Evidence of the Biochemical Basis of Host Virulence in the Greenbug Aphid, Schizaphis graminum (Homoptera: Aphididae) (original) (raw)
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ABSTRACT: Biotypes of aphids and many other insect pests are defined based on the phenotypic response of host plants to the insect pest without considering their intrinsic characteristics and genotypes. Plant breeders have spent considerable effort developing aphid-resistant, small-grain varieties to limit insecticide control of the greenbug, Schizaphis graminum. However, new S. graminum biotypes frequently emerge that break resistance. Mechanisms of virulence on the aphid side of the plant−insect interaction are not well understood. S. graminum biotype H is highly virulent on most small grain varieties. This characteristic makes biotype H ideal for comparative proteomics to investigate the basis of biotype virulence in aphids. In this study, we used comparative proteomics to identify protein expression differences associated with virulence. Aphid proteins involved in the tricarboxylic acid cycle, immune system, cell division, and antiapoptosis pathways were found to be up-regulated...
Cryptic virulence and avirulence alleles revealed by controlled sexual recombination in pea aphids
Although aphids are worldwide crop pests, little is known about aphid effector genes underlying virulence and avirulence. Here we show that controlling the genetics of both aphid and host can reveal novel recombinant genotypes with previously undetected allelic variation in both virulence and avirulence functions. Clonal F1 progeny populations were derived from reciprocal crosses and selfmatings between two parental genotypes of pea aphid (Acyrthosiphon pisum) differing in virulence on a Medicago truncatula host carrying the RAP1 and RAP2 resistance genes. These populations showed Mendelian segregation consistent with aphid performance being controlled largely by a dominant virulence allele derived from only one parent. Altered segregation ratios on near-isogenic host genotypes differing in the region carrying RAP1 were indicative of additional heritable functions likely related to avirulence genes originating from both parents. Unexpectedly, some virulent F1 progeny were recovered from selfing of an avirulent parent, suggesting a reservoir of cryptic alleles. Host chlorosis was associated with virulence whereas necrotic hypersensitive-like response was not. No maternal inheritance was found for any of these characters, ruling out sex-linked, cytoplasmic and endosymbiotic factors. Our results demonstrate the tractability of dissecting the genetic basis of pesthost resistance mechanisms, and indicate that the annual sexual cycle in aphids may lead to frequent novel genotypes with both increased and decreased virulence. Availability of genomes for both pest and host can facilitate definition of cognate gene-for-gene relationships, potentially leading to selection of crop genotypes with multiple resistance traits. the world's crops: an identification and information guide. John Wiley & Sons.
We propose sequencing of the 300Mb nuclear genome of the pea aphid, Acyrthosiphon pisum. Aphids display a diversity of biological problems that are not easily studied in other genetic model systems. First, because they are the premier model for the study of bacterial endosymbiosis and because they vector many well-studied plant viruses, aphids are an excellent model for studying animal interactions with microbes. Second, because their normal life cycle displays extreme developmental plasticity as well as both clonal and sexual reproduction, aphids provide the opportunity to understand the basis of phenotypic plasticity as well as the genomic consequences of sexual versus asexual reproduction. Their alternative reproductive modes can also be exploited in genetic experiments, because clones can be maintained indefinitely in the laboratory with sexual generations induced at will 1,2. Third, aphids provide some of the best studied instances of adaptation, in the form of both insecticide resistance, which has evolved through several molecular mechanisms, and host plant adaptation, which has repeatedly generated novel aphid lineages specialized to particular crop plant cultivars and which is presumably the basis for the radiation of aphids onto many specialized host plants during their long evolutionary history. Finally, an aphid genome will provide important phylogenetic information, serving as an outgroup to the many genomes being sequenced in holometabolous insects (flies, beetles, bees, moths) and providing a valuable resource for annotation of the genomes of other hemimetabolous insects, most of which have much larger genomes than the aphid. Aphid biology is relevant to human health in several ways. First, aphids cause crop damage on the order of hundreds of millions of dollars in lost production each year 3,4. Second, pest aphid populations are controlled primarily by pesticides. These pesticides may persist on harvested crops and in the environment, to the detriment of human health and environmental quality. Third, bacterial symbiosis in aphids may serve as a general model for understanding processes of bacterial infection 5-7. Fourth, aphids transmit some viruses in ways that resemble insect-borne human viruses and thus provide models for studying insect-vector viral disease 8,9. Finally, because aphids display dramatic phenotypic plasticity 10,11 , they provide a model system for how environmental and genetic factors interact in determining the phenotype. There is growing awareness that phenotypic plasticity, for example differential response to drugs, is an important component of human welfare 12. As a group, aphids are among the most intensively studied insects and are the focus of a large community of researchers. Several labs have developed genomic tools for studying aphids, including genetic maps, BAC libraries, EST sequences and microarrays.
