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Comparative gut proteomics study revealing adaptive physiology of Eurasian spruce bark beetle, Ips typographus (Coleoptera: Scolytinae).

ABSTRACT: The bark beetle, Ips typographus (L.), is a major pest of Norway spruce, Picea abies (L.), causing enormous economic losses globally. The adult stage of the I. typographus has a complex life cycle (callow and sclerotized); the callow beetles feed ferociously, whereas sclerotized male beetles are more aggressive and pioneers in establishing new colonies. We conducted a comparative proteomics study to understand male and female digestion and detoxification processes in callow and sclerotized beetles. Proteome profiling was performed using high-throughput liquid chromatography-mass spectrometry. A total of >3000 proteins were identified from the bark beetle gut, and among them, 539 were differentially abundant (fold change ±2, FDR <0.05) between callow and sclerotized beetles. The differentially abundant proteins (DAPs) mainly engage with binding, catalytic activity, anatomical activity, hydrolase activity, metabolic process, and carbohydrate metabolism, and hence may be crucial for growth, digestion, detoxification, and signalling. We validated selected DAPs with RT-qPCR. Gut enzymes such as NADPH-cytochrome P450 reductase (CYC), glutathione S-transferase (GST), and esterase (EST) play a crucial role in the I. typographus for detoxification and digesting of host allelochemicals. We conducted enzyme activity assays with them and observed a positive correlation of CYC and GST activities with the proteomic results, whereas EST activity was not fully correlated. Furthermore, our investigation revealed that callow beetles had an upregulation of proteins associated with juvenile hormone (JH) biosynthesis and chitin metabolism, whereas sclerotized beetles exhibited an upregulation of proteins linked to fatty acid metabolism and the TCA cycle. These distinctive patterns of protein regulation in metabolic and functional processes are specific to each developmental stage, underscoring the adaptive responses of I. typographicus in overcoming conifer defences and facilitating their survival. Taken together, it is the first gut proteomic study comparing males and females of callow and sclerotized I. typographus, shedding light on the adaptive ecology at the molecular level. Furthermore, the information about bark beetle handling of nutritionally limiting and defence-rich spruce phloem diet can be utilized to formulate RNAi-mediated beetle management.

SUBMITTER: Ashraf MZ

PROVIDER: S-EPMC10703158 | biostudies-literature | 2023

REPOSITORIES: biostudies-literature

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Comparative gut proteomics study revealing adaptive physiology of Eurasian spruce bark beetle, Ips typographus (Coleoptera: Scolytinae).

Ashraf Muhammad Zubair MZ Mogilicherla Kanakachari K Sellamuthu Gothandapani G Siino Valentina V Levander Fredrik F Roy Amit A

Frontiers in plant science 20231121

The bark beetle, Ips typographus (L.), is a major pest of Norway spruce, Picea abies (L.), causing enormous economic losses globally. The adult stage of the I. typographus has a complex life cycle (callow and sclerotized); the callow beetles feed ferociously, whereas sclerotized male beetles are more aggressive and pioneers in establishing new colonies. We conducted a comparative proteomics study to understand male and female digestion and detoxification processes in callow ...[more]

PMID: 38078109

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Project description:Eurasian spruce bark beetle, Ips typographus is a destructive pest of the Norway spruce (Picea abies). Recent outbreaks in Europe have been attributed to global warming and other anthropogenic impacts. Bark beetles are guided by multiple complex olfactory cues throughout their life cycle. Male-produced aggregation pheromones, comprising 2-methyl-3-buten-2-ol and cis-verbenol, have been identified as the most powerful attractants for dispersing conspecifics. In addition to host trees, bark beetles interact with multiple organisms, including symbiotic ophiostomatoid fungi, which may promote beetle colonization success and offspring development. Previously, in a short-distance laboratory assay, we demonstrated that I. typographus adults are attracted to the volatile organic compounds (VOCs) produced by three symbiotic fungi: Grosmannia penicillata, Endoconidiophora polonica, and Leptographium europhioides. Furthermore, the abundant fusel alcohols and their acetates were found to be the most attractive odorants in the fungal VOC profile. In this study, using a long-distance field-trapping experiment, we analyzed the role of fungal VOCs as attractants for dispersing I. typographus. Two types of fungal lures were tested in combination with pheromones in traps: (1) live cultures of fungi grown on potato dextrose agar (PDA) and (2) dispensers containing synthetic fusel alcohols and their acetates in equal proportions. Subsequently, the composition of VOCs emitted from live fungal lures were analyzed. We found that the symbiotic fungi synergistically increased the attraction of beetles to pheromones in field traps and the attractiveness of live fungal lures depended on the fungal load. While one Petri dish with E. polonica, when combined with pheromones synergistically increased trapping efficiency, three Petri dishes with L. europhioides were required to achieve the same. The synthetic mix of fungal fusel alcohols and acetates improved the catch efficiency of pheromones only at a low tested dose. VOC analysis of fungal cultures revealed that all the three fungi produced fusel alcohols and acetates but in variable composition and amounts. Collectively, the results of this study show that, in addition to pheromones, bark beetles might also use volatile cues from their symbiotic fungi to improve tree colonization and reproductive success in their breeding and feeding sites.

