The effect of resistance to Amphorophora rubi in raspberry (Rubus idaeus) on the spread of aphid-borne viruses

The effectiveness of resistance to the aphid Amphorophora rubi in restricting the spread of aphid-borne viruses was assessed in a field experiment using six genotypes of red raspberry. In one block of the experiment, the genotypes alternated with rows of virus-infected Mailing Jewel raspberry, and in the other they alternated with virus-free Mailing Jewel. During 4 years, the numbers of A. rubi and the amount of 52V virus spread in the two blocks were similar, suggesting that this virus was mostly introduced from outside the plots. Lloyd George and Mailing Jewel raspberry became heavily infested with A. rubi and were rapidly infected with raspberry leaf mottle, raspberry leaf spot and 52V viruses. Glen Clova and Norfolk Giant raspberry, which contain minor genes for resistance to A. rubi, were infested with fewer A. rubi and virus spread more slowly in these cultivars. A. rubi were rare on Mailing Orion and an East Mailing raspberry selection (888/49) which have genes A₁ and A₁₀ respectively for resistance to A.rubi, and these plants remained largely free of virus. The role of minor and major gene resistance to A. rubi in restricting virus spread is discussed. A few Macrosiphum euphorbiae and Myzus ornatus were recorded on several of the raspberry genotypes.     

Effectiveness of resistance genes to the large raspberry aphid, Amphorophora idaei Börner, in different raspberry (Rubus idaeus L.) genotypes and under different environmental conditions

The introduction into commerce of raspberry cultivars with major gene resistance to the large raspberry aphid, Amphorophora idaei, an important pest and virus vector on red raspberry in Europe, has been very effective both in decreasing pest numbers and greatly restricting infection with the viruses it transmits. However, biotypes of the aphid able to overcome these genes have developed in the field in recent years. Additionally, in field and laboratory tests, the response to aphid biotypes and recognised aphid strains of certain raspberry cultivars, such as Glen Prosen and Delight, differ markedly despite the fact that they are reputed to contain the same A. idaei‐resistance gene, A₁. In attempts to understand the reasons for this difference in response, analysis was made of the segregation of progeny seedlings from crosses between A. idaei‐resistant and ‐susceptible cultivars to two recognised strains of the aphid. These studies showed that, as expected, cv. Autumn Bliss contained the A. idaei‐resistance gene, A₁₀, and cvs Delight and Glen Prosen each contained the A. idaei‐resistance gene, A₁. When progeny seedlings were assayed in a heated glasshouse as young plants and in an unheated Tygan house as 1 m tall plants, the segregation ratios for resistance and susceptibility to A. idaei were largely unchanged. However, when the resistance of individual progeny plants was assessed, c. 37% of the putative gene A₁‐containing progeny and 9–23% of the putative gene A₁₀‐containing progeny, behaved differently in these two environments. Experiments involving an A. idaei‐resistant and ‐susceptible parent cultivar showed that shading plants increased their susceptibility to A. idaei colonisation. Whilst this shading effect has implications for experimentally detecting A. idaei‐resistant progeny in segregating raspberry seedlings, it does not explain the difference in field resistance to A. idaei of cvs Delight and Glen Prosen. Such differences in the field seem best explained by the presence in these cultivars of ‘minor’ genes for A. idaei resistance and/or susceptibility that influences the effectiveness of gene A₁.     

Evidence that elevated CO2 reduces resistance to the European large raspberry aphid in some raspberry cultivars

