Genetic, biochemical, and behavioral uniformity among populations of Myzus nicotianae and Myzus persicae

Prior to designation as distinct species, an appellation presently in question, the tobacco aphid, Myzus nicotianae Blackman (Homoptera: Aphididae), was classified as a tobacco-feeding form of the green peach aphid, Myzus persicae (Sulzer). In this study, RAPD polymorphisms distinguished members of the Myzus persicae complex (M. persicae and M. nicotianae) from three outgroup Myzus species (M. cerasi (F.), M. hemerocallis Takahashi, and M. varians Davidson). Polymorphisms within the complex did not separate populations on the basis of host association (tobacco versus other host plants) or geographic origin (collections from the United States, Europe, and Japan). Similarly, while GC-MS analysis of cuticular hydrocarbon profiles revealed both developmental and inter-populational differences within the M. persicae complex, it did not separate populations of tobacco feeding aphids from those collected off non-tobacco hosts. Finally, with the exception of their responses to a choice between lettuce and collards, the host preference behavior of a green peach aphid population, a red tobacco aphid population, and a green tobacco aphid population was indistinguishable in host preference experiments. These results add to a growing body of evidence suggesting M. nicotianae and M. persicae are conspecific.     

Response of Solanum tuberosum to Myzus persicae infestation at different stages of foliage maturity

Young leaves of the potato Solanum tuberosum L. cultivar Kardal contain resistance factors to the green peach aphid Myzuspersicae （Sulzer） （Hemiptera： Aphididae） and normal probing behavior is impeded. However, M. persicae can survive and reproduce on mature and senescent leaves of the cv. Kardal plant without problems. We compared the settling ofM. persicae on young and old leaves and analyzed the impact of aphids settling on the plant in terms of gene expression. Settling, as measured by aphid numbers staying on young or old leaves, showed that after 21 h significantly fewer aphids were found on the young leaves. At earlier time points there were no difference between young and old leaves, suggesting that the young leaf resistance factors are not located at the surface level but deeper in the tissue. Gene expression was measured in plants at 96 h postinfestation, which is at a late stage in the interaction and in compatible interactions this is long enough for host plant acceptance to occur. In old leaves of cv. Kardal （compatible interaction）, M. persicae infestation elicited a higher number of differentially regulated genes than in young leaves. The plant response to aphid infestation included a larger number of genes induced than repressed, and the proportion of induced versus repressed genes was larger in young than in old leaves. Several genes changing expression seem to be involved in changing the metabolic state of the leaf from source to sink.     

Aphids (Hemiptera,Aphididae) on ornamental plants in greenhouses in Bulgaria

Investigations on the species composition and host range of aphids on ornamental greenhouse plants in Bulgaria was conducted over a period of five years, from 2008 to 2012. Twenty greenhouses, growing ornamentals for landscaping, plant collections and other purposes were observed. They were located in the regions of Sofia, Plovdiv, Smolyan, Pavlikeni, Varna and Burgas. The total number of collected aphid samples was 279. Their composition included 33 aphid species and one subspecies from 13 genera and 5 subfamilies. Twenty-eight species were found to belong to subfamily Aphidinae. Almost 70 % of all recorded species were polyphagous. The most widespread aphid species was Myzus persicae, detected in 13 greenhouses all year round, followed by Aulacorthum solani (10 greenhouses) and Aphis gossypii (9 greenhouses). The widest host range was shown by Myzus persicae (43 hosts), Aulacorthum solani (32 hosts) and Aulacorthum circumflexum (23 hosts).The list of host plants includes 114 species from 95 genera and 58 families. The greatest variety of aphid species was detected on Hibiscus (9 species). Out of all aphid samples 12.9 % were collected on Hibiscus and 6.8 %, on Dendranthema. The greatest variety of aphid species was detected on Hibiscus (9 species).Periphyllus californiensis and Aphis (Aphis) fabae mordvilkoi are reported for the first time for Bulgaria. Furthermore, Aphis spiraecola has been found in new localities and has widened its host range in this country.     