Aphid-encoded variability in susceptibility to a parasitoid
BMC Evolutionary Biology, 2014
Background: Many animals exhibit variation in resistance to specific natural enemies. Such variation may be encoded in their genomes or derived from infection with protective symbionts. The pea aphid, Acyrthosiphon pisum, for example, exhibits tremendous variation in susceptibility to a common natural enemy, the parasitic wasp Aphidius ervi. Pea aphids are often infected with the heritable bacterial symbiont, Hamiltonella defensa, which confers partial to complete resistance against this parasitoid depending on bacterial strain and associated bacteriophages. That previous studies found that pea aphids without H. defensa (or other symbionts) were generally susceptible to parasitism, together with observations of a limited encapsulation response, suggested that pea aphids largely rely on infection with H. defensa for protection against parasitoids. However, the limited number of uninfected clones previously examined, and our recent report of two symbiont-free resistant clones, led us to explicitly examine aphid-encoded variability in resistance to parasitoids. Results: After rigorous screening for known and unknown symbionts, and microsatellite genotyping to confirm clonal identity, we conducted parasitism assays using fifteen clonal pea aphid lines. We recovered significant variability in aphid-encoded resistance, with variation levels comparable to that contributed by H. defensa. Because resistance can be costly, we also measured aphid longevity and cumulative fecundity of the most and least resistant aphid lines under permissive conditions, but found no trade-offs between higher resistance and these fitness parameters. Conclusions: These results indicate that pea aphid resistance to A. ervi is more complex than previously appreciated, and that aphids employ multiple tactics to aid in their defense. While we did not detect a tradeoff, these may become apparent under stressful conditions or when resistant and susceptible aphids are in direct competition. Understanding sources and amounts of variation in resistance to natural enemies is necessary to understand the ecological and evolutionary dynamics of antagonistic interactions, such as the potential for coevolution, but also for the successful management of pest populations through biological control.
BMC Genomics, 2014
Background: Grain aphid (Sitobion avenae F) and pea aphid (Acyrthosiphon pisum) are two agriculturally important pest species, which cause significant yield losses to crop plants each year by inflicting damage both through the direct effects of feeding and by vectoring debilitating plant viruses. Although a close phylogenetic relationship between grain aphid and pea aphid was proposed, the biological variations between these two aphid species are obvious. While the host ranges of grain aphid is restricted to cereal crops and in particular wheat, that of pea aphid is wider, mainly colonizing leguminous plant species. Until now, the genetic factors underlying the divergence between grain aphid and pea aphid still remain unclear due to the limited genomic data of grain aphid available in public databases. Results: Based on a set of transcriptome data of grain aphid generated by using Roche 454 GS-FLX pyrosequencing, comparative analysis between this set of transcriptome data of grain aphid and mRNA sequences of pea aphid available in the public databases was performed. Compared with mRNA sequences of pea aphid, 4,857 unigenes were found to be specifically presented in the transcriptome of grain aphid under the rearing conditions described in this study. Furthermore, 3,368 orthologous pairs which could be calculated with both nonsynonymous (Ka) and synonymous (Ks) substitutions were used to infer their sequence divergences. The average differences in the coding, 5′ and 3′ untranslated regions of these orthologs were 10.53%, 21.29% and 18.96%, respectively. Moreover, of 340 orthologs which were identified to have evolved in response to positive selection based on the rates of Ka and Ks substitutions, 186 were predicted to be involved in secondary metabolism and xenobiotic metabolisms which might contribute to the divergence of these two aphid species. Conclusions: The comprehensive transcriptome divergent sequence analysis between grain aphid and pea aphid provides an invaluable resource for the investigation of genes involved in host plant adaptation and evolution. Moreover, the demonstration of divergent transcriptome sequences between grain aphid and pea aphid pave the way for the investigation of the molecular mechanisms underpinning the biological variations of these two agriculturally important aphid species.