Project description:The Eurasian spruce bark beetle Ips typographus is known for its devasting attack on the host tree Picea abies, a common conifer in Europe. The beetle uses various pheromone components (2-methyl-3-buten-2-ol and cis-verbenol) for mass aggregation to overcome the tree defence compounds such as terpenes. Though this aggregation pheromone biosynthesis and respective precursors via terpenes detoxification mechanism was investigated for a few decades, gene-level understanding behind these biosynthesis pathways are uncertain yet in I. typographus. Though, applying Juvenile hormone (JH III) on the beetles have induced specific pheromone biosynthesis in many bark beetle species, irrespective of their life stage, it is not uniform found in all Ips species. While investigating pheromone biosynthesis among various life stages of I. typographus, we have also reported recently about the JHIII induction of aggregation pheromone biosynthesis from the gut tissue of the beetle. Thus, in this study, we have applied the concept of JHIII induction on I. typographus and analyzed the respective pheromone and possible biosynthesis precursors from via pathway gene families from the gut tissue of the beetle. A comparative approach from transcriptome and proteome study has revealed the mevalonate pathway genes including isoprenyl-di-phosphate synthase (IPDS) gene (Ityp09271) was upregulated over 5-fold change after JHIII induction in I. typographus. The identified IPDS is suspected to directly involve in 2-methyl-3-buten-2-ol, a vital aggregation pheromone of I. typographus. Added to that, a hydrolase gene family was found upregulated over 2-fold change, specifically in the male gut tissue after JHIII treatment. Furthermore, another vital gene family, CytochromeP450 have shown the upregulated (transcript) in the male gut tissue after treatment. Especially Previously reported CyP450 candidates Ityp3140 and Ityp03153 for pheromone compounds cis/trans- verbenol and ipsdienol biosynthesis respectively. Along with CyP450 candidates, the hydrolase gene candidates could possibly involve in braking down the detox compounds such as diglycosylated terpenes and stored wax esters (verbenyl oleate) from the gut possibly provided from the of the beetle body as a reservoir. An added metabolomic analysis has confirmed these compounds abundance was in the gut tissue. Especially, the abundance of the related fatty acid ester (verbenyl oleate) has reduced half in male gut tissue after the treatment. Hence, we have shed light on three possible genes from different families for the respective pheromone and its precursors biosynthesis after JHIII application over I. typographus. This approach would lead us to elucidate the molecular basis of stored pheromone biosynthesis and the derived knowledge from this study would lead to eco-friendly pest management for this aggressive pest. Key words: Ips typographus, bark beetle, pheromone biosynthesis, de novo, Juvenile hormone treatment.

Project description:Ips typographus (Coleoptera, Scolytinae) is a spruce-infesting bark beetle that occurs throughout Europe and Asia. The beetle can cause considerable damage, especially when colonized trees are stressed and beetle populations increase. Although some studies have shown that populations of I. typographus in Europe, China and Japan are genetically distinct, these populations are biologically similar, including a strong association with ophiostomatoid fungi. To date, only two Leptographium spp. have been reported from the beetle in China, while 40 species have been reported from Europe and 13 from Japan. The aims of this study were to identify the ophiostomatoid fungal associates of I. typographus in north-eastern China, and to determine whether the fungal assemblages reflect the different geographical populations of the beetle. Field surveys in Jilin and Heilongjiang provinces yielded a total of 1 046 fungal isolates from 145 beetles and 178 galleries. Isolates were grouped based on morphology and representatives of each group were identified using DNA sequences of the ribosomal LSU, ITS, β-tubulin, calmodulin and elongation factor 1-α gene regions. A total of 23 species of ophiostomatoid fungi were identified, including 12 previously described species and 11 novel species, all of which are described here. The dominant species were Ophiostoma bicolor, Leptographium taigense and Grosmannia piceiperda D, representing 40.5 %, 27.8 % and 17.8 % of the isolates, respectively. Comparisons of species from China, Europe and Japan are complicated by the fact that some of the European and all the Japanese species were identified based only on morphology. However, assuming that those identifications are correct, five species were shared between Europe, Japan and China, two species were shared between China and Japan, five between Europe and China, and two between Europe and Japan. Consequently, Ips typographus populations in these different geographic areas have different fungal assemblages, suggesting that the majority of these beetle-associations are promiscuous. The results also suggested that the symbionts of the bark beetle do not reflect the population structures of the beetle. The use of fungal symbiont assemblages to infer population structures and invasion history of its vectors should thus be interpreted with circumspection.

Dataset Information

Comparative gut proteomics study revealing adaptive physiology of Eurasian spruce bark beetle, Ips typographus (Coleoptera: Scolytinae).

Publications

Comparative gut proteomics study revealing adaptive physiology of Eurasian spruce bark beetle, <i>Ips typographus</i> (Coleoptera: Scolytinae).

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