Argasid systematics and the evolution of blood-feeding behavior: Perspectives from salivary gland transcriptomes

AbstractAnopheles is a genus belonging to the Culicidae family, which has great medical importance due to its role as a vector of Plasmodium, the parasite responsible for malaria. From Anopheles’ functional genomics, great focus has been given to the salivary gland proteins (SGPs) group. This class of proteins is essential to blood-feeding behavior as they have attributes such as vasodilators and anti-clotting properties. Recently, a comprehensive review on Anopheles SGPs was performed, however the authors did not deeply explore the adaptive molecular evolution of these genes. In this context, this work aimed to perform a more detailed analysis of the adaptive molecular evolution of SGPs in Anopheles, carrying out positive selection and gene families evolution analysis on 824 SGPs. Our results show that most SGPs have positively selected sites that can be used as targets in the development of new strategies for vector control. Notably, we were not able to find any evidence of an accelerated shift in the copy-number variation of SGPs compared with other proteins, as suggested in previous works.Significance StatementSalivary gland proteins (SGPs) are essential to blood-feeding behavior in Anopheles and they are the most studied class of proteins in blood-feeding insects. However a proper molecular evolution analysis on SGPs in Anopheles is missing. In our analyses we observed that most SGPs have positively selected sites and we were not able to find any evidence of an accelerated shift in the copy-number of SGPs compared with other proteins, as stated in the literature. Our results can open new venues in the development of new strategies for vector control.

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A method for observing the blood-feeding behavior of aedine mosquitoes

Medical Entomology and Zoology ◽

10.7601/mez.33.17 ◽

1982 ◽

Vol 33 (1) ◽

pp. 17-20

Author(s):

Hiroshi YAMANISHI

Keyword(s):

Feeding Behavior ◽

Blood Feeding

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Beyond Nature and Nurture: Phenotypic Plasticity in Blood-Feeding Behavior of Anopheles gambiae s.s. When Humans Are Not Readily Accessible

American Journal of Tropical Medicine and Hygiene ◽

10.4269/ajtmh.2009.09-0124 ◽

2009 ◽

Vol 81 (6) ◽

pp. 1023-1029 ◽

Cited By ~ 77

Author(s):

Thierry Lefèvre ◽

Frédéric Thomas ◽

François Renaud ◽

Eric Elguero ◽

Didier Fontenille ◽

...

Keyword(s):

Phenotypic Plasticity ◽

Feeding Behavior ◽

Anopheles Gambiae ◽

Blood Feeding ◽

Anopheles Gambiae S.S ◽

Nature And Nurture

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Comparative sialomics between hard and soft ticks: Implications for the evolution of blood-feeding behavior

Insect Biochemistry and Molecular Biology ◽

10.1016/j.ibmb.2007.09.003 ◽

2008 ◽

Vol 38 (1) ◽

pp. 42-58 ◽

Cited By ~ 112

Author(s):

Ben J. Mans ◽

John F. Andersen ◽

Ivo M.B. Francischetti ◽

Jesus G. Valenzuela ◽

Tom G. Schwan ◽

...

Keyword(s):

Feeding Behavior ◽

Blood Feeding

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Salivary AsHPX12 influence pre-blood meal associated behavioral properties in the mosquito Anopheles stephensi

10.1101/2020.06.12.147959 ◽

2020 ◽

Cited By ~ 2

Author(s):

Seena Kumari ◽

Tanwee Das De ◽

Charu Chauhan ◽

Jyoti Rani ◽

Sanjay Tevatiya ◽

...

Keyword(s):

