Biotic unpredictability and sexual reproduction: Do aphid genotype-host genotype interactions favor aphid sexuality?

Summary The possibility that genetic variation among host plants favors sexuality in aphids is explored in the context of Williams and Mitton's (1973) aphid-rotifer model of sib competition. A survey of studies concerning plant resistance to aphids suggests that conditions favoring sexuality can occur where different aphid genotypes are adapted to different host plant species, or where major plant resistance genes differentially affect colonizing success of aphid genotypes. These phenomena are apparently uncommon, however. Thus it is unlikely that genetic heterogeneity among host plants is of major importance for the retention of sexuality in aphid life cycles.     

The molecular bases of plant resistance and defense responses to aphid feeding: current status

Plant genes participating in the recognition of aphid herbivory in concert with plant genes involved in defense against herbivores mediate plant resistance to aphids. Several such genes involved in plant disease and nematode resistance have been characterized in detail, but their existence has only recently begun to be determined for arthropod resistance. Hundreds of different genes are typically involved and the disruption of plant cell wall tissues during aphid feeding has been shown to induce defense responses in Arabidopsis, Triticum, Sorghum, and Nicotiana species. Mi‐1.2, a tomato gene for resistance to the potato aphid, Macrosiphum euphorbiae (Thomas), is a member of the nucleotide‐binding site and leucine‐rich region Class II family of disease, nematode, and arthropod resistance genes. Recent studies into the differential expression of Pto‐ and Pti1‐like kinase genes in wheat plants resistant to the Russian wheat aphid, Diuraphis noxia (Mordvilko), provide evidence of the involvement of the Pto class of resistance genes in arthropod resistance. An analysis of available data suggests that aphid feeding may trigger multiple signaling pathways in plants. Early signaling includes gene‐for‐gene recognition and defense signaling in aphid‐resistant plants, and recognition of aphid‐inflicted cell damage in both resistant and susceptible plants. Furthermore, signaling is mediated by several compounds, including jasmonic acid, salicylic acid, ethylene, abscisic acid, giberellic acid, nitric oxide, and auxin. These signals lead to the development of direct chemical defenses against aphids and general stress‐related responses that are well characterized for a number of abiotic and biotic stresses. In spite of major plant taxonomic differences, similarities exist in the types of plant genes expressed in response to feeding by different species of aphids. However, numerous differences in plant signaling and defense responses unique to specific aphid–plant interactions have been identified and warrant further investigation.     

Independent action and contrasting phenotypes of resistance genes against spotted alfalfa aphid and bluegreen aphid in Medicago truncatula

Host resistance to aphids is poorly understood. Medicago truncatula, a model legume and cultivated pasture species, was used to elucidate defense against two aphid species, Therioaphis trifolii f. maculata (spotted alfalfa aphid, SAA) and Acyrthosiphon kondoi (bluegreen aphid, BGA). Aphid performance and plant damage were compared between near-isogenic cultivars, Mogul and Borung, that differ in resistance to both aphids. Analyses of aphid resistance in Mogul x Borung F2 plants and their progeny revealed modes of action and chromosome locations of resistance genes. Separate genes were identified for SAA resistance (TTR) and BGA resistance (AKR); both mapped to chromosome 3 but were found to act independently to reduce survival and growth of their target aphid species. The TTR locus controls distinct, and contrasting, local and systemic plant responses between the near-isogenic cultivars. TTR-mediated plant responses imply interaction between a resistance factor(s) in vascular tissue and a bioactive component(s) of SAA saliva. Features of both resistance traits suggest homology to aphid resistance in other legumes; elucidation of their molecular mechanisms will likely apply to other aphid-plant interactions.     

Fitness trade-off in peach-potato aphids (Myzus persicae) between insecticide resistance and vulnerability to parasitoid attack at several spatial scales

Insecticide-resistant clones of the peach-potato aphid, Myzus persicae (Sulzer), have previously been shown to have a reduced response to aphid alarm pheromone compared to susceptible ones. The resulting vulnerability of susceptible and resistant aphids to attack by the primary endoparasitoid, Diaeretiella rapae (McIntosh), was investigated across three spatial scales. These scales ranged from aphids confined on individual leaves exposed to single female parasitoids, to aphids on groups of whole plants exposed to several parasitoids. In all experiments, significantly fewer aphids from insecticide-susceptible clones became parasitised compared to insecticide-resistant aphids. Investigations of aphid movement showed at the largest spatial scale that more susceptible aphids than resistant aphids moved from their inoculation leaves to other leaves on the same plant after exposure to parasitoids. The findings imply that parasitoids, and possibly other natural enemies, can influence the evolution and dynamics of insecticide resistance through pleiotropic effects of resistance genes on important behavioural traits.     