Suitability of three aphid species for Aphidius gifuensis (Hymenoptera: Braconidae): Parasitoid performance varies with hosts of origin

Oviposition behavior and offspring fitness of the parasitoid Aphidius gifuensis (Ashmead) were compared on three aphid species, Sitobion avenae F., Myzus persicae (Sulzer), and Aphis gossypii Glover using wasps collected from both S. avenae and M. persicae. A. gifuensis produced more mummies and adults on S. avenae and M. persicae than on A. gossypii regardless of the host of origin. Mummy production was influenced by attack rate and percentage of aphids superparasitized. The F₁ generations from S. avenae and M. persicae were more female-biased and wasps were larger than those from A. gossypii. Although there were significant differences in development time of A. gifuensis in the three aphid species, the difference was generally shorter than one day. Fewer mummies were produced when A. gifuensis was transferred between S. avenae and M. persicae, but no significant difference was observed in emergence rate, percentage of female offspring, or body size. The effects of host species on A. gifuensis female performance and offspring fitness are discussed, along with the potential for using A. gifuensis to control M. persicae and A. gossypii.     

Attraction of the predator,Harmonia axyridis (Coleoptera: Coccinellidae), to its prey,Myzus persicae (Hemiptera: Aphididae), feeding on Chinese cabbage

The predatory multicolored Asian lady beetle, Harmonia axyridis, was attracted to volatiles released from Chinese cabbage infested by the green peach aphid, Myzus persicae, in T-tube olfactometer choice tests. However, lady beetle adults and larvae did not respond to clean air, Chinese cabbage alone or green peach aphid alone. Of different prey densities, H. axyridis adults were most attracted to Chinese cabbage infested by 60 M. persicae adults after 24 h. However, H. axyridis larvae were not attracted to Chinese cabbage infested by M. persicae. Mechanically damaged Chinese cabbage attracted neither lady beetle adults nor larvae. Predatory adults were attracted to 60 M. persicae adults after 24 and 48 h, and to 90 M. persicae adults after 12 h, suggesting that the predatory response depends on the prey density. Lady adult beetles did not prefer the volatiles induced by Diamondback moth, Plutella xylostella, indicating that specific host insect specificity attracts respective natural enemies. It can be explained that the volatile compounds emitted from the host plant as a result of herbivore attack preferred by the specific insect species.     

Host Generated siRNAs Attenuate Expression of Serine Protease Gene in Myzus persicae

Background

Sap sucking hemipteran aphids damage diverse crop species. Although delivery of ds-RNA or siRNA through microinjection/feeding has been demonstrated, the efficacy of host-mediated delivery of aphid-specific dsRNA in developing aphid resistance has been far from being elucidated.

Methodology/Principal Findings

Transgenic Arabidopsis expressing ds-RNA of Myzus persicae serine protease (MySP) was developed that triggered the generation of corresponding siRNAs amenable for delivery to the feeding aphids. M. persicae when fed on the transgenic plants for different time intervals under controlled growth conditions resulted in a significant attenuation of the expression of MySP and a commensurate decline in gut protease activity. Although the survivability of these aphids was not affected, there was a noticeable decline in their fecundity resulting in a significant reduction in parthenogenetic population.

Conclusions/Significance

The study highlighted the feasibility of developing host based RNAi-mediated resistance against hemipteran pest aphids.     

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.     

Biological performance of Myzus persicae and Macrosiphum euphorbiae (Homoptera: Aphididae) on seven wild Solanum species

