Expression Profiles of Digestive Genes in the Gut and Salivary Glands of Tarnished Plant Bug (Hemiptera: Miridae)

Abstract

Host plant preference of agricultural pests may shift throughout the growing season, allowing the pests to persist on wild hosts when crops are not available. Lygus Hahn (Hemiptera: Miridae) bugs are severe pests of cotton during flowering and fruiting stages, but can persist on alternative crops, or on weed species. Diversity of digestive enzymes produced by salivary glands and gut tissues play a pivotal role in an organism’s ability to utilize various food sources. Polyphagous insects produce an array of enzymes that can process carbohydrates, lipids, and proteins. In this study, the digestive enzyme repertoire of the tarnished plant bug, Lygus lineolaris (Palisot de Beauvois), was identified by high-throughput sequencing followed by cDNA cloning and sequencing. This study identified 87 digestive genes, including 30 polygalacturonases (PG), one β-galactosidase, three α-glucosidases, six β-glucosidases, 28 trypsin-like proteases, three serine proteases, one apyrase-like protease, one cysteine protease, 12 lipases, and two transcripts with low similarity to a xylanase A-like genes. RNA-Seq expression profiles of these digestive genes in adult tarnished plant bugs revealed that 57 and 12 genes were differentially expressed in the salivary gland and gut (≥5-fold, P ≤ 0.01), respectively. All polygalacturonase genes, most proteases, and two xylanase-like genes were differentially expressed in salivary glands, while most of the carbohydrate and lipid processing enzymes were differentially expressed in the gut. Seven of the proteases (KF208689, KF208697, KF208698, KF208699, KF208700, KF208701, and KF208702) were not detected in either the gut or salivary glands.

Comparative analyses of the venom components in the salivary gland transcriptomes and saliva proteomes of some heteropteran insects

“…C. lectularius , which does not share a common ancestor with other blood‐feeding insects, possesses novel ubiquitous enzymes such as acetyl/butyryl cholinesterase, Nudix‐type hydrolases, and novel peptides with unknown functions (Francischetti et al ., 2010). Since host plants such as cotton defend themselves by rapidly responding to different insect feeding mechanisms, insects adjust their expression patterns depending on the developmental stages or feeding sites of the host plant, which are important factors in the evolution of both insects and plants (Tan et al ., 2016; Perera et al ., 2021). The adaptation of phytophagous heteropteran species to plant feeding can be observed not only in the increased activities of their digestive enzymes, including pectinase, amylase, and cellulase, and in the saliva of phytophagous Apolygus lucorum with age, but also the increased activities of the salivary digestive enzymes of the corn bug Eurygaster integriceps in response to feeding (Mehrabadi et al ., 2014; Tan et al ., 2016).…”

“…Sap‐feeding aphids are known to deliver protein effectors from their saliva to the inside of their host to modulate the host immune system (Bos et al ., 2010). In recent studies, an abundant amount of digestive enzymes and several immune‐related transcripts were represented in sialotranscriptome data of the tarnished plant bug, which might be involved in the solubilization of nutrients from plant tissues and counteracting plant defense responses (Showmaker et al ., 2016; Perera et al ., 2021). This could have been one of the adaptations to become a major insect group (Schaefer & Panizzi, 2000).…”

High-quality chromosome-level genome assembly of the plant bug Pachypeltis micranthus provides insights into the availability of Mikania micrantha control

“…The lique ed materials are further digested and absorbed in the gut. As we stated previously, the digestive enzymes remaining in plants cause continuous tissue damage for an extended period, leading to a decrease in the growth rate and loss of owers [18][19][20]. The digestive enzyme is an essential factor in the adaption of P. micranthus to M. micrantha and also provides a new strategy to control M. micrantha.…”

“…Like other mirid bugs, P. micranthus feed by inserting its stylet into plant tissues and injecting enzyme-containing saliva (digestive enzymes); the injected saliva is responsible for stylet lubrication and preliminary digestion of plant tissues [13,16,17]. The salivary enzymes remaining in the feeding site cause continuous tissue damage for an extended period, leading to a decrease in the growth rate and loss of owers [18][19][20]. The primary damage caused by mirid bugs during feeding is due to saliva rather than mechanical damage caused by stylet [19].…”

“…In the past, salivary gland transcriptome analysis has mainly focused on blood feeding [17]. For mirid bugs, only the salivary gland transcriptomes of Lygus lineolaris were reported [17,20], providing valuable information for omnivorous mirid bugs. However, the salivary gland transcriptome of P. micranthus is needed, and generating this data will increase our knowledge of how the oligophagous mirid bugs can adapt to the speci c host.…”