Global climate change, such as elevated atmospheric carbon dioxide (eCO₂), may accelerate the breakdown of crop resistance to insect pests by compromising expression of resistance genes. This study investigated how eCO₂ (700 μmol/mol) affected the susceptibility of red raspberry (Rubus idaeus) to the European large raspberry aphid (Amphorophora idaei) Börner (Homoptera: Aphididae), using a susceptible cultivar (Malling Jewel) and cultivars containing either the A₁ (Glen Lyon) or A₁₀ (Glen Rosa) resistance genes. Compared to plants grown at ambient CO₂ (aCO₂) (375 μmol/mol), growth rates were significantly increased (ranging from 42–300%) in all cultivars at eCO₂. There was some evidence that plants containing the A₁ gene were more susceptible to aphids at eCO₂, with aphid populations doubling in size compared to the same plants grown at aCO₂. Moreover, aphids grew 38% larger (1.36 mg compared with 0.98 mg) on plants with the A₁ resistance gene at eCO₂ compared with those at aCO₂. Aphid performance on plants containing the A₁ gene grown at eCO₂ was therefore similar to that of aphids reared on entirely susceptible plants under either CO₂ treatment. In contrast, aphids did not respond to eCO₂ when reared on plants with the A₁₀ resistance gene, suggesting that plants with this resistance gene remained resistant to aphids at eCO₂.     

Further evidence that resistance in raspberry to the virus vector aphid, Amphorophora idaei, is related to the chemical composition of the leaf surface

In an approach to understand the mechanism(s) of resistance in raspberry to infestation by the aphid Amphorophora idaei, progeny plants segregating for the A. idaei resistance gene, A₁₀, were bioassayed and dichloromethane extracts from the leaf surface were examined by capillary column gas chromatography (GC). No single GC peak was detected that was present in only the resistant progeny plants. Nevertheless, thirteen compounds present in all samples were quantified and identified by mass spectrometry. They were of four major classes; straight chain hydrocarbons, acetic acid esters of long chain alcohols, tocopherols and triterpenoid compounds, including α and β amyrin. Several of these compounds were not recorded previously in raspberry leaves. Linear discriminant analysis, applied to the standardised chromatographic data in an attempt to relate chemical composition to resistance, successfully partitioned 24 of the 26 plants into resistant and susceptible types as determined by bioassay. These data provide further evidence that resistance in raspberry to A. idaei is related to the chemical composition of the leaf surface.     

Mapping of A1 conferring resistance to the aphid Amphorophora idaei and dw (dwarfing habit) in red raspberry (Rubus idaeus L.) using AFLP and microsatellite markers

Background  

Raspberry breeding programmes worldwide aim to produce improved cultivars to satisfy market demands and within these programmes there are many targets, including increased fruit quality, yield and season, and improved pest and disease resistance and plant habit. The large raspberry aphid, Amphorophora idaei, transmits four viruses and vector resistance is an objective in raspberry breeding. The development of molecular tools that discriminate between aphid resistance genes from different sources will allow the pyramiding of such genes and the development of raspberry varieties with superior pest resistance. We have raised a red raspberry (Rubus idaeus) F₁ progeny from the cross 'Malling Jewel' × 'Malling Orion' (MJ × MO), which segregates for resistance to biotype 1 of the aphid Amphorophora idaei and for a second phenotypic trait, dwarf habit. These traits are controlled by single genes, denoted (A ₁) and (dw) respectively.     

Epicuticular wax composition in relation to aphid infestation and resistance in red raspberry (Rubus idaeus L.)

Epicuticular waxes from the aphid-resistant red raspberry (Rubus idaeus) cultivar Autumn Bliss and the aphid-susceptible cultivar Malling Jewel were collected from the newly emerging crown leaves, and also from the group of four more mature leaves immediately below the crown. Resistance and susceptibility status of the leaves to infestation by the large raspberry aphid, Amphorophora idaei, were determined by bioassay with the insect just prior to collection of the wax. Analysis showed the waxes to consist of a complex mixture of free fatty acids; free primary alcohols and their acetates; secondary alcohols; ketones; terpenoids including squalene, phytosterols, tocopherol and amyrins; alkanes and long chain alkyl and terpenyl esters. Compositional differences which may relate to A. idaei-resistance status were noticeably higher levels of sterols, particularly cycloartenol, together with the presence of branched alkanes, and an absence of C₂₉ ketones and the symmetrical C₂₉ secondary alcohol in wax from the resistant cultivar Bliss. There were also differences between the cultivars in the distribution of individual amyrins and tocopherols and in the chain length distribution for homologues of fatty acids, primary alcohols and alkanes, and these may also be related to resistance to A. idaei. Emerging leaves had lower levels of primary alcohols and terpenes, but higher levels of long-chain alkyl esters, and in general, more compounds of shorter chain-length than the more mature leaves. During bioassay A. idaei displayed a preference to settle on the more mature leaves. This may be due to greater wax coverage and higher levels of the compounds of shorter chain length found in the newly emerged younger leaves at the crown of the plant.     