Salivary Gland ◽

Blood Meal ◽

Anopheles Stephensi ◽

Blood Feeding ◽

Vital Role ◽

Host Attraction ◽

Altered Expression ◽

Rnaseq Data ◽

Transcriptional Modulation ◽

Physiological Homeostasis

AbstractIn the adult female mosquito, successful blood meal acquisition is accomplished by salivary glands, which releases a cocktail of proteins to counteract vertebrate host’s immune-homeostasis. However, the biological relevance of many salivary proteins remains unknown. Here, we characterize a salivary specific Heme peroxidase family member HPX12, originally identified from Plasmodium vivax infected salivary RNAseq data of the mosquito Anopheles stephensi. We demonstrate that dsRNA silencing mediated mRNA depletion of salivary AsHPX12 (80-90%), causes enhanced host attraction but reduced blood-meal acquisition abilities, by increasing probing propensity (31%), as well as probing time (100–200s, P<0.0001) as compared to control (35-90s) mosquitoes group. Altered expression of the salivary secretory and antennal proteins may account for an unusual fast release of salivary cocktail proteins, but the slowing acquisition of blood meal, possibly due to salivary homeostasis disruption of AsHPX12 silenced mosquitoes. A parallel transcriptional modulation in response to blood feeding and P. vivax infection, further establish a possible functional correlation of AsHPX12 role in salivary immune-physiology and Plasmodium sporozoites survival/transmission. We propose that salivary HPX12 may have a vital role in the management of ‘pre- and post’-blood meal associated physiological-homeostasis and parasite transmission.Graphical abstractFigure 1:Schematic representation of mosquito’s blood meal acquisition and upshot on blood-feeding after silencing of salivary gland HPX-12. (A) After landing over host skin, mosquito mouthparts (proboscis) actively engaged to search, probe, and pierce the skin followed by a rapid release of the pre-synthesized salivary cocktail, which counteracts the host homeostasis, inflammation, and immune responses, during blood meal uptake. (B) Silencing of HPX-12 disrupts salivary gland homeostasis, enhancing mosquito attraction, possibly by up-regulating odorant-binding proteins genes-OBP-7,10 and OBP-20 expression in the Olfactory System. However, HPX-12 disruption may also cause significant effects on pre-blood meal associated probing abilities, which may be due to fast down-regulation of salivary cocktail proteins such as Anopheline, Apyrase, D7L proteins.

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Changes in Protein Phosphorylation during Salivary Gland Degeneration in Haemaphysalis longicornis

The Korean Journal of Parasitology ◽

10.3347/kjp.2020.58.2.161 ◽

2020 ◽

Vol 58 (2) ◽

pp. 161-171

Author(s):

Qi Xiao ◽

Yuhong Hu ◽

Xiaohong Yang ◽

Jianna Tang ◽

Xiaoshuang Wang ◽

...

Keyword(s):

Salivary Gland ◽

Rna Interference ◽

Protein Phosphorylation ◽

Quantitative Study ◽

Quantitative Proteomics ◽

Blood Feeding ◽

Study Data ◽

Haemaphysalis Longicornis ◽

Phosphorylated Proteins ◽

Data Independent Acquisition

The ticks feed large amount of blood from their hosts and transmit pathogens to the victims. The salivary gland plays an important role in the blood feeding. When the female ticks are near engorgement, the salivary gland gradually loses its functions and begins to rapidly degenerate. In this study, data-independent acquisition quantitative proteomics was used to study changes in the phosphorylation modification of proteins during salivary gland degeneration in <i>Haemaphysalis longicornis</i>. In this quantitative study, 400 phosphorylated proteins and 850 phosphorylation modification sites were identified. Trough RNA interference experiments, we found that among the proteins with changes in phosphorylation, apoptosis-promoting Hippo protein played a role in salivary gland degeneration.

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Characterization of a vasodilator from the salivary glands of the yellow fever mosquito Aedes aegypti

Journal of Experimental Biology ◽

10.1242/jeb.165.1.61 ◽

1992 ◽

Vol 165 (1) ◽

pp. 61-71 ◽

Cited By ~ 4

Author(s):

J. M. Ribeiro

Keyword(s):

Salivary Gland ◽

Aedes Aegypti ◽

Salivary Glands ◽

Posterior Part ◽

Aortic Ring ◽

Blood Feeding ◽

Reversed Phase ◽

Relative Molecular Mass ◽

Vasodilatory Activity ◽

Carboxy Terminal

Salivary gland homogenates and oil-induced saliva of the mosquito Aedes aegypti dilate the rabbit aortic ring and contract the guinea pig ileum. The vasodilatory activity is endothelium-dependent, heat-stable, sensitive to both trypsin and chymotrypsin treatments, and both smooth muscle activities cross-desensitize to the tachykinin peptide substance P. Both bioactivities co-elute when salivary gland homogenates are fractionated by reversed-phase HPLC. Molecular sieving chromatography indicates a relative molecular mass of 1400. A monoclonal antibody specific to the carboxy terminal region of tachykinins reacts with material in the posterior part of the central lobe of paraformaldehyde-fixed salivary glands. The presence of a vasodilatory peptide of the tachykinin family in the salivary glands of A. aegypti is proposed and its role in blood feeding is discussed.

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