Water deficit and aphid resilience on wheat: examining Sitobion avenae F. and their bacterial symbionts interplay under controlled laboratory conditions.

BACKGROUND: Climate change has far-reaching effects on food security and agriculture, affecting crop yields and food distribution. Agriculture relies heavily on water for irrigation and production, making it vulnerable to water scarcity. Additionally, climate change can affect crop pest insects, leading to increased global crop losses, particularly in cereals, an important component of the human diet. Aphids are major crop pests and have a symbiotic relationship with bacterial endosymbionts that can contribute to their success as pests under a climate change scenario. To test the effect of drought on aphids, we examined varying levels of water deficit and endosymbiont composition on the grain aphid (Sitobion avenae) performance on wheat under controlled laboratory conditions. We measured the intrinsic rate of population increase (rm), the body weight of adult aphids, and the pre-reproductive period for different genotypes of the grain aphid (including Chilean superclones) under different irrigation regimes. We also analyzed the relative abundance of their endosymbionts under the different water treatments. RESULTS: Our findings revealed that water deficit affects each aphid genotype differently, impacting various traits. For instance, the body weight of adult aphids was notably affected by different water treatments, with aphids grown under intermediate water deficit (IW) being significantly bigger. The relative abundance of endosymbionts also varied among genotypes and water treatments-specifically Regiella insecticola had a noticeably higher abundance under IW (P < 0.05). CONCLUSION: This study provides valuable insights into the impact of water deficit on aphid performance and the role of endosymbionts in mitigating the effects of water deficit. © 2024 Society of Chemical Industry.

An Aphid Pest Superclone Benefits From a Facultative Bacterial Endosymbiont in a Host-Dependent Manner, Leading to Reproductive and Proteomic Changes.

The English grain aphid, Sitobion avenae, is a significant agricultural pest affecting wheat, barley, and oats. In Chile, the most prevalent and persistent clone (superclone) of S. avenae harbors the facultative endosymbiont bacterium Regiella insecticola. To determine the role of this bacterium in the reproductive success of this superclone, the presence of R. insecticola was manipulated to assess its impact on (1) the reproductive performance of this clone on two host plant species (wheat and barley), (2) the production of winged morphs, (3) changes in the insects' proteomic profiles, and (4) the root/shoot ratio of plant. It was found that the reproductive performance of this S. avenae superclone varied across host plants, depending on the presence of the facultative bacterial endosymbiont. Aphids infected with R. insecticola showed higher reproductive success on wheat, while the opposite effect was observed on barley. Aphid biomass was greater when infected with R. insecticola, particularly on barley. Additionally, aphids harboring R. insecticola exhibited a higher proportion of winged individuals on both host plants. Protein regulation in aphids on wheat was lower compared to those on barley. A higher root/shoot biomass ratio was observed in wheat plants compared to barley when infested by R. insecticola-infected aphid. Thus, R. insecticola significantly influences the reproductive performance and proteomic profile of a S. avenae superclone, with these effects shaped by the host plant. This suggests that the interaction between the host plant and the facultative endosymbiont contributes to the ecological success of this superclone.

Facultative endosymbionts modulate the aphid reproductive performance on wheat cultivars differing in contents of benzoxazinoids.

BACKGROUND: Facultative bacterial endosymbionts have the potential to influence the interactions between aphids, their natural enemies, and host plants. Among the facultative symbionts found in populations of the grain aphid Sitobion avenae in central Chile, the bacterium Regiella insecticola is the most prevalent. In this study, we aimed to investigate whether infected and cured aphid lineages exhibit differential responses to wheat cultivars containing varying levels of the benzoxazinoid DIMBOA (2,4-dihydroxy-7-methoxy-2H-1,4-benzoxazin-3(4H)-one), which is a xenobiotic compound produced by plants. Specifically, we examined the reproductive performance responses of the most frequently encountered genotypes of Sitobion avenae when reared on wheat seedlings expressing low, medium, and high concentrations of DIMBOA. RESULTS: Our findings reveal that the intrinsic rate of population increase (rm ) in cured lineages of Sitobion avenae genotypes exhibits a biphasic pattern, characterized by the lowest rm and an extended time to first reproduction on wheat seedlings with medium levels of DIMBOA. In contrast, the aphid genotypes harbouring Regiella insecticola display idiosyncratic responses, with the two most prevalent genotypes demonstrating improved performance on seedlings featuring an intermediate content of DIMBOA compared to their cured counterparts. CONCLUSION: This study represents the first investigation into the mediating impact of facultative endosymbionts on aphid performance in plants exhibiting varying DIMBOA contents. These findings present exciting prospects for identifying novel targets for aphid control by manipulating the presence of aphid symbionts. © 2023 Society of Chemical Industry.

Comparative transcriptomic analysis of chemoreceptors in two sympatric scarab beetles, Hylamorpha elegans and Brachysternus prasinus.