Common resistance in red raspberry to Botrytis cinerea and Didymella applanata, two pathogens occupying the same ecological niche

Comparisons were made between Botrytis cinerea and Didymella applanata, which occupy the same ecological niche on canes of red raspberry. Isolates of B. cinerea from diverse localities within the British Isles were pathogenic to the SCRI selection M30 when internodal wounds on young canes were inoculated. A single inoculation frequently caused the buds at several nodes to fail the following spring. Differences in the lengths of the stem lesions that formed indicated differences in isolate pathogenicity, but these were not related to isolate origin. Bud suppression and lateral shoot failure also occurred when petioles of cvs Mailing Orion, Mailing Jewel and Glen Clova were wound inoculated with B. cinerea up to late August. The relative resistance of seven cultivars to three isolates of each pathogen was determined. Principal components analysis of data from five estimates of resistance to each pathogen showed that 40% of the variation described a common resistance to the two diseases. Further analysis showed that cvs Chilcotin and Meeker had the strongest common resistance and that cvs Glen Prosen and Mailing Jewel had the weakest. The remaining variation described cultivar differences in relative bud length after petiole inoculation with either pathogen, and differences in the relative importance of spring and autumn symptoms. Only 7% of the variation indicated independent resistance to the two pathogens and this was not influenced by cultivar differences.     

Inheritance of resistance to yellow rust (Phragmidium rubi-idaei) in red raspberry

The inheritance of resistance in red raspberry (Rubus idaeus) to yellow rust (Phragmidium rubi-idaei) was studied in a diallel cross among the cultivars Boyne, Meeker, Mailing Jewel, Glen Prosen and Glen Clova. The progenies and clonally propagated parents were exposed initially in a rust-infected plantation where the incidence and severity of infection was assessed at the telial stage. The following spring leaves on new canes of the same plants were inoculated with urediniospores in a glasshouse at 18 ± 2 °C. The latent period and number of uredinia per cm² of abaxial leaf surface were determined 13 and 18 days after inoculation. Cv. Boyne developed only chlorotic flecking on inoculated leaves in the glasshouse and no sporulation was observed. It is postulated that this reaction was determined by a major gene which is designated Yr. Some of the other parents showed incomplete resistance of the slow rusting type, and segregants of Boyne selfed that were susceptible also showed low levels of rust, which suggests that Boyne carries both major- and minor-gene resistance. Diallel analyses of both the field and glasshouse data from the susceptible segregates indicated that the degree of incomplete resistance present was determined predominantly by additive gene action, though small but significant non-additive effects also occurred: cv. Meeker was the most resistant parent and contributed the most resistance to the progenies. The Meeker progenies also segregated for gene H, which determines cane hairiness and is known to be associated with resistance to other diseases. Segregants without hairs (genotypes hh) were found to be the more resistant to rust.     

Inherited resistance of sugar beet to aphid colonization

Results of glasshouse experiments have confirmed that inbred lines of sugar beet differ in each of three types of resistance to Myzus persicae Sulz. and Aphis fabae Scop., namely: resistance to settling, resistance to multiplication, and tolerance. Resistance to multiplication was not invariably associated with resistance to settling, although plants of some lines showed both forms of resistance. Plants that were resistant to settling of alatae were not always resistant to apterae of the same species, and there was not a close relationship between resistance to M. persicae and to A. fabae. The mechanisms involved in resistance to aphids in sugar beet are not understood. Progenies of plants, selected for resistance to aphids from inbred lines, were often more resistant than progenies of unselected plants. Inheritance of each type of resistance is probably polygenic. The potential value of the different kinds of resistance, in reducing direct feeding damage and controlling the spread of virus yellows in the field, is discussed. The ultimate breeding objective is to produce commercial varieties in which appropriate kinds of resistance to aphids are combined with resistance to virus yellows. The use of such varieties would reduce the need to control aphids in the field by applications of chemicals.     