Field and laboratory evaluations of soybean lines against soybean aphid (Hemiptera: Aphididae)

The soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), is a major pest of soybean, Glycine max (L.). Merr., that significantly reduces yield in northern production areas of North America. Insecticides are widely used to control soybean aphid outbreaks, but efforts are underway to develop host plant resistance as an effective alternative management strategy. Here, previously identified resistant lines were evaluated in laboratory tests against field-collected populations of soybean aphid and in field-plot tests over 2 yr in South Dakota. Six lines previously identified with resistance to soybean aphid--Jackson, Dowling, K1639, Cobb, Palmetto and Sennari--were resistant in this study, but relatively high aphid counts on Tie-feng 8 in field plots contrasted with its previously reported resistance. Bhart-PI 165989 showed resistance in one of two laboratory tests, but it had relatively large aphid infestations in both years of field tests. Intermediate levels of soybean aphid occurred in field plots on lines previously shown to have strong (Sugao Zairai, PI 230977, and D75-10169) or moderate resistance to soybean aphid (G93-9223, Bragg, Braxton, and Tracy-M). Sugao Zairai also failed to have a significant proportion of resistant plants in two laboratory tests against aphids field-collected in 2008, but it was resistant in laboratory tests with aphids collected in 2002, 2005, and 2006. Overall, results showed that lines with Rag (i.e., Jackson) or Rag1 gene (i.e., Dowling) had low aphid numbers, whereas lines with Rag2 (i.e., Sugao Zairai, Sennari) had mixed results. Collectively, responses of soybean aphid populations in laboratory and field tests in 2008 resembled a virulence pattern reported previously for biotype 3 soybean aphids, but virulence in soybean aphid populations was variable and dynamic over years of the study. These results, coupled with previous reports of biotypes virulent to Rag1, suggest that deployment of lines with a single aphid-resistance gene is limited for soybean aphid management, and that deployment strategies relying on multiple resistance genes may be needed to effectively use plant resistance against soybean aphid.     

Plant-aphid interactions: molecular and ecological perspectives

Many aphids are major agricultural pests because of their unparalleled reproductive capacity and their ability to manipulate host plant physiology. Aphid population growth and its impact on plant fitness are strongly influenced by interactions with other organisms, including plant pathogens, endophytes, aphid endosymbionts, predators, parasitoids, ants, and other herbivores. Numerous molecular and genomic resources have recently been developed to identify sources of aphid resistance in plants, as well as potentially novel targets for control in aphids. Moreover, the same model systems that are used to explore direct molecular interactions between plants and aphids can be utilized to study the ecological context in which they occur.     

Facultative 'secondary' bacterial symbionts and the nutrition of the pea aphid, Acyrthosiphon pisum

Abstract.  Facultative 'secondary' bacterial symbionts influence various traits of aphids, including plant utilization patterns and resistance to parasitoids. The present study is designed to test the hypothesis that these multiple effects are underlain by symbiont-mediated changes to the aphid requirement for the dominant dietary nutrients, sucrose and amino acids. The performance of pea aphids ( Acyrthosiphon pisum ) on chemically defined diets of systematically altered sucrose and amino acid content varies among eight parthenogenetic clones, with a pattern that does not match the aphid complements of secondary symbionts, Hamiltonella defensa , Regiella insecticola and Serratia symbiotica . Aphid performance is reduced, increased and unaffected by elimination of S. symbiotica , R. insecticola and H. defensa , respectively, but with no significant effect on the range of diets on which aphids performed well. It is concluded that the impact of secondary symbionts on aphid traits is most unlikely to have a purely nutritional basis.     

