having different virulence traits and to find genes that may be related to this difference. Our data provide a rich molecular resource for future functional studies on salivary glands and will be useful for elucidating the molecular mechanisms underlying BPH feeding and virulence differences.
Highlights
Insect herbivore saliva contains digestive enzymes, such as alkaline phosphatase, esterase, amylase and b-glucosidase, as well as other components, such as elicitors that induce plant defense, effectors that inhibit plant defense, and proteins related to pathogen transmission [1,2,3]
The length distributions of the unigenes were similar between the two populations, suggesting there was no bias in the cDNA library construction (Figure S1)
The total number of unigenes obtained was much higher than the number of brown planthopper (BPH) salivary gland expressed sequence tags (ESTs) identified by Noda et al [6], indicating the depth of coverage possible using HiSeq technology
Summary
Insect herbivore saliva contains digestive enzymes, such as alkaline phosphatase, esterase, amylase and b-glucosidase, as well as other components, such as elicitors that induce plant defense, effectors that inhibit plant defense, and proteins related to pathogen transmission [1,2,3]. The transcriptome and/or proteome of the salivary glands and/or saliva of several herbivore species – mostly hemipterans such as rice brown planthopper (BPH; Nilaparvata lugens (Stal)); Hemiptera: Delphacidae) [6,7], pea aphid (Acyrthosiphon pisum; Hemiptera: Aphididae) [8,9,10], green peach aphid (Myzus persicae; Hemiptera: Aphididae) [11,12], whitefly (Bemisia tabaci (Gennadius); Hemiptera: Aleyrodidae) [13], and potato leafhopper (Empoasca fabae (Harris); Hemiptera: Cicadellidae) [14] – have been analyzed These studies found several hundred proteins in the saliva [4,6,7,8,9,10,11,12,13,14]. Far little is known about BPH saliva at the molecular level, especially its role in virulence and BPH–rice interaction
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