Insect Biochemistry and Molecular Biology, 2008
Host insects are either susceptible or resistant to parasitoids, where resistant hosts express immunity factors and compatible parasitoids express virulence factors that may reveal the manipulation of susceptible hosts. Using proteomics we compared responses of the same host, the aphid Macrosiphum euphorbiae, challenged by a well-adapted parasitoid Aphidius nigripes or by a less adapted relative, Aphidius ervi. The host was found to be equally acceptable to both parasitoids, but while A. nigripes normally developed and killed hosts (high susceptibility), development of the incompatible A. ervi was arrested at the primary egg stage (high resistance). Two-dimensional gels at two stages of parasitism revealed divergence in patterns of protein regulation of the M. euphorbiae host, responding to A. ervi or A. nigripes, with the greatest number of protein modulations in the host resistance response. In A. erviresistant hosts, proPO was strongly up-regulated, as were also three cuticle proteins, suggesting a PO basis and exoskeleton reinforcement as early and late responses of M. euphorbiae to the risk of parasitism. Resistance also correlated with up-regulation of antioxidative, energy-related, cytoskeleton and heat shock proteins. In A. nigripes-susceptible hosts, various proteins implicated in host and bacterial symbiont metabolism were significantly altered, suggesting complex host nutritional modulation. Over-expression of energy-related proteins also increased when A. nigripes established and developed. Aphid proteomes of compatible and incompatible Aphidius parasitism provide an integrative basis for consolidating our knowledge of host-parasitoid interactions.
PLoS Genetics, 2010
Aphids are amongst the most devastating sap-feeding insects of plants. Like most plant parasites, aphids require intimate associations with their host plants to gain access to nutrients. Aphid feeding induces responses such as clogging of phloem sieve elements and callose formation, which are suppressed by unknown molecules, probably proteins, in aphid saliva. Therefore, it is likely that aphids, like plant pathogens, deliver proteins (effectors) inside their hosts to modulate host cell processes, suppress plant defenses, and promote infestation. We exploited publicly available aphid salivary gland expressed sequence tags (ESTs) to apply a functional genomics approach for identification of candidate effectors from Myzus persicae (green peach aphid), based on common features of plant pathogen effectors. A total of 48 effector candidates were identified, cloned, and subjected to transient overexpression in Nicotiana benthamiana to assay for elicitation of a phenotype, suppression of the Pathogen-Associated Molecular Pattern (PAMP)-mediated oxidative burst, and effects on aphid reproductive performance. We identified one candidate effector, Mp10, which specifically induced chlorosis and local cell death in N. benthamiana and conferred avirulence to recombinant Potato virus X (PVX) expressing Mp10, PVX-Mp10, in N. tabacum, indicating that this protein may trigger plant defenses. The ubiquitin-ligase associated protein SGT1 was required for the Mp10-mediated chlorosis response in N. benthamiana. Mp10 also suppressed the oxidative burst induced by flg22, but not by chitin. Aphid fecundity assays revealed that in planta overexpression of Mp10 and Mp42 reduced aphid fecundity, whereas another effector candidate, MpC002, enhanced aphid fecundity. Thus, these results suggest that, although Mp10 suppresses flg22-triggered immunity, it triggers a defense response, resulting in an overall decrease in aphid performance in the fecundity assays. Overall, we identified aphid salivary proteins that share features with plant pathogen effectors and therefore may function as aphid effectors by perturbing host cellular processes.
Factors driving susceptibility and resistance in aphids that share specialist fungal pathogens
Current Opinion in Insect Science, 2019
Highlights Two aphid species in cereals, Sitobion avenae and Rhopalosiphum padi, share the fungal pathogens Pandora neoaphidis and Entomophthora planchoniana Aphid behavior and aphid morph are important factors governing host susceptibility and resistance, and endosymbionts may also play a role The life cycles of hosts and pathogens are influential to transmission routes of pathogens from conspecific to heterospecific host Laboratory experiments suggest that the conspecific host is more susceptible than the heterospecific host Secretome analysis of entomophthoralean infection in S. avenae suggest a weak hosts immune response