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.     

Rates of growth and increase ofMyzus persicae on virus-infected potatoes according to type of virus-vector relationship

Growth, reproduction and survival (=performance) of the aphidMyzus persicae Sulzer was measured on virus-free and virus-infected potato plants The principle objective was to evaluate if various viral infections affected aphid performance differently, and if so, whether any order in the performance response of the aphid was discernible according to the type of virus-vector relationship. Three viruses varying in their dependency onM. persicae as a vector were used. Plants infected with potato leafroll virus (PLRV), a circulative virus highly dependent uponM. persicae for dispersal and transmission, were superior hosts as determined by the significantly greater mean relative growth rate (MRGR) and intrinsic rate of increase (r_m) ofM. persicae compared with those of aphids reared on other plants. Plants infected with potato virus Y, a noncirculative virus less dependent uponM. persicae for dispersal than PLRV, were intermediate in their quality based upon intermediate MRGR and r_m values. Plants infected with potato virus X, a nonvectored virus independent ofM. persicae, were least suitable hosts along with the group of virus-free plants according to the lower MRGR and r_m values.     

Factors affecting aphid acquisition and transmission of soybean mosaic virus

Myzus persicae transmitted soybean mosaic virus (SMV) most efficiently following 30 or 60 s acquisition probes on infected plants. There were no differences in susceptibility to SMV infection of soybean plants 1 to 12 wk old, but symptoms were more severe in plants inoculated when young than when old. Soybeans inoculated between developmental stages R3 and R6 only showed yellowish-brown blotching on one or more leaves. There were no observable differences in the time of appearance or type of symptoms shown by soybean seedlings inoculated either by sap or by aphids; infected plants became acquisition hosts for aphids 5–6 days after inoculation. There was no change in the efficiency with which M. persicae transmitted SMV from source plants up to 18 wk after inoculation. M. persicae transmitted SMV from leaves of field-grown soybeans when plants were inoculated at developmental stages V6, R2, and R3 and tested as sources 57–74 days after inoculation but not from plants inoculated at R5 and tested as sources 14 to 32 days after inoculation. M. persicae acquired SMV from soybean buds, flowers, green bean pods, and unifoliolate, trifoliolate, and senescent leaves. Middle-aged and deformed leaves were better sources of the virus than buds, unfolding and old symptomless leaves. The results are being incorporated into a computer model of SMV epidemiology.     

Failure of British isolates of beet western yellows virus to infect potato

Potato cultivars were tested for susceptibility to two British isolates of beet western yellows virus originally obtained from sugar beet and oil seed rape. Neither isolate was transmitted by Myzus persicae to virus-free potato plants, either by itself or in association with potato leafroll virus.     

Effects of sucrose sprays and darkness on aphid colonization of sugar beet and on aphid transmission of yellowing viruses

In the glasshouse, adult, apterous Myzus persicae (Sulz.) and Aphis fabae Scop, settled better and deposited more larvae on sucrose-sprayed sugar-beet plants than on water-sprayed plants. M. persicae settled badly and deposited few larvae on plants that were kept in the dark before or after infestation. The effects of darkness on aphids were reduced by spraying the host plants with 10% solutions of sucrose before infestation. Viruliferous M. persicae transmitted beet yellows virus (BYV) and beet mild yellowing virus (BMYV) less efficiently to dark-treated plants than to those grown in normal daylight. Spraying sugar beet with sucrose before inoculation with viruliferous M. persicae increased the proportion of successful BYV transmissions but only when the plants were dark-treated. The effects of sucrose and darkness on settling and larviposition of aphids and on virus transmission may be related to changes in the concentration of carbohydrates, particularly sugars, in the leaves.     

Comparative Studies on Aphid Transmission of the Sudanese Strain of Peanut Stunt Virus

The Sudanese strain of peanut stunt virus was transmitted by Aphis craccivora, Aphis solanella, Myzus persicae and Liaphis erysimi. Of these, A. solanella and L. erysimi were reported for the first time as vectors of peanut stunt virus. A. gossypii, A. solani and Rhopalosiphum maidis failed to transmit the virus. Viruliferous aphids retained the virus for 30 minutes but post-acquisition starvation beyond 30 minutes resulted in almost complete loss of the virus. A. craccivora transmitted the virus to four consecutive test plants and A. solanella, L. erysimi and M. persicae transmitted the virus to three consecutive test plants. It has been suggested that future research programmes should, include resistance to the virus in the major legume crops and that a crop like lucerne (Medicago sativa) which harbours both the virus and its vectors, should not be introduced in the major peanut-growing areas of the Sudan.     