Differential colonization of wheat cultivars by two biotypes of Russian wheat aphid （Homoptera： Aphididae）

Susceptible and resistance wheat cultivars, Triticum aestivum L, were presented to two biotypes of Russian wheat aphid, Diuraphis noxia （Mordvilko）, in multiple choice tests to assay their relative acceptability as host plants. Both apterae （third and fourth instars） and alate adults were offered plants at the two-leaf stage in different cultivar combinations at 22±1℃ and 16：8 （L： D） hour photoperiod. Apterae were released from Petri dishes in the center of a circle of test plants, whereas alatae dispersed from a mature aphid colony to settle on plants arranged in rows. Both alatae and apterous nymphs of both biotypes readily colonized all cultivars tested：‘2137＇, ‘Akron＇,‘Ankor’,‘ Halt’ ,‘ Jagger’ ,‘ Prairie Red’ , ‘Stanton＇,‘TAM 107＇,‘TAM 110＇,‘Trego＇, ‘ Yuma＇, and ‘Yumar＇. Fewer biotype I apterae responded （settled and fed） in the combination containing more resistant （Dn4- and Dny-expressing） cultivars, compared to the combinations that had fewer. The reverse was true for biotype 2 apterae; more aphids responded in the combination containing the largest number of Dn4 expressing cultivars. Differential colonization of cultivars was observed in only one combination, in which biotype 2 apterae colonized Akron and Yumar in larger numbers than they did Stanton and Yuma. A separate experiment confirmed that, 48 hours after infestation, more biotype 2 apterae abandoned plants of Yuma than plants of Yumar. This differential response was likely due to genetic differences between the two ＇ near isogenic＇ lines that include the lack of Dn4 expression in Yuma. Choice tests with alatae did not result in differential rates of cultivar colonization by either biotype in any combination tested. These results suggest that young wheat plants appear to lack any meaningful antixenosis toward D. noxia, even though the aphids appear to perceive, and sometimes respond to, certain differences in cultivar suitability.     

Effects of maternal diet on offspring fitness in the bird cherry‐oat aphid

1. Maternal and offspring diet effects on life‐history traits of the bird cherry‐oat aphid Rhopalosiphum padi were tested on three wheat varieties. Using nine reciprocal combinations of wheat varieties, the effects of previous experience (maternal diet effect) on the aphid's response to resistant and susceptible varieties (offspring diet effect) were tested. Batis was susceptible, and Xiaoyan22 and Ww2730 were both resistant, but with different mechanisms. 2. Aphids produced the most alatae in the treatments with the most resistant maternal diet variety Xiaoyan22. The fecundity (F) and intrinsic rate of increase (r_m) of these alatae were at their greatest in the most resistant offspring diet variety, but these traits were not influenced in the apterae. 3. There were significant interactions in the alatae production and apterae life‐history traits, such as r_m, development time, weight gain, and mean relative growth rate, between the maternal and offspring diet varieties. The interactions in apterae responses between varieties, some of which were reciprocal, indicated phenotypic plasticity in these parthenogenetic aphids. 4. Rhopalosiphum padi produced more alatae on the most resistant variety; the alatae would disperse and were more fecund. The growth responses of the apterae showed phenotypic plasticity to the different combinations of maternal and offspring diet varieties. The phenotypic plasticity would allow R. padi to better utilise the variable environments represented by the small wheat plots of different varieties in China.     

