Transcriptomic and proteomic analyses provide insights into host adaptation of a bamboo-feeding aphid

Abstract

IntroductionSalivary glands and their secreted proteins play an important role in the feeding process of sap-sucking aphids. The determination of saliva composition is an important step in understanding host plant adaptation of aphids. Pseudoregma bambucicola is a severe bamboo pest in subtropical areas and the only aphid species that can exclusively feed on hard stalks of bamboos. How this species can penetrate and degrade hard bamboo cell walls and utilize a very specialized niche are important unanswered questions.MethodsIn this study, comprehensive analyses based on transcriptome sequencing, RT-qPCR, liquid chromatography-tandem spectrometry (LC–MS/MS) and bioinformatics were conducted on dissected salivary glands and secreted saliva of P. bambucicola to characterize the overall gene expression and salivary protein composition, and to identify putative effector proteins important for aphid-plant interactions. Results and DiscussionSome secretory proteins homologous to known aphid effectors important for aphid–plant interactions, such as digestive enzymes, detoxifying and antioxidant enzymes and some effectors modulating plant defenses, are also detected in salivary gland transcriptome and salivary gland and/or saliva secretomes in P. bambucicola. This indicates that these effectors are probably be essential for enabling P. bambucicola feeding on bamboo host. Although several plant cell wall degrading enzymes (PCWDEs) can be identified from transcriptome, most of the enzymes identified in salivary glands showed low expression levels and they only represent a small fraction of the complete set of enzymes for degrading cellulose and hemicellulose. In addition, our data show that P. bambucicola has no its own ability to produce pectinases. Overall, our analyses indicate that P. bambucicola may lose its own ability to express and secrete key PCWDEs, and its adaptation to unique feeding habit may depend on its symbiotic bacteria.

Proteomic Analysis of Cowpea Aphid <i>Aphis craccivora</i> Koch Salivary Gland Using LC-MS/MS Analysis

“…Aphids, to avoid plant toxic metabolites, utilize detoxification enzymes, primarily cytochrome P450, esterase, carboxypeptidase, and glutathione peroxidase, in their saliva and these enzymes are known in this study. These detoxification enzymes were commonly reported in insects, including aphids (Bos et al, 2010;Rao et al, 2013;Thorpe et al, 2017;Zhang et al, 2023), hoppers (Hattori et al, 2015;Liu et al, 2016), whiteflies (Su et al, 2012;Huang et al, 2020), thrips (Stafford-Banks et al, 2014), and psyllids (Wu et al, 2021). The trehalse enzyme has been detected in the proteome of cowpea aphids and has also been documented in the salivary glands of numerous insects (Nicholson et al, 2012;Liu et al, 2016;Yu and Killiny, 2018;Zhang et al, 2023).…”

“…Some of these potential effectors have functions known as pectinases, glucanases, or amylases involved in the degradation of the wall of plant cells. Other potentially secreted proteins have detoxification functions such as metalloproteases, oxidoreductases, peroxidases, or phenol oxidases (Rao et al, 2013;Thorpe et al, 2016;Zhang et al, 2017;Zhang et al, 2023). The cowpea aphid, Aphis craccivora Koch (Hemiptera: Aphididae), is an important legume pest and poses a severe threat to agriculture causing yield losses of up to 40% and also transmits harmful plant pathogenic viruses, including cowpea aphid-borne mosaic virus and others (Blackman and Eastop, 2000;Boukar et al, 2016).…”

Symbiotic Bacterial Communities of Insects Feeding on the Same Plant Lineage: Distinct Composition but Congruent Function

“…All insects in our study, and especially aphid species, harbor Buchnera , which plays a crucial role in providing nutrition. Previous studies reported that P. bambusicola loses its ability to feed on Bambusa , so their symbiotic bacteria help them to receive nutrition [ 75 ]. Treponema was only detected in termites ( Figure 2 B), which help them to degrade cellulose.…”