蚜虫唾液蛋白研究进展

蚜虫属于半翅目蚜科,多为重要的农业害虫,通过刺吸式口器吸食植物汁液,传播病毒,其爆发常常造成重大经济损失。在漫长的协同进化历程中,植物建立了高效的防御系统以应对蚜虫威胁。为了克服植物的防御反应,蚜虫也发展了相应的反制手段,其中蚜虫在取食过程中分泌的唾液蛋白能调控植物防御反应,降解植物次生物质,从而在蚜虫与植物互作中发挥着至关重要的作用。本文综述了蚜虫唾液蛋白的组分鉴定方法和相关蛋白的功能,并对唾液蛋白在蚜虫防治的应用和今后的研究方向进行了展望。常见的蚜虫唾液蛋白组分的鉴定和分析方法包括唾液蛋白的酶活性分析、唾液蛋白组学分析、唾液腺转录组学和蛋白组学分析等。但这些方法各有利弊,仅采取一种分析方法不能客观全面地反映蚜虫唾液蛋白分泌谱,多种技术手段联合分析方可提供更为逼真详实的信息。蚜虫唾液蛋白种类繁多,可分为解毒酶、保护酶、水解酶、结合功能蛋白以及分类未知的效应蛋白等。蚜虫唾液蛋白功能多样,能参与唾液鞘的形成,诱导植物防御反应,促进蚜虫取食,提高蚜虫繁殖力等。通过RNAi干扰唾液蛋白编码基因会显著改变蚜虫取食行为,并降低蚜虫存活率、产蚜量和适合度。因此,唾液蛋白是防控蚜虫的理想靶标。目前,采用寄主诱导的基因沉默(host-induced gene silencing, HIGS)技术已培育了数种靶向唾液蛋白基因的高效抗蚜作物品系,展示出了良好的应用前景。从目前研究来看,各种蚜虫唾液蛋白谱急需采用多组学手段联合分析的方法来进行完整解析。各种唾液蛋白的具体功能方面的研究还严重缺乏,需从蚜虫、植物、两者之间的互作等多维度探究唾液蛋白的作用及相关的分子机制,为发展基于蚜虫唾液蛋白调控的蚜虫防治新策略打下基础。     

Field evaluation of emmer wheat-derived synthetic hexaploid wheat for resistance to Russian wheat aphid (Homoptera: Aphididae)

Broadening the genetic base for resistance to Russian wheat aphid, Diuraphis noxia (Mordvilko) (Homoptera: Aphididae), in bread wheat, Triticum aestivum L., is desirable. To date, identified Russian wheat aphid resistance genes are either located to the D chromosomes or to rye translocation of wheat, and resistance derived from the A or B genomes of tetraploid Triticum spp. would therefore be highly beneficial. Fifty-eight synthetic hexaploid wheat, derived from interspecific crosses of Triticum dicoccum Schrank. and Aegilops tauschii (Coss.) Schmal. and their parents were evaluated for resistance to Russian wheat aphid under field conditions. Plots infested with aphids were compared with plots protected with insecticides. The T. dicoccum parents were highly resistant to Russian wheat aphids, whereas the Ae. tauschii parents were susceptible. Resistance levels observed in the synthetic hexaploids were slightly below the levels of their T. dicoccum parents when a visual damage scale was used. but no major resistance suppression was observed among the synthetics. Russian wheat aphid infestation on average reduced plant height and kernel weight at harvest in the synthetic hexaploids and the T. dicoccum parents by 3-4%, whereas the susceptible control 'Seri M82' suffered losses of above 20%. Because resistance in the synthetic hexaploid wheat is derived from their T. dicoccum parent, resistance gene(s) must be located on the A and/or B genomes. They must therefore be different from previously identified Russian wheat aphid resistance genes, which have all been located on the D genome of wheat or on translocated segments.     

Overexpression of IRM1 Enhances Resistance to Aphids in Arabidopsis thaliana

Aphids are insects that cause direct damage to crops by the removal of phloem sap, but more importantly they spread devastating viruses. Aphids use their sophisticated mouthpart (i.e. stylet) to feed from the phloem sieve elements of the host plant. To identify genes that affect host plant resistance to aphids, we previously screened an Arabidopsis thaliana activation tag mutant collection. In such mutants, tagged genes are overexpressed by a strong 35S enhancer adjacent to the natural promoter, resulting in a dominant gain-of-function phenotype. We previously identified several of these mutants on which the aphid Myzus persicae showed a reduced population development compared with wild type. In the present study we show that the gene responsible for the phenotype of one of the mutants is At5g65040 and named this gene Increased Resistance to Myzus persicae 1 (IRM1). Overexpression of the cloned IRM1 gene conferred a phenotype identical to that of the original mutant. Conversely, an IRM1 knockout mutant promoted aphid population development compared to the wild type. We performed Electrical Penetration Graph analysis to investigate how probing and feeding behaviour of aphids was affected on plants that either overexpressed IRM1 or contained a knockout mutation in this gene. The EPG results indicated that the aphids encounter resistance factors while reaching for the phloem on the overexpressing line. This resistance mechanism also affected other aphid species and is suggested to be of mechanical nature. Interestingly, genetic variation for IRM1 expression in response to aphid attack was observed. Upon aphid attack the expression of IRM1 was initially (after 6 hours) induced in ecotype Wassilewskija followed by suppression. In Columbia-0, IRM1 expression was already suppressed six hours after the start of the infestation. The resistance conferred by the overexpression of IRM1 in A. thaliana trades off with plant growth.     