Chemoreception through odorant receptors (ORs), ionotropic receptors (IRs) and gustatory receptors (GRs) represents the functions of key proteins in the chemical ecology of insects. Recent studies have identified chemoreceptors in coleopterans, facilitating the evolutionary analysis of not only ORs but also IRs and GRs. Thus, Cerambycidae, Tenebrionidae and Curculionidae have received increased attention. However, knowledge of the chemoreceptors from Scarabaeidae is still limited, particularly for those that are sympatric. Considering the roles of chemoreceptors, this analysis could shed light on evolutionary processes in the context of sympatry. Therefore, the aim of this study was to identify and compare the repertoires of ORs, GRs and IRs between two sympatric scarab beetles, Hylamorpha elegans and Brachysternus prasinus. Here, construction of the antennal transcriptomes of both scarab beetle species and analyses of their phylogeny, molecular evolution and relative expression were performed. Thus, 119 new candidate chemoreceptors were identified for the first time, including 17 transcripts for B. prasinus (1 GR, 3 IRs and 13 ORs) and 102 for H. elegans (22 GRs, 14 IRs and 66 ORs). Orthologs between the two scarab beetle species were found, revealing specific expansions as well as absence in some clades. Purifying selection appears to have occurred on H. elegans and B. prasinus ORs. Further efforts will be focused on target identification to characterize kairomone and/or pheromone receptors.

TPC1-Type Channels in Physcomitrium patens: Interaction between EF-Hands and Ca2.

Two-pore channels (TPCs) are members of the superfamily of ligand-gated and voltage-sensitive ion channels in the membranes of intracellular organelles of eukaryotic cells. The evolution of ordinary plant TPC1 essentially followed a very conservative pattern, with no changes in the characteristic structural footprints of these channels, such as the cytosolic and luminal regions involved in Ca2+ sensing. In contrast, the genomes of mosses and liverworts encode also TPC1-like channels with larger variations at these sites (TPC1b channels). In the genome of the model plant Physcomitrium patens we identified nine non-redundant sequences belonging to the TPC1 channel family, two ordinary TPC1-type, and seven TPC1b-type channels. The latter show variations in critical amino acids in their EF-hands essential for Ca2+ sensing. To investigate the impact of these differences between TPC1 and TPC1b channels, we generated structural models of the EF-hands of PpTPC1 and PpTPC1b channels. These models were used in molecular dynamics simulations to determine the frequency with which calcium ions were present in a coordination site and also to estimate the average distance of the ions from the center of this site. Our analyses indicate that the EF-hand domains of PpTPC1b-type channels have a lower capacity to coordinate calcium ions compared with those of common TPC1-like channels.

A mutation increases the specificity to plant compounds in an insect chemosensory protein.

Host plant recognition are highly dependent on chemosensory perception, which involves chemosensory proteins (CSPs) that bind key chemical compounds the host plants. In this work, we hypothesize that two closely related aphid taxa, which differ in diet breadth, also differ in their CSPs. We detected a non-synonymous difference (lysine for asparagine) between M. persicae sensu stricto (Mpp) and the subspecies M. p. nicotianae (Mpn) in the sequence of a CSP (CSP5). We modeled in silico the binding capacity of both CSP5s variants with 163 different potential ligands from their host plants (120 unique from tobacco, 29 unique from peach, and 14 common ligands). After docking analysis with all ligands, we selected the three best ligands for each variant to perform molecular dynamics (tobacco: 2-cyclopentene-1,4-dione, salicylaldehyde, and benzoic acid; peach: phenol, valeric acid, and benzonitrile). The binding energy of the MpnCSP5 model to the studied ligands was, in all cases, lower than with the MppCSP5 model. The ligands from the host plants showed more stable binding with MpnCSP5 than with MppCSP5. This result suggests that the set of CSPs studied among M. persicae s. str. and M. p. nicotianae are very similar, but focusing on the CSP5 protein, we found a single key mutation that increases affinities for host compounds for M. p. nicotianae, which might have contributed to the specialization to tobacco. This study provides new insights into an evolutionary trend toward specificity in a binding protein.

Sex- and tissue-specific expression of odorant-binding proteins and chemosensory proteins in adults of the scarab beetle Hylamorpha elegans (Burmeister) (Coleoptera: Scarabaeidae).