Resistance level of seven accessions of wild Solanum species (Solanaceae) to Myzus persicae and Macrosiphum euphorbiae (Homoptera: Aphididae) was evaluated by measuring survival and fecundity during sleeve cage experiments and population growth on whole plants in a controlled environment. The survival was lowest on the Solanum circaeifolium spp. capsicibaccatum, Solanum pinnatisectum and Solanum trifidum accessions for M. persicae and on the S. circaeifolium spp. capsicibaccatum, Solanum okadae and S. trifidum, accessions with M. euphorbiae. Plant species significantly influenced the fecundity of both aphid species. Aphid population growth on whole plants was negatively affected by the age of the plant, but generally followed the levels of net reproductive rate on different plant species observed during the sleeve cage experiment. The population of M. persicae varied among the seven wild potato accessions with the lowest growth rates on S. circaeifolium spp. capsicibaccatum, Solanum polyadenium, Solanum tarijense and S. trifidum. The number of M. euphorbiae also varied among accessions but the smallest population was collected from S. polyadenium. The results can be used to identify sources of resistance to aphids within those accessions already known to be resistant to the Colorado potato beetle. This study highlights the difficulties involved in developing a high-throughput screening test for aphid resistance compatible with a potato breeding programme.     

‘Myrosin cells’ are not a prerequisite for aphid feeding on oilseed rape (Brassica napus) but affect host plant preferences

The enzyme myrosinase (EC 3.2.3.1.147) is present in specialised myrosin cells and forms part of the glucosinolate–myrosinase system, also known as ‘the mustard oil bomb’, which has an important role in the defence system of cruciferous plants against insect pests. Transgenic Brassica napus MINELESS have been produced by transgenic ablation of myrosin cells. This prompted us to investigate the importance of myrosin cells in plant–aphid interactions. In order to study this, we challenged transgenic MINELESS and wild‐type cultivar Westar seedlings with the aphids Brevicoryne brassicae (a specialist) and Myzus persicae (a generalist). Our study included aphid free‐choice and aphid fecundity experiments. Data from these experiments showed that B. brassicae prefers wild‐type seedlings and M. persicae prefers MINELESS. B. brassicae and M. persicae showed significant variation in establishment on plants regardless of whether they were wild type or MINELESS and also differed significantly in affecting plant parts. Myrosinase activity in MINELESS control seedlings was 83.6% lower than the wild‐type control seedlings. Infestation with either of the two aphid species induced myrosinase levels in both wild‐type and MINELESS seedlings. Infestation with M. persicae reduced the concentration of most glucosinolates while B. brassicae had the opposite effect. B. brassicae enhanced the formation of glucosinolate hydrolysis products both in wild‐type and MINELESS seedlings. However, M. persicae decreased All ITC but increased 3,4ETBut NIT in wild‐type seedlings. Taken together, the investigation shows that the presence of myrosin cells affects the preference of generalist and specialist aphid species for Brassica napus plants.     

Local and systemic responses induced by aphids in Solanum tuberosum plants

The aphids Macrosiphum euphorbiae (Thomas) and Myzus persicae (Sulzer) (Homoptera: Aphididae) are serious pests of potato (Solanum tuberosum L.) (Solanaceae), notably in transmitting several plant viruses. Heterospecific interactions may occur between these two species as they are often seen at the same time on the same potato plant in the field. As aphid infestation is known to induce both local and systemic changes, we conducted experiments to determine the effect of previous infestation on probing behaviour and feeding‐related parameters. We used the DC electrical penetration graph technique to characterize the influence of previous infestation by conspecific M. persicae or by heterospecific Ma. euphorbiae on M. persicae feeding behaviour at both local and systemic levels, i.e., on previously infested leaves and on non‐previously infested leaves of infested plants, respectively. Conspecific and heterospecific infestation led to similar modification of M. persicae feeding activities. However, the effects of previous infestation occurring at the local level were opposite to those observed at the systemic level. Myzus persicae food acceptance was slightly enhanced on previously infested leaves, whereas it was inhibited on non‐infested leaves of infested plants, which indicated an induced resistance mechanism. Our results advance the understanding of the mechanisms involved in aphid–host plant acceptance and colonization processes on potato plants in conspecific and heterospecific situations.     