Biology and trophic interactions of lucerne aphids

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Transcriptional profile and differential fitness in a specialist milkweed insect across host plants varying in toxicity

Interactions between plants and herbivorous insects have been models for theories of specialization and co‐evolution for over a century. Phytochemicals govern many aspects of these interactions and have fostered the evolution of adaptations by insects to tolerate or even specialize on plant defensive chemistry. While genomic approaches are providing new insights into the genes and mechanisms insect specialists employ to tolerate plant secondary metabolites, open questions remain about the evolution and conservation of insect counterdefences, how insects respond to the diversity defences mounted by their host plants, and the costs and benefits of resistance and tolerance to plant defences in natural ecological communities. Using a milkweed‐specialist aphid (Aphis nerii) model, we test the effects of host plant species with increased toxicity, likely driven primarily by increased secondary metabolites, on aphid life history traits and whole‐body gene expression. We show that more toxic plant species have a negative effect on aphid development and lifetime fecundity. When feeding on more toxic host plants with higher levels of secondary metabolites, aphids regulate a narrow, targeted set of genes, including those involved in canonical detoxification processes (e.g., cytochrome P450s, hydrolases, UDP‐glucuronosyltransferases and ABC transporters). These results indicate that A. nerii marshal a variety of metabolic detoxification mechanisms to circumvent milkweed toxicity and facilitate host plant specialization, yet, despite these detoxification mechanisms, aphids experience reduced fitness when feeding on more toxic host plants. Disentangling how specialist insects respond to challenging host plants is a pivotal step in understanding the evolution of specialized diet breadths.     

Compatibility of aphid resistance in soybean and biological control by the parasitoid Aphidius colemani (Hymenoptera: Braconidae)

Biological control and soybean cultivars bred for increased resistance to the soybean aphid (Aphis glycines) are two approaches used to manage this serious pest of soybeans in North America. However, as with many other pest systems, the compatibility of these two pest management approaches has not been studied in detail. The aphidiine wasp Aphidius colemani is one of several candidate species for biological control of the soybean aphid in soybean in North America. Resistance to the soybean aphid in the USDA soybean cultivar Dowling is largely controlled by a single dominant gene Rag1, which is the focus of plant breeding programs directed against the soybean aphid. In this study, we measured developmental and behavioral differences in the parasitic wasp A. colemani when it attacked soybean aphids feeding on either the aphid-resistant Dowling or aphid-susceptible Glenwood cultivars of soybean. We used a combination of choice and no-choice experiments to examine the effects of host plant cultivar on the number of parasitized aphids formed and the sex ratio and body weights of adult offspring produced. Significantly more aphids were parasitized when they fed on Glenwood compared to Dowling and these offspring were larger when they developed in aphids that fed on Glenwood soybeans. To distinguish between effects on foraging decisions and offspring survivorship, we conducted an additional experiment that followed the oviposition decisions and fate of each parasitized aphid. Foraging female A. colemani spent less time handling individual aphids and encountered and attacked aphids at a higher rate when they fed on aphids feeding on Glenwood soybeans than aphids feeding on Dowling soybeans. Furthermore, wasp survivorship in aphids was greater on Glenwood than Dowling. Taken together, aphid-resistance in soybeans has negative effects on foraging behavior and offspring fitness of A. colemani raising concerns about the compatibility of these two pest management approaches.     