In this study, we addressed the sex- and tissue-specific expression patterns of odorant-binding proteins (OBPs) and chemosensory proteins (CSPs) in Hylamorpha elegans (Burmeister), an important native scarab beetle pest species from Chile. Similar to other members of its family, this scarab beetle exhibit habits that make difficult to control the pest by conventional methods. Hence, alternative ways to manage the pest populations based on chemical communication and signaling (such as disrupting mating or host finding process) are highly desirable. However, developing pest-control methods based on chemical communication requires to understand the molecular basis for pheromone recognition/chemical perception in this species. Thus, with the aim of discovering olfaction-related genes, we obtained the first reference transcriptome assembly of H. elegans. We used different tissues of adult beetles from males and females: antennae and maxillary palps, which are well known for embedded sensory organs. Then, the expression of predicted odorant-binding proteins (OBPs) and chemosensory proteins (CSPs) was analyzed by qRT-PCR. In total, 165 transcripts related to chemoperception were predicted. Of these, 16 OBPs, including one pheromone-binding protein (PBP), and four CSPs were successfully amplified by qRT-PCR. All of these genes were differentially expressed in the sensory tissues with respect to the tibial tissue that was used as a control. The single predicted PBP found was highly expressed in the antennal tissues, particularly in males, while several OBPs and one CSP showed male-biased expression patterns, suggesting that these proteins may participate in sexual recognition process. In addition, a single CSP was expressed at higher levels in female palps than in any other studied condition, suggesting that this CSP would participate in oviposition process. Finally, all four CSPs exhibited palp-biased expression while mixed results were obtained for the expression of the OBPs, which were more abundant in the palps than in the antennae. These results suggest that these chemoperception proteins would be interesting novel targets for control of H. elegans, thus providing a theoretical basis for further studies involving new pest control methods.

Analysis of the grapevine moth Lobesia botrana antennal transcriptome and expression of odorant-binding and chemosensory proteins.

The grapevine moth, Lobesia botrana, is considered a harmful pest for vineyards in Chile as well as in North America and Europe. Currently, monitoring and control methods of L. botrana are based on its main sex pheromone component, being effective for low population densities. In order to improve control methods, antennal olfactory proteins in moths, such as odorant-binding proteins (OBPs) and odorant receptors (ORs) have been studied as promising targets for the discovery of new potent semiochemicals, which have not been reported for L. botrana. Therefore, the objective of this study was to identify the repertoire of proteins related to chemoreception in L. botrana by antennal transcriptome and analyze the relative expression of OBPs and CSPs in male and female antennae. Through next-generation sequencing of the antennal transcriptome by Ilumina HiSeq2500 we identified a total of 118 chemoreceptors, from which 61, 42 and 15 transcripts are related to ORs, ionotropic receptors (IRs) and gustatory receptors (GRs), respectively. Furthermore, RNA-Seq data revealed 35 transcripts for OBPs and 18 for chemosensory proteins (CSPs). Analysis by qRT-PCR showed 20 OBPs significantly expressed in female antennae, while 5 were more expressed in males. Similarly, most of the CSPs were significantly expressed in female than male antennae. All the olfactory-related sequences were compared with homologs and their phylogenetic relationships elucidated. Finally, our findings in relation to the improvement of L. botrana management are discussed.

Expression differences in Aphidius ervi (Hymenoptera: Braconidae) females reared on different aphid host species.

The molecular mechanisms that allow generalist parasitoids to exploit many, often very distinct hosts are practically unknown. The wasp Aphidius ervi, a generalist koinobiont parasitoid of aphids, was introduced from Europe into Chile in the late 1970s to control agriculturally important aphid species. A recent study showed significant differences in host preference and host acceptance (infectivity) depending on the host A. ervi were reared on. In contrast, no genetic differentiation between A. ervi populations parasitizing different aphid species and aphids of the same species reared on different host plants was found in Chile. Additionally, the same study did not find any fitness effects in A. ervi if offspring were reared on a different host as their mothers. Here, we determined the effect of aphid host species (Sitobion avenae versus Acyrthosiphon pisum reared on two different host plants alfalfa and pea) on the transcriptome of adult A. ervi females. We found a large number of differentially expressed genes (between host species: head: 2,765; body: 1,216; within the same aphid host species reared on different host plants: alfalfa versus pea: head 593; body 222). As expected, the transcriptomes from parasitoids reared on the same host species (pea aphid) but originating from different host plants (pea versus alfalfa) were more similar to each other than the transcriptomes of parasitoids reared on a different aphid host and host plant (head: 648 and 1,524 transcripts; body: 566 and 428 transcripts). We found several differentially expressed odorant binding proteins and olfactory receptor proteins in particular, when we compared parasitoids from different host species. Additionally, we found differentially expressed genes involved in neuronal growth and development as well as signaling pathways. These results point towards a significant rewiring of the transcriptome of A. ervi depending on aphid-plant complex where parasitoids develop, even if different biotypes of a certain aphid host species (A. pisum) are reared on the same host plant. This difference seems to persist even after the different wasp populations were reared on the same aphid host in the laboratory for more than 50 generations. This indicates that either the imprinting process is very persistent or there is enough genetic/allelic variation between A. ervi populations. The role of distinct molecular mechanisms is discussed in terms of the formation of host fidelity.