Soybean Mosaic Virus: Vector Specificity and Coat Protein Properties

Aphid transmission studies of two soybean mosaic virus isolates have shown that both isolates are transmitted by Myzus persicae. Only one of the isolates is transmitted by Rhopalosiphum maidis. The R. madis non-transmissible isolate could be transmitted from plants co-infected with the R. maidis transmissible isolate; aphid acquisition factor did not seem to mediate this transmission. The two isolates could be differentiated by enzyme-linked immunosorbent assay experiments, but peptide mapping experiments revealed few differences between the isolates.     

The role of flying aphid vectors in the transmission of cucumber mosaic virus and potato virus Y to peppers in Israel

More than 44 species of aphids were trapped by suction during the spring seasons of 1981, 1982 and 1983 over a pepper field at Bet Dagan, Israel. Nineteen species transmitted cucumber mosaic virus (CMV), while seven transmitted potato virus Y (PVY) at least once. Over 80% of the CMV and of the PVY infection among test plants (Capsicum annuum cv. Weindale) exposed to trapped aphids was caused by Aphis citricola and two or three other Aphis species, Myzus persicae and Macrosiphum euphorbiae. Landing rate was determined by comparing the proportion of each species found on green tiles or pepper plants with that found in suction traps. A. citricola was the most common but was found in a much lower proportion on plants than either in flight or on green tiles. Aphis spp. and M. persicae were more than 2–5 times more frequent (relative to other species) on green tiles than in flight. M. persicae and M. euphorbiae, which colonise peppers, were found on peppers at a proportion several times higher than either on green tiles or in the air. The relative importance of the different vector species was calculated by multiplying abundance by the proportion of transmitters and the landing rate. A. citricola and Aphis spp. were responsible for more than 50% of the total transmission of either CMV in 1981 and 1982 and of PVY in 1981. Peaks of CMV infection of bait plants coincided with peaks of transmitters of A. citricola and Aphis spp. caught in suction traps. The significance of these findings in primary infection of peppers with CMV and PVY is discussed.     

Aphid-transmitted viruses from lilies in Britain

Three aphid-transmitted viruses, tulip breaking, lily symptomless and cucumber mosaic, were obtained from lilies in Britain. Tulip breaking virus was detected by the leaf mottle produced in Lilium formosanum, cucumber mosaic virus by inoculation of sap to Nicotiana clevelandii and Chenopodium quinoa, and lily symptomless virus by electron microscopy of crude leaf extracts from symptomless L. formosanum. Liiy symptomless virus was transmitted by Myzus persicae, Macrosiphum euphorbiae, Aulacorthum solani and Aphis fabae. M. persicae, which in a small experiment appeared a more efficient vector than A. fabae, transmitted the virus in a non-persistent manner. This conflicts with the original report of transmission in a persistent manner by A. gossypii but no transmission by M. persicae. The possibility that there are two distinct viruses with similar pathological effects is discussed. Tulip breaking and lily symptomless viruses spread to bait plants of L. formosanum within a field planting of lilies in Scotland especially during July to September; lily symptomless virus was the more prevalent. No spread of cucumber mosaic virus was detected.     

Effect of Fungicides on the Viability of Phylophthora cactorum Propagules m the Soil

Vein-clearing followed by downward rolling and necrosis of leaves and severe stunting of groundnut (Arachis hypogaea) plants were caused by cowpea mild mottle virus (CMMV). The virus was readily transmitted by mechanical sap inoculations to groundnut and to 10 plant species belonging to Leguminosae, Chenopodiaceae and Solanaceae. Chenopodium quinoa and Beta vulgaris were good diagnostic hosts. Diseased sap remained infective at 10^–3 but not 10^–4, when stored 8 to 9 days at 25 °C; for 10min at 75 °C but not 80°C. In limited tests, virus was not seed-transmitted m groundnut or soybean. Virus was transmitted by Bemisia tabaci but not by Aphis craccivora or Myzus persicae. An antiserum for CMMV was produced and virus was serologically related to CMMV reported on cowpea and groundnut crinkle virus (GCV) from West Africa. Employing carbon diffraction grating replica as a standard the modal length of virus particles to be 610 nm. Infected cells contained large number of virus particles associated with endoplasmic reticulum.     