Transgenic potatoes with enhanced levels of nematode resistance do not have altered susceptibility to nontarget aphids

Cysteine proteinase inhibitors (cystatins) confer resistance to plant-parasitic nematodes when expressed in transgenic plants. The survival and growth of nymphs of the peach-potato aphid, Myzus persicae, were adversely affected when cystatins were added to artificial diets. When aphids were clip-caged onto transgenic plants expressing chicken egg white cystatin (CEWc) there was no adverse effect on aphid fitness. Field populations of aphids on transgenic Desiree potatoes, expressing CEWc or a modified version of oryzacystatin I, were not significantly different from populations on control Desiree plants. The effect of other nematode management options on aphid numbers was also studied. A conventionally bred cultivar, with partial nematode resistance, supported higher populations of aphids than the transgenic lines at the beginning of the sampling period. Peak aphid densities on the untreated control and untreated transgenic lines were 7 and 5.2 aphids per plant. Aldicarb, commonly used to control nematodes on potatoes, reduced the value to less than 0.2 aphids per plant. The results demonstrate that levels of expression in the plant tissue actually consumed are important in determining the risk of cystatins to nontarget invertebrates. The study also highlights the importance of including currently used management options in any assessment of the impact of transgenic plants on nontarget organisms.     

Combined effects of host-plant resistance and intraguild predation on the soybean aphid parasitoid Binodoxys communis in the field

Soybean varieties that exhibit resistance to the soybean aphid Aphis glycines have been developed for use in North America. In principle, host-plant resistance to soybean aphid can influence the interactions between the soybean aphid and its natural enemies. Resistance could change the quality of soybean aphids as a food source, the availability of soybean aphids, or resistance traits could directly affect aphid predators and parasitoids. Here, we focus on the effect of soybean aphid resistance on the interactions between soybean aphids, the parasitoid Binodoxys communis (Hymenoptera: Braconidae), and predators of these two species. We determined whether host-plant resistance affected within-season persistence of B. communis by releasing parasitoids into resistant and susceptible soybean plots. We observed higher B. communis densities in susceptible soybean plots than in resistant plots. There were also higher overall levels of intraguild predation of B. communis in susceptible plots, although the per-capita risk of intraguild predation of B. communis was affected neither by plant genotype nor by aphid density. We discuss these effects and whether they were caused by direct effects of the resistant plants on B. communis or indirect effects through soybean aphid or predators.     

Association between Aphis gossypii genotype and phenotype on melon accessions

Development of molecular markers has allowed the characterization of several host–aphid interactions. We investigated the usefulness of microsatellite markers to characterize the plant resistance interaction in the model Aphis gossypii/Cucumis melo. Six aphid clones, collected in different localities and years and belonging to two multilocus genotypes (MLGs) based on eight microsatellite markers, were phenotyped on a set of 33 melon accessions, some of them known to carry the Vat gene. Three parameters were used: acceptance of plant, ability to colonize the plant and resistance to virus when inoculated by aphids. Concordance and correlation analyses showed that aphid clones sharing a same MLG exhibited a very agreeable phenotype on the set of accessions for acceptance of plant and resistance to virus when inoculated by aphids. From host point of view, melon accessions were grouped into four clear categories, resistant to aphids of both MLGs, only resistant to the NM1 MLG, only resistant to the C9 MLG, susceptible to both MLGs and another group of unclear characteristics. The four categories revealed different patterns of virulence for NM1 and C9 MLGs that are likely controlled by a single avirulence gene in accordance with a gene for gene interaction. In contrast, the ability to colonize the plant appeared slightly variable among clones sharing a same MLG. We hypothesize it is due to the putative polygenic control of this aphid trait. Because the phenotypic variability of A. gossypii matched the genetic variability revealed by eight microsatellite markers, these markers could be used to infer the frequency of biotypes in field experiments and help to elucidate the allele diversity of melon resistance genes.     

Tolerance of antibiotic and susceptible cereal seedlings to the aphids Metopolophium dirhodum and Rhopalosiphum padi

Some cereal seedlings exhibit antibiotic and antixenotic resistance to the aphids Metopolophium dirhodum (Walker) and Rhopalosiphum padi (L.), because the seedlings contain hydroxamic acids or gramine. The association between tolerance to aphids and aphid antibiosis was investigated for three cereals, Dollarbird wheat Vulcan wheat and Yagan barley. The dry biomass gained by the aphids and the simultaneous reduction in the biomass of the plants (biomass conversion ratio) quantified tolerance. Biomass production and the density dependence of biomass production by the aphids quantified antibiosis more effectively than fecundity. Vulcan wheat, which has more hydroxamic acid than Dollarbird wheat showed the highest level of antibiosis, and the barley was not antibiotic for either aphid. The biomass conversion ratio was a constant; the biomass of an infested plant was reduced by 3 mg for each mg of aphid biomass gained, regardless of aphid species, plant cultivar, or aphid density. The three plants showed no differential tolerance to the aphids, and therefore tolerance is not associated with antibiosis in this case.