The effect of co-infestation by conspecific and heterospecific aphids on the feeding behaviour of <Emphasis Type="Italic">Nasonovia ribisnigri</Emphasis> on resistant and susceptible lettuce cultivars

Aphid saliva can suppress the blocking of sieve elements, a reaction that plants employ to inhibit aphid feeding, but aphid saliva can also elicit plant defence responses. Such plant responses might affect interactions between different aphid species and intraspecifically, e.g. among different biotypes. The objectives of our study were to investigate if feeding behaviour and performance of two biotypes of the lettuce aphid Nasonovia ribisnigri are affected by (1) feeding by the other biotype and (2) feeding by the green peach aphid Myzus persicae or the potato aphid Macrosiphum euphorbiae. Additionally the effect of feeding in a group was studied. All experiments were performed on both a resistant and an isogenic susceptible lettuce cultivar. Feeding or probing by conspecific or heterospecific aphids had different effects on Nasonovia ribisnigri biotypes. Aphids were only slightly affected by feeding or probing of the same biotype on both susceptible and resistant lettuce. N. ribisnigri virulent biotype Nr:1 suppressed the resistance against Nr:0 in the resistant cultivar. In contrast, defence was induced by Nr:1 against Nr:0 in susceptible lettuce. Co-infestation by M. euphorbiae and M. persicae had minor effects on Nr:0. Defence against Nr:1 was induced on both susceptible lettuce and resistant lettuce by Nr:0 and M. euphorbiae. Additionally, M. persicae induced defence in resistant lettuce against Nr:1. Effectors in the saliva of Nr:1 aphids are likely responsible for the defence suppression in lettuce. Identification of these effectors could lead to a better understanding of the mechanism of virulence in N. ribisnigri.     

Infection of Arabidopsis by cucumber mosaic virus triggers jasmonate-dependent resistance to aphids that relies partly on the pattern-triggered immunity factor BAK1

Many aphid-vectored viruses are transmitted nonpersistently via transient attachment of virus particles to aphid mouthparts and are most effectively acquired or transmitted during brief stylet punctures of epidermal cells. In Arabidopsis thaliana, the aphid-transmitted virus cucumber mosaic virus (CMV) induces feeding deterrence against the polyphagous aphid Myzus persicae. This form of resistance inhibits prolonged phloem feeding but promotes virus acquisition by aphids because it encourages probing of plant epidermal cells. When aphids are confined on CMV-infected plants, feeding deterrence reduces their growth and reproduction. We found that CMV-induced inhibition of growth as well as CMV-induced inhibition of reproduction of M. persicae are dependent upon jasmonate-mediated signalling. BRASSINOSTEROID INSENSITIVE1-ASSOCIATED KINASE1 (BAK1) is a co-receptor enabling detection of microbe-associated molecular patterns and induction of pattern-triggered immunity (PTI). In plants carrying the mutant bak1-5 allele, CMV induced inhibition of M. persicae reproduction but not inhibition of aphid growth. We conclude that in wildtype plants CMV induces two mechanisms that diminish performance of M. persicae: a jasmonate-dependent and PTI-dependent mechanism that inhibits aphid growth, and a jasmonate-dependent, PTI-independent mechanism that inhibits reproduction. The growth of two crucifer specialist aphids, Lipaphis erysimi and Brevicoryne brassicae, was not affected when confined on CMV-infected A. thaliana. However, B. brassicae reproduction was inhibited on CMV-infected plants. This suggests that in A. thaliana CMV-induced resistance to aphids, which is thought to incentivize virus vectoring, has greater effects on polyphagous than on crucifer specialist aphids.     

Probing behavior of aposymbiotic green peach aphid (Myzus persicae) on susceptible Solanum tuberosum and resistant Solanum stoloniferum plants