Effects on Myzus persicae (Sulz.) and transmission of beet yellows virus of applying certain trace elements to sugar beet

Applications of lithium chloride (LiCl), zinc sulphate (ZnSO₄) or nickel sulphate (NiSO₄) to the roots of sugar-beet plants in the glasshouse encouraged settling on the leaves of adult apterae from a clone of Myzus persicae (Sulz.); conversely, treatment with boric acid (H₂B₂O₇) inhibited aphid settling. Larviposition of M. persicae was increased by NiSO₄ and tin chloride (SnCl₂). Viruliferous M. persicae transmitted beet yellows virus (BYV) more efficiently to plants treated with LiCl or H₂B₂O₇ than to those treated with copper sulphate (CuSO₄), ZnSO₄ or SnCl₂. The sulphate and chloride anions of the applied chemicals appeared to have little effect on M. persicae and virus transmission. It is suggested that applications of trace elements to sugar beet affected M. persicae and virus transmission by changing the concentrations of trace elements in the aphids' diet and by altering the metabolism of the leaf tissues in the host plant.     

Virus-Vector Cell Interactions Regulating Transmission Specificity of Soybean Dwarf Luteoviruses

Transmission of soybean dwarf viruses (SbDV) indigenous to Japan (SbDV‐D) and to the eastern United States (SbDV‐Va19) were compared in vector and nonvector aphid species. Absolute vector‐specificity was maintained when Aulacorthum solani, Acyrthosiphon pisum, and Myzus persicae were allowed to feed on solutions of either virus (100 μg/ml) through Parafil© membranes. SbDVD was transmitted only by A. solani, and SbDV‐Va19 was transmitted only by A. pisum and M. persicae. Similar results were obtained when individual aphids were micro‐injected with 2 ng virus and subsequently allowed to feed on healthy plants. Ultrastructural studies of A. solani and M. persicae indicated that both SbDV‐D and SbDV‐Va20 were acquired specifically through the aphid hindgut. No difference in hindgut acquisition specificity was observed, and both A. solani and M. persicae were able to transport SbDV‐D and SbDV‐Va20 into the haemocoel by endocytotic/exocytotic pathways. When injected, SbDV was shown to be associated with only the accessory salivary glands (ASG) in aphids, indicating a high level of tissue specificity. Two different interactions with the ASG were observed for SbDV‐D and SbDV‐Va20 in A. solani and M. persicae. SbDV‐D penetrated the ASG basal lamina of A. solani, but was never observed in the basal lamina of M. persicae. The ASG basal lamina was a barrier to SbDV‐D transmission by M. persicae. SbDV‐Va19 penetrated the ASG basal lamina of both A. solani and M. persicae. However, SbDV‐Va20 was not observed in the ASG cytoplasm in A. solani, indicating that the basal plasmalemma functioned as the transmission barrier. Observations indicated that capsid protein structure, aphid basal lamina composition and cell membrane components influenced virus‐aphid interactions regulating SbDV transmission.     

Comparative transmission of bean leaf roll and pea enation mosaic viruses by aphids

Acyrthosiphon pisum was a more efficient vector than Myzus persicae of bean leaf roll virus (BLRV), but the two species transmitted pea enation mosaic virus (PEMV) equally well and much more often than Megoura viciae. M. viciae did not transmit BLRV, and Aphis fabae did not transmit BLRV or PEMV. BLRV and PEMV were transmitted more often by nymphs of A. pisum than by adult apterae or alatae that fed on infected plants only as adults, but both viruses were readily transmitted by adults that had developed on infected plants. The shortest time in which nymphs acquired BLRV was 2 h, and 50 % transmitted after an acquisition period of 4 days. Some nymphs acquired PEMV in 30 min and 50% in 8 h. The shortest time for inoculation of BLRV by adults was 15 min, but some transmitted PEMV in probes lasting less than 1 min. The median latent periods of BLRV and PEMV in aphids fed for 12 h on infected plants were, respectively, 105 and 44 h. Clones of A. pisum differed in their ability to transmit BLRV and PEMV, and efficiency in transmitting the two viruses seemed to be unrelated. Some aphids that fed successively on plants infected with each virus transmitted both viruses, and infectivity with one virus did not seem to affect transmission of the other.     

