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. 2019 Jul 1;19(4):3.
doi: 10.1093/jisesa/iez061.

The Anatomy and Ultrastructure of the Digestive Tract and Salivary Glands of Hishimonus lamellatus (Hemiptera: Cicadellidae)

Lizhen Dai  1 , Baodong Yang  1 , Jinzhong Wang  1 , Zhiyong Zhang  1 , Rui Yang  1 , Tieqiang Zhang  1 , Zhengguang Ren  1 , Caili Lin  2
Affiliations

The Anatomy and Ultrastructure of the Digestive Tract and Salivary Glands of Hishimonus lamellatus (Hemiptera: Cicadellidae)

Lizhen Dai et al. J Insect Sci. .

Abstract

In recent years, we found that Hishimonus lamellatus Cai et Kuoh is a potential vector of jujube witches'-broom phytoplasma. However, little is known about the anatomy and histology of this leafhopper. Here, we examined histology and ultrastructure of the digestive system of H. lamellatus, both by dissecting and by semi- and ultrathin sectioning techniques. We found that the H. lamellatus digestive tract consists of an esophagus, a filter chamber, a conical midgut and midgut loop, Malpighian tubules, an ileum, and a rectum. Furthermore, both the basal region of the filter chamber epithelium and the apical surface of the midgut epithelium have developed microvilli. We also identify the perimicrovillar membrane, which ensheaths the microvilli of midgut loop enterocyte, and the flame-like luminal membrane, which covers the microvilli of the conical midgut epithelium. In addition, H. lamellatus has the principal and accessory salivary glands. Our observations also showed that the endoplasmic reticulum, mitochondria, and secretory granules were all highly abundant in the secretory cells of the principal salivary glands, while the accessory glands consist of only one ovate or elbow-like acinus. We also briefly contrast the structure of the gut of H. lamellatus with those of other leafhopper species. These results intend to offer help for the future study on the histological and subcellular levels of phytopathogen-leafhopper relationships, including transmission barriers and the binding sites of pathogens and other microorganisms within their leafhopper vectors.

Keywords: leafhopper; Malpighian tubule; digestive system; histology; ultrastructure.

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Figures

Fig. 1.
Fig. 1.
Light micrograph of the alimentary canal of H. lamellatus. CM, conical midgut; FC, filter chamber; IL, ileum; ML, midgut loop; MT, Malpighian tubule; OE, esophagus; RE, rectum.
Fig. 2.
Fig. 2.
Semi-thin section of the digestive tract of H. lamellatus. BM, basement membrane; CEC, columnar epithelial cell; CM, conical midgut; ML, midgut loop; N, nucleus.
Fig. 3.
Fig. 3.
Transmission electron microscopy (TEM) photographs of the filter chamber and conical midgut of H. lamellatus. (A) Cross-section of the filter chamber (partial). (B) Secretory vesicles in the cells are amplified. (C) Basement membrane infolding in the filter chamber cells. (D) Microvilli developing in the basement membrane. (E) Cross-section of the conical segment (partial). (F) Conical midgut cells are attached to a flame-like luminal membrane (black arrow). CMU, circular muscle; FLM, flame-like luminal membrane; IF, infolding; L, lumen; LMU, longitudinal muscles; MIT, mitochondria; MV, microvilli; N, nucleus; PM, peritoneal membrane; RER, rough endoplasmic reticulum; SD, septate desmosomes; SV, secretory vesicle.
Fig. 4.
Fig. 4.
Transmission electron microscopy (TEM) photographs of the midgut loop of H. lamellatus. (A) Midgut loop (partial) cross-section. (B) Longitudinal muscle at the peritoneal membrane. (C) Lysosome in the cytoplasm. (D) Microvilli at the lumen of the midgut. CMU, circular muscle; L, lumen; LMU, longitudinal muscle; LY, lysosome; MIT, mitochondria; MV, microvilli; PM, peritoneal membrane; PMM, perimicrovillar membrane; SD, septate desmosomes; SV, secretory vesicle; TR, tracheole.
Fig. 5.
Fig. 5.
Transmission electron microscopy (TEM) photographs of the ileum of H. lamellatus. (A) Ileum cross-section. (B) A section of panel A is enlarged to show an abundance of mitochondria. (C) Microorganisms (black arrows) are present in ileum cells. N1 and N2, nucleus; CMU, circular muscle; L, lumen; MIT, mitochondria; RER, rough endoplasmic reticulum; SV, secretory vesicle.
Fig. 6.
Fig. 6.
Transmission electron microscopy (TEM) photograph of a Malpighian tubule of H. lamellatus. (A) Cross-section of the cell tip region. (B) A developed rough endoplasmic reticulum near the secretory vesicles. (C) A section of panel A is enlarged to show different forms of brochosomes. Also visible is an inclusion in the central cavity of BR1, the fact that the cavity of BR2 is transparent, and that the center of BR3 is a plurality of small cavities. Brochosomes in the opaque center (white arrow). (D) Sparse microvilli. BR, brochosomes; BV, brochosomes vesicles; MIT, mitochondria; MV, microvilli; RER, rough endoplasmic reticulum; SV, secretory vesicle.
Fig. 7.
Fig. 7.
Light microscopy photograph of the salivary glands of H. lamellatus. (A) Overall morphology of the salivary gland. (B) Unilateral salivary gland morphology. AD, accessory duct; AG, accessory gland; AL, anterior lobe; PD, principal duct; PG, principal gland; PL, posterior lobe.
Fig. 8.
Fig. 8.
Transmission electron microscopy (TEM) photograph of the principal gland of H. lamellatus. (A) Salivary gland cells are highly enlarged to show the multicellular nucleus. (B) The tracheole, present near the basement membrane. (C) A cross-section of the salivary duct. AMP, apical plasma membrane; CU, cuticle; MIT, mitochondria; N, nucleus; RER, rough endoplasmic reticulum; SD, salivary duct; SG, secretory granule; SV, secretory vesicle; TR, tracheole; *The contents of the lumen.
Fig. 9.
Fig. 9.
Transmission electron microscopy (TEM) photograph of the principal gland of H. lamellatus. (A) Secretory granules are placed at higher magnification. (B) Secretory vesicles are placed at higher magnifications. (C) Muscle tissue in salivary glands. (D) Microorganisms (black arrows) in the host cells. MU, muscle; RER, rough endoplasmic reticulum; SG1 and SG2, secretory granule; SV, secretory vesicle.
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