Study on inheritance of resistance to root aphid, Pemphigus bursarius, in lettuce

The inheritance of resistance to lettuce root aphid, Pemphigus bursarius, was studied in lettuce using the Wellesbourne cultivars Avondefiance and Avoncrisp as resistant parents and Borough Wonder and Webb's Wonderful as aphid-susceptible parents. All four cultivars were crossed in all possible combinations including reciprocals and the response to root aphid of plants in the P₁F₁F₂ and BC generations was assessed using apterae of P. bursarius from the lettuce cv. Iceberg. Resistance to attack was clearly inherited and the parents appeared to be homozygous for their resistance or susceptibility. In the F₁ generation, however, in all crosses between resistant and susceptible parents, segregation into susceptible, resistant and some slightly less resistant plants occurred. This and the highly significant differences in segregation between pairs of reciprocal crosses in the F₁ and other generations indicate that the inheritance of resistance to root aphid is controlled by extra-nuclear factors. Modifying genes might also be involved but there appears to be no linkage of root aphid resistance with resistance to downy mildew, for which the Wellesbourne lettuces were bred.     

Effects of Didymella applanata and Botrytis cinerea on axillary buds, lateral shoots and yield of red raspberry

The viability of axillary buds and the growth and potential yield of lateral shoots at nodes of red raspberry (Rubus idaeus) infected naturally by Didymella applanata or Botrytis cinerea were measured on excised nodes, decapitated nursery canes or on canes from fruiting plantations. In comparison with lesion-free nodes, buds at infected nodes were smaller and fewer of them were capable of growth when excised and ‘forced’, although the difference in growth between infected and uninfected nodes decreased during late winter. After February, those buds at infected nodes which were capable of forced growth did so as early and with a similar growth rate as those at lesion-free nodes. In April, 70% of buds at infected nodes were capable of growth compared with 94% of those at lesion-free nodes. When nursery canes of cv. Mailing Delight were decapitated above infected nodes the emergence of lateral shoots from the terminal infected node did not differ significantly from that at lesion-free nodes. On a range of farm sites in Scotland the emergence of shoots at infected nodes in the cropping region of canes was significantly poorer than from uninfected nodes but substantially better at infected nodes of cv. Glen Clova than at those of cvs Mailing Jewel and Mailing Orion. It is suggested that cv. Glen Clova is relatively tolerant of spur blight and cane botrytis. The length and potential yield of laterals which developed at infected nodes in the cropping region of canes in these three cultivars did not differ significantly from those at lesion-free nodes. In all tests there was no significant difference in growth at nodes infected by D. applanata and B. cinerea which may indicate a common mechanism for suppression of buds.     

Further studies on the effect of resistance to Amphorophora idaei in raspberry (Rubus idaeus) on the spread of aphid-borne viruses

The rate of spread of viruses transmitted by the aphid Amphorophora idaei into genotypes of raspberry differing in resistance to infestation by A. idaei was studied in a field experiment which exposed plants to large numbers of infective aphids. Under these conditions, genotypes that are readily colonised by A. idaei were totally infected with virus after two to three growing seasons, whereas genotypes with a high degree of resistance were substantially free of virus after four growing seasons but 56% of plants were infected after seven seasons. Genotypes with intermediate resistance were also substantially free of virus after three seasons but 76% of plants were virus infected after seven seasons. The effectiveness of resistance to A. idaei in raspberry in restricting spread of viruses transmitted by this aphid is discussed.     

Association of different kinds of bacilliform particle with vein chlorosis and mosaic diseases of raspberry (Rubus idaeus)

Thin sections of diseased raspberry (Rubus idaeus) were examined by electron microscopy. Plants of the cv. Baumforth's B and of an aphid (Amphorophora rubi)-resistant breeding selection (6820/54), both infected with raspberry vein chlorosis virus (RVCV) but not with other detectable viruses, contained large bacilliform particles c. 430 × 65 nm. Particles occurred in the cytoplasm and perinuclear space of a small proportion of xylem parenchyma cells. They had an inner core c. 25–30 nm in diameter with cross-banding of periodicity 4·5 nm, and were bounded by an outer membrane. They are probably the particles of RVCV. Plants of cv. Mailing Jewel and of a selection (M14) both showing symptoms of raspberry mosaic (veinbanding) disease contained smaller bacilliform particles c. 125 × 30 nm, which occurred singly or in clusters in the cytoplasm of a small proportion of vascular parenchyma cells. It is not known which, if any, of the viruses associated with raspberry mosaic are represented by the particles.     

