Abstract

BackgroundMany leafhoppers are known as pests and disease vectors of economically important plants. Previous studies of the physiological functions of vector leafhoppers have mainly focused on the salivary glands and the alimentary tract that are deemed to be associated with digestion, host defense and phytoplasma and/or virus transmission. By contrast, the significance of Malpighian tubules (MTs) is less studied. To clarify the physiological function of MTs of the vector leafhopper Psammotettix striatus that transmits phytoplasma triggering the wheat blue dwarf disease, we performed a transcriptome study on P. striatus MTs and compared gene expression profiles among different anatomical regions in the tubules (i.e., MT1+2, the anterior segment together with the sub-anterior segment; MT3, the inflated segment; and MT4, the distal segment).ResultsTranscriptome of P. striatus MTs generate a total of 42,815 high-quality unigenes, among which highly expressed unigenes are mainly involved in organic solute transport, detoxification and immunity in addition to osmoregulation. Region-specific comparative analyses reveal that all these MT regions have functions in osmoregulation, organic solute transport and detoxification, but each region targets different substrates. Differential expression and regional enrichment of immunity-related effector activities and molecules involved in phagocytosis and the biosynthesis of antimicrobial peptides among different regions indicate that MT1+2 and MT4 have the ability to eliminate the invading pathogens. However, in MT3 which secrets brochosomes to the integument and eggs as physical barriers, disulfide-isomerase, acidic ribosomal protein P and many other unigenes were highly expressed, which can be attractive candidate genes for future studies of the biosynthesis and the origin of brochosomes.ConclusionsPsammotettix striatus MTs perform multiple physiological functions as versatile organs than just excretory organs with osmoregulatory function. Heterogeneity of physiological functions among different MT regions is related to organic solute transport, detoxification, immunity and brochosome biosynthesis in addition to osmoregulation, and each region targets different substrates. These functions may be helpful for P. striatus to resist pathogens from habitats and to utilize a wider range of host plants, which may assist the transmission and spread of phytoplasmas. The results provide potential molecular targets for the exploit of chemical and/or gene-silencing insecticides.

Highlights

  • Many leafhoppers are known as pests and disease vectors of economically important plants

  • De novo assembly and annotation We combined the nine complementary DNA (cDNA) libraries constructed from The anterior segment (MT1)+2, The inflated segment (MT3) and The distal segment (MT4), respectively, to generate the complete assembly of P. striatus Malpighian tubules (MTs)

  • Results displayed that the GC content is about 52% in all the nine sequencing libraries, and the Q20 of all libraries is above 97%, indicating that the transcriptome sequencing quality is sufficient for further analyses

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Summary

Introduction

Many leafhoppers are known as pests and disease vectors of economically important plants. To clarify the physiological function of MTs of the vector leafhopper Psammotettix striatus that transmits phytoplasma triggering the wheat blue dwarf disease, we performed a transcriptome study on P. striatus MTs and compared gene expression profiles among different anatomical regions in the tubules (i.e., MT1+2, the anterior segment together with the sub-anterior segment; MT3, the inflated segment; and MT4, the distal segment). MTs express multiple detoxification-related genes, e.g., cytochrome P450 monooxygenases (P450s), glutathione S-transferases (GSTs), alcohol dehydrogenases (ADHs), uridine diphosphate-glycosyltransferases (UGTs) and ATP-binding cassette (ABC) transporters, suggesting that the tubules have physiological functions in the detoxification of endogenous secondary metabolites and xenobiotics (e.g., plant allelochemicals: ouabain, salicylate and vinblastine) or toxins (e.g., insecticides) [5,6,7,8]. MTs are involved in carbohydrate transport and metabolism, development and reproduction [5, 23,24,25,26]

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