The green peach aphid, Myzus persicae Sulzer (Hemiptera: Aphididae) is one of the potato important pests; it is the most efficient vector of potato viruses. Myzus persicae harbors the endosymbiotic bacteria Buchnera aphidicola which supplements their diet. There is increasing evidence that B. aphidicola is involved in plant–aphid interactions and we previously demonstrated that B. aphidicola disruption (aposymbiosis) affected the probing behavior of M. persicae on radish plants, delaying host plant acceptance. In this work, we evaluated the effect of aposymbiosis on the probing behavior of M. persicae on 2 Solanum species with different compatibility with M. persicae, Solanum tuberosum (susceptible) and Solanum stoloniferum (resistant) with the electrical penetration graph technique (EPG). To disrupt B. aphidicola, rifampicin was administered to aphids through artificial diets. Aposymbiotic aphids, on both plant species, showed increased pathway activities, mechanical problems with the stylets, and delayed salivation in the phloem. The extended time in derailed stylet mechanics affected the occurrence of most other probing activities; it delayed the time to the first phloem phase and prevented ingestion from the phloem. The effect of aposymbiosis was more evident in the compatible interaction of M. persicae–S. tuberosum, than in the incompatible interaction with S. stoloniferum, which generated the M. persicae–S. tuberosum interaction to become incompatible. These results confirm that B. aphidicola is involved in the plant–aphid interaction in relation to plant acceptance, presumably through a role in stylets penetration in the plant.     

Host range limitation caused by incomplete host regulation in an aphid parasitoid

Defining host ranges in parasitoid insects is important both from a theoretical and an applied point of view. Based on the literature, some species seem able to use a wide range of hosts, while field studies indicate possible local host specialization. In koinobiont endoparasitoid species, such specialization could involve physiological processes. We tested the ability of two strains of the cosmopolitan and polyphagous parasitoid Diaeretiella rapae, to develop in three of its recorded aphid host species. Both strains produced high parasitism rates on the cabbage aphid Brevicoryne brassicae and the green peach aphid Myzus persicae but almost no progeny on the cherry-oat aphid Rhopalosiphum padi. This last species was less attacked by female parasitoids. Moreover, parasitoid eggs and larvae were smaller than in the two other host aphid species and their development was delayed. This abnormal development appeared to be due to an incomplete host regulation process, probably related to the low number and the size of teratocytes produced by D. rapae in R. padi individuals. Such a failure as far as gaining control of the host's metabolism is concerned could play an important role in shaping the host range of parasitoid insects, leading to local variation of the host spectrum in populations from various geographical areas.     

Comparative analysis of Solanum stoloniferum responses to probing by the green peach aphid Myzus persicae and the potato aphid Macrosiphum euphorbiae

Abstract Plants protect themselves against aphid attacks by species‐specific defense mechanisms. Previously, we have shown that Solanum stoloniferum Schlechtd has resistance factors to Myzus persicae Sulzer (Homoptera: Aphididae) at the epidermal/mesophyll level that are not effective against Macrosiphum euphorbiae Thomas (Homoptera: Aphididae). Here, we compare the nymphal mortality, the pre‐reproductive development time, and the probing behavior of M. persicae and M. euphorbiae on S. stoloniferum and Solanum tuberosum L. Furthermore, we analyze the changes in gene expression in S. stoloniferum 96 hours post infestation by either aphid species. Although the M. euphorbiae probing behavior shows that aphids encounter more probing constrains on phloem activities–longer probing and salivation time– on S. stoloniferum than on S. tuberosum, the aphids succeeded in reaching a sustained ingestion of phloem sap on both plants. Probing by M. persicae on S. stoloniferum plants resulted in limited feeding only. Survival of M. euphorbiae and M. persicae was affected on young leaves, but not on senescent leaves of S. stoloniferum. Infestation by M. euphorbiae changed the expression of more genes than M. persicae did. At the systemic level both aphids elicited a weak response. Infestation of S. stoloniferum plants with a large number of M. persicae induced morphological changes in the leaves, leading to the development of pustules that were caused by disrupted vascular parenchyma and surrounding tissue. In contrast, an infestation by M. euphorbiae had no morphological effects. Both plant species can be regarded as good host for M. euphorbiae, whereas only S. tuberosum is a good host for M. persicae and S. stoloniferum is not. Infestation of S. stoloniferum by M. persicae or M. euphorbiae changed the expression of a set of plant genes specific for each of the aphids as well as a set of common genes.