Serological Detection of Beet Western Yellows Luteovirus in the Non-vector,Brevicoryne brassicae (Homoptera: Aphididae)

The interaction between beet western yellows luteovirus (BWYV) and the aphid species Brevicoryne brassicae was investigated using virus transmission and serological detection experiments. This species failed to transmit a BWYV isolate from infected to healthy oilseed rape plants, although virus was readily detected by double-antibody sandwich enzyme-linked immunosorbent assay (DAS-ELISA) in single B. brassicae adults. When virus-carrying adults were tested by ELISA after different inoculation access periods, the number of virus-positive individuals decreased after 5 days, whereas with the efficient vector Myzus persicae, virus-positive individuals were found even after 10 days. This confirms the inability of B. brassicae to transmit BWYV, even though it may acquire the virus. It is suggested that B. brassicae, as compared with the efficient vector M. persicae, may serve as an experimental model for studying the mechanisms of the luteovirus-vector specificity     

The combined use of mineral oils and pyrethroids to control plant viruses transmitted non- and semi-persistently by Myzus persicae

A mixture of the pyrethroid WL85871 (an enriched form of cypermethrin) and the mineral oil SC811 intoxicated adult apterae of an insecticide-susceptible clone of the peach-potato aphid Myzus persicae at a similar rate to a treatment containing only WL85871, but the mixture killed more. Mixtures of WL85871 andSC811 also gave better control of both acquisition and inoculation by M. persicae of the non-persistent potato virus Y (PVY) than either component alone. A mixture of the pyrethroids deltamethrin, cypermethrin and PP321 with SC811, or a mixture of WL85871 with the mineral oil Bayol 52 also decreased acquisition of PVY, and a mixture of WL85871 with SC811 decreased acquisition of another non-persistently transmitted virus, beet mosaic virus. Control with mixtures was generally better than that provided by each component applied separately. When testing acquisition or inoculation of the semi-persistent beet yellows virus, fewest plants were infected in treatments incorporating both WL85871 and SC811.     

Stabilization, culture and some properties of tulip halo necrosis virus

Tulip halo necrosis virus, obtained from tulips with leaf necrosis, is very labile in crude sap but can be transmitted consistently by inoculating Nicotiana clevelandii plants with extracts made in pH 8 phosphate buffer containing a stabilizing agent such as 0.2M 2-mercaptoethanol or 0.01M dithiothreitol. Of the fifteen species in five families of Angiosperms infected by inoculation with sap, few are suitable as sources of inoculum. Cultures of the virus can be maintained in Nicotiana clevelandii kept at 14 or 18d?C but not at 21d?C. Infectivity can be assayed in Chenopodium quinoa, in which necrotic local lesions are produced. Stabilized extracts of leaves were infective at a dilution of 1/16 but rarely at 1/32, and infectivity decreased disproportionately with dilution. Infectivity of all extracts was abolished in 10 min at 50d?C and of some at 45d?C, but survived when extracts were clarified using diethyl ether or trichlorotrifluoroethane. The virus was not transmitted by the aphid Myzus persicae.     

The occurrence of beet mild yellowing virus in Czechoslovakia

The occurrence of beet mild yellowing virus (BMYV) on feeding- and sugar-beet in Czechoslovakia has been proved. The virus was transmitted by aphidMyzus persicae (Sulz.) on indicator plantsSinapis alba L.,Capsella bursa-pastoris Medik, andClaytonia perfoliata Donn and from these plants back to sugar-beet cv. ‘Dobrovická A.’ A weed plantRaphanus raphanistrum L. was identified as a new natural host plant of BMYV. The virus was identified in ten of twelve biologically examined samples of beet with BMYV-like symptoms, which were collected at various places in Czechoslovakia     

Quantitative studies on the uptake and retention of potato leafroll virus by aphids in laboratory and field conditions

