Gene expression profiles in Malpighian tubules of the vector leafhopper Psammotettix striatus (L.) revealed regional functional diversity and heterogeneity

Abstract

Background Many 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). Results Transcriptome 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. Conclusions Psammotettix 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.

Diversity and Dynamics of Bacterial Communities in the Digestive and Excretory Systems across the Life Cycle of Leafhopper, Recilia dorsalis

“…In this study, Pantoea was found to be the most abundant bacteria in the Malpighian tubules of R. dorsalis fifth-instar larvae. The Malpighian tubules are the primary excretory organs of leafhoppers, responsible for the formation of primary urine and the elimination of metabolic waste [ 66 ]. Our unpublished study has shown that Pantoea bacteria in R. dorsalis play a crucial role in the recycling of nitrogenous waste.…”

Insights into Brochosome Distribution, Synthesis, and Novel Rapid-Release Mechanism in Maiestas dorsalis (Hemiptera: Cicadellidae)

“…Notably, the Malpighian tubules of leafhoppers lack any structures for storing brochosomes, suggesting that these are stored inside cells until they are quickly discharged into the lumen and pumped through the proximal parts of the Malpighian tubules to the hindgut and rectum shortly before the leafhopper extrudes droplets of secretory fluid and applies them onto the body surface [ 3 ]. In leafhoppers such as Psammotettix striatus (Linnaeus 1758) and Graphocephala fennahi (Young, 1977), studies have demonstrated that the brochosomes released into the Malpighian tubule lumen in a cytosolic-like manner through BVs merge with the apical plasma membrane [ 18 , 21 , 23 , 24 ]. However, this “exocytosis” process seems applicable only to brochosomes housed within vacuoles situated near the plasma membrane periphery.…”

“…Moreover, due to the continuous shedding of brochosomes during the grooming process and in daily activities, this anointing behavior might be repeated multiple times between two molts to replenish the shed brochosomes on the body surface [ 6 , 20 ]. Previous research has suggested that brochosomes merge with the apical plasma membrane through brochosome-containing vacuoles and are released into the lumen, following a process similar to exocytosis [ 18 , 21 , 23 , 24 ]. Additionally, the leafhopper’s Malpighian tubules lack a dedicated storage structure for brochosomes.…”

Malpighian tubules of Rhodnius prolixus: More than post-prandial diuresis

“…AMP transcripts are actually constitutively expressed in D. melanogaster tubules, and AMP production, which is upregulated several fold in response to an immune challenge, relies upon the IMD pathway and is independent of the Toll pathway ( 40 ). In Aedes aegypti Malpighian tubules, upregulation of the Toll pathway results in the expression of immune effectors, including AMPs ( 22 ), and in the leaf hopper Psammotettix striatus , AMPs are highly expressed, but differentially, in regions of the Malpighian tubules ( 41 ).…”