Effects of spur blight (Didymella applanata) and premature defoliation on axillary buds and lateral shoots of red raspberry

Nodal lesions typical of natural infections of Didymella applanata were produced on young raspberry canes when wounded petioles were inoculated with mycelium. The buds which developed in the axils of these inoculated petioles were smaller and less likely to produce lateral shoots than those in the axils of delaminated or undamaged petioles, but only when the petioles were inoculated in the field before the end of July. This effect was more pronounced in cv. Mailing Jewel than in cv. Glen Clova which suggests that the latter is more tolerant of D. applanata. Sprays to control D. applanata in the cropping region of canes will probably be effective in Scotland only if applied before the end of July.     

Isolates of raspberry bushy dwarf virus differing in Rubus host range

Isolates of raspberry bushy dwarf virus (RBDV) occurring in the field at East Mailing Research Station (EMRS), and an isolate from raspberry seed imported from the USSR, were found to differ from the Scottish type isolate (D200) of RBDV in that they infected red raspberry cultivars that are resistant, possibly immune, to isolate D200. Of several red raspberry, blackberry and hybrid berry cultivars and EMRS raspberry selections graft-inoculated with these recently discovered RBDV isolates only two raspberry cvs (Haida and Rannaya Sladkaya) and one EMRS selection did not become infected. Differences in the conclusions reached in two previous studies on the inheritance of resistance to RBDV in raspberry can be explained by the use of virus isolates that differed in Rubus host range.     

Further studies on the occurrence and inheritance of resistance in red raspberry to a resistance-breaking strain of raspberry bushy dwarf virus

A strain of raspberry bushy dwarf virus (RBDV-RB), discovered in England in 1981, readily infects by grafting many raspberry cvs that have gene Bu, which confers strong resistance or immunity to isolates of the common strain. Haida is one of two cultivars that are highly resistant or immune from RBDV-RB, but both its parents, cvs Creston and Malling Promise, are infectible. Studies of the segregation of resistance to both RBDV-RB and a common strain of RBDV (D200) in four progenies related to cv. Haida or its two parents, showed that resistance to RBDV-RB was heritable and occurred when gene Bu was present with a second resistance component whose inheritance is probably multigenic. There was some indication that the second component might be a form of partial resistance to graft inoculation of varying expression, and that cv. Haida possesses this resistance at a high level that has not been distinguished from immunity in the graft inoculations used. Cultivars Creston and Malling Promise possibly have this resistance to a lesser degree, while resistance in cv. Heritage has been distinguished from immunity only by extensive graft tests. Some possible implications for breeding RBDV-RB resistant cultivars are discussed.     

Top‐down control by Harmonia axyridis mitigates the impact of elevated atmospheric CO2 on a plant–aphid interaction

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A comparison of fungicides for the control of raspberry spur blight

Effective control of raspberry spur blight (Didymella applanata) and increased crop yields in the following season were obtained in a plantation of cv. Mailing Jewel with a programme of four or five sprays commencing when the new canes first appeared. Treatments were applied at 14-day intervals and continued until c. 2 wk before harvest. Thiram (0.16% a.i), benomyl (0.025% a.i.), dichlofluanid (0.10% a.i.) and captan (0.10% a.i.) gave good control of the disease but as benomyl and dichlofluanid were also effective in controlling powdery mildew (Sphaero-theca macularis) and Botrytis cinerea on the berries these fungicides appear to be the most suitable.