Enzyme-linked immunosorbent assay (ELISA) was adapted for the efficient detection and assay of potato leafroll virus (PLRV) in aphids. Best results were obtained when aphids were extracted in 0.05 M phosphate buffer, pH 7.0, and the extracts incubated at 37 °C for 1 h before starting the assay. Using batches of 20 green peach aphids (Myzus persicae), about 0.01 ng PLRV/aphid could be detected. The virus could also be detected in single aphids allowed a 1-day acquisition access period on infected potato leaves. The PLRV content of aphids depended on the age of potato source-plants and the position of source leaves on them. It increased with increase in acquisition access period up to 7 days but differed considerably between individual aphids. A maximum of 7 ng PLRV/aphid was recorded but aphids more usually accumulated about 0.2 ng PLRV per day. When aphids were allowed acquisition access periods of 1–3 days, and then caged singly on Physalis floridana seedlings for 3 days, the PLRV content of each aphid, measured subsequently, was not strongly correlated with the infection of P. floridana. The concentration of PLRV in leaf extracts differed only slightly when potato plants were kept at 15, 20, 25 or 30 °C for 1 or 2 wk, but the virus content of aphids kept on leaves at the different temperatures decreased with increase of temperature. PLRV was transmitted readily to P. floridana at all temperatures, but by a slightly smaller proportion of aphids, and after a longer latent period, at 15 °C than at 30 °C. The PLRV content of M. persicae fed on infected potato leaves decreased with increasing time after transfer to turnip (immune to PLRV). The decrease occurred in two phases, the first rapid and the second very slow. In the first phase the decrease was faster, briefer and greater at 25 and 30 °C than at 15 and 20 °C. No evidence was obtained that PLRV multiplies in M. persicae. These results are compatible with a model in which much of the PLRV in aphids during the second phase is in the haemocoele, and transmission is mainly limited by the rate of passage of virus particles from haemolymph to saliva. The potato aphid, Macrosiphum euphorbiae, transmitted PLRV much less efficiently than M. persicae. Its inefficiency as a vector could not be ascribed to failure to acquire or retain PLRV, or to the degradation of virus particles in the aphid. Probably only few PLRV particles pass from the haemolymph to saliva in this species. The virus content of M. euphorbiae collected from PLRV-infected potato plants in the field increased from early June to early July, and then decreased. PLRV was detected both in spring migrants collected from the plants and in summer migrants caught in yellow water-traps. PLRV was also detected in M. persicae collected from infected plants in July and August, and in trapped summer migrants, but their PLRV content was less than that of M. euphorbiae, and in some instances was too small for unequivocal detection.     

Can plants use an entomopathogenic virus as a defense against herbivores?

It is by now well established that plants use various strategies to defend themselves against herbivores. Besides conventional weapons such as spines and stinging hairs and sophisticated chemical defenses, plants can also involve the enemies of the herbivores in their defense. It has been suggested that plants could even use entomopathogens as part of their defense strategies. In this paper, we show that Brassica oleraceae plants that are attacked by Myzus persicae aphids infected with an entomopathogenic parvovirus (M. persicae densovirus) transport the virus through the phloem locally and systematically. Moreover, healthy aphids that fed on the same leaf, but separated from infected aphids were infected via the plant. Hence, this is proof of the principle that plants can be vectors of an insect virus and can possibly use this virus as a defense against herbivores.     

Éléments pour la prise en considération des Aphides dans la lutte intégrée en vergers de pêchers

Résumé Les auteurs présentent une analyse de la dynamique des populations de pucerons réalisée dans un verger expérimental de Pêchers dont les conditions de milieu sont précisées (climat, sol, pratiques culturales). La méthode d'estimation des effectifs a permis de suivre l'évolution des populations deMyzus persicae et des autres Aphides en rapport avec l'aetivité de leurs principaux ennemis naturels. Les conditions dans lesquelles se développe le phénomène de résistance deMyzus persicae aux esters phosphoriques ont été abordées. Des seuils de tolérance provisoires sont proposés pour les deux espèces les plus dangereuses:Myzus persicae etHyalopterus pruni.

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Summary The sampling method adopted for the survey of populations of the Peach tree Aphids, consists in estimating, for each Aphid species, the total number of aphids per tree and in classifying the degree of infestation according to the power of five (degree 0=no aphids; degree 1∶1 to 5 aphids; degree 2∶6 to 25 aphids etc.). Each sample has been taken from 50 trees. By this method it was possible to estimate the highest degrees of infestation tolerated by the trees without apparent damage. The following economic thresholds are provisionally considered: degree 5 in May forMyzus persicae, degree 4 at the beginning of June forHyalopterus pruni. Experiments on artificial contamination of peach trees byMyzus persicae indicate that resistance of this species to organophosphates appears and is maintained on peach trees without any immigration of winged individuals of anholocyclic clones from secondary host plants. The biology and trends in populations on Peach trees of the following species:Hyalopterus pruni Geoff.,Brachycandus prunicola Kltb.,B. amygdalinus Schout.,B. persicae Pass.,Myzus varians Davids are discussed. The current research on Aphids is reconsidered within the larger framework of integrated control in Peach orchards.