Resistance to Lettuce Aphid (Nasonovia ribisnigri) Biotype 0 in Wild Lettuce Accessions PI 491093 and PI 274378

in HortScience

The lettuce aphid, Nasonovia ribisnigri Mosley (Hemiptera: Aphididae), is a major insect pest of lettuce, Lactuca sativa L, in many commercial lettuce production areas around the world. Resistance to lettuce aphid biotype 0 (Nr:0) was first reported in Lactuca virosa L. accession IVT 280 and characterized as complete, i.e., virtually no aphids survived, and genetically dominant to partial resistance in L. virosa accession IVT 273. Complete and partial resistances to Nr:0 were conditioned by two alleles, Nr (complete resistance) and nr (partial resistance), but the genetic relationship to susceptibility was not reported. We previously reported two new potential sources of unique genes for resistance to Nr:0 in Lactuca serriola L. accession PI 491093 and L. virosa PI 274378. We report on the genetic and phenotypic nature of resistance to Nr:0 in these two wild lettuce accessions. Resistance to Nr:0 in PI 274378 is complete and allelic to complete resistance in IVT 280. Resistance to Nr:0 in PI 491093 was partial, recessive to complete resistance in ‘Barcelona’ that was derived from IVT 280, but dominant to susceptibility in ‘Salinas’. We propose the revised gene symbols for resistance to Nr:0: Nr:0C for complete resistance and Nr:0P for partial resistance, which was originally designated as nr but may now be regarded as the symbol for susceptibility to all strains of lettuce aphid. The dominance relationships among these three alleles are Nr:0C (in IVT 280, ‘Barcelona’) > Nr:0P (in PI 491093) > nr (in susceptible genotypes). Expression of partial resistance in PI 491093 was variable in controlled infestation tests, but in a naturally infested field test provided a potentially useful level of resistance to Nr:0. Partial resistance, where complete resistance has not been widely deployed, may either alone or as a component of integrated pest management delay or prevent emergence of genotypes that overcome complete resistance controlled by Nr:0C.

Abstract

The lettuce aphid, Nasonovia ribisnigri Mosley (Hemiptera: Aphididae), is a major insect pest of lettuce, Lactuca sativa L, in many commercial lettuce production areas around the world. Resistance to lettuce aphid biotype 0 (Nr:0) was first reported in Lactuca virosa L. accession IVT 280 and characterized as complete, i.e., virtually no aphids survived, and genetically dominant to partial resistance in L. virosa accession IVT 273. Complete and partial resistances to Nr:0 were conditioned by two alleles, Nr (complete resistance) and nr (partial resistance), but the genetic relationship to susceptibility was not reported. We previously reported two new potential sources of unique genes for resistance to Nr:0 in Lactuca serriola L. accession PI 491093 and L. virosa PI 274378. We report on the genetic and phenotypic nature of resistance to Nr:0 in these two wild lettuce accessions. Resistance to Nr:0 in PI 274378 is complete and allelic to complete resistance in IVT 280. Resistance to Nr:0 in PI 491093 was partial, recessive to complete resistance in ‘Barcelona’ that was derived from IVT 280, but dominant to susceptibility in ‘Salinas’. We propose the revised gene symbols for resistance to Nr:0: Nr:0C for complete resistance and Nr:0P for partial resistance, which was originally designated as nr but may now be regarded as the symbol for susceptibility to all strains of lettuce aphid. The dominance relationships among these three alleles are Nr:0C (in IVT 280, ‘Barcelona’) > Nr:0P (in PI 491093) > nr (in susceptible genotypes). Expression of partial resistance in PI 491093 was variable in controlled infestation tests, but in a naturally infested field test provided a potentially useful level of resistance to Nr:0. Partial resistance, where complete resistance has not been widely deployed, may either alone or as a component of integrated pest management delay or prevent emergence of genotypes that overcome complete resistance controlled by Nr:0C.

Lettuce (Lactuca sativa L.) is a major leafy vegetable that is grown and harvested year-round in the United States (Davis et al., 1997). California and Arizona produce 68% and 22%, respectively, of the lettuce grown in the United States (Mou, 2009) with the balance produced in 17+ other states (USDA, 2011a). Head and leaf lettuce crops were harvested from 56,660 ha in Monterey County, CA, and valued at $1.24 billion in 2010 (Lauritzen, 2011). Fresh lettuce leaves are commonly consumed in salads or sandwiches in the United States, Europe, and Australia, but in some countries, elongated stems are eaten; raw in Egypt; and cooked in China (Ryder, 2002).

Lettuce aphid, Nasonovia ribisnigri Mosley (Hemiptera: Aphididae), is an economically important pest of lettuce in Europe (Arend et al., 1999), Canada (Forbes and MacKenzie, 1982), the United States (Chaney, 1999; Palumbo, 2000), New Zealand (Stufkens and Teulon, 2003), Tasmania (Stufkens et al., 2002, 2004), and Australia (Anonymous, 2004). Lettuce aphid may colonize lettuce at any time from the seedling stage of growth onward. High densities of lettuce aphid can deform lettuce heads and change leaf color. Lettuce aphid is also listed as a vector of Cucumber mosaic virus and Lettuce mosaic virus (Blua, 1997), although no incidents of virus transmission have been reported from any lettuce production areas. Lettuce aphid not only reduces marketability of infested lettuce in domestic markets but poses as a phytosanitary barrier for lettuce exports to some overseas markets such as Japan and Taiwan where lettuce aphid is quarantined.

Lettuce aphid is difficult to manage. Its propensity for colonizing the young (core) leaves makes it virtually impossible to control with contact insecticides during head maturation (Liu, 2004). In addition, it can develop resistance to insecticides (Barber et al., 1999; Stufkens and Wallace, 2004). Postharvest control of lettuce aphid on exported lettuce is also challenging. Methyl bromide fumigation causes injuries to lettuce and there are no safe alternative fumigants. Although ultralow oxygen treatment was reported to be safe and effective to control lettuce aphid on harvested head lettuce, the treatment was not effective against leafminer, Liriomyza langei Frick, which is also quarantined in Japan and often intercepted on exported lettuce (Liu, 2005). Genetically based host plant resistance is an economical and environmentally desirable means to control lettuce aphid infestation of lettuce (Painter, 1980).

Two biotypes of lettuce aphid have been known in Europe since 2007 and were designated by The Netherlands Inspection Service for Horticulture (Naktuinbow) as Nr:0 and Nr:1 (Thabuis et al., 2011). Biotype Nr:0 is known worldwide, and biotype Nr:1 is, thus far, known only in Europe. Complete and partial types of resistance to Nr:0 were described in Lactuca virosa L., a wild, distant relative of cultivated lettuce (Eenink and Dieleman, 1983). Complete resistance to Nr:0 was the result of a single gene (Nr) that was partially dominant in segregating (F2) families from resistant L. virosa × susceptible L. virosa crosses but completely dominant after introgression to cultivated lettuce, L. sativa (Eenink and Dieleman, 1983; Eenink et al., 1982b). Partial resistance to Nr:0 in L. virosa was the result of a recessive allele, nr, at the same locus (Eenink and Dieleman, 1983). Complete resistance to Nr:0 in L. virosa accession IVT 280 was transferred to cultivated lettuce (Arend et al., 1999) and is highly effective against California strains of Nr:0 (Liu and McCreight, 2006).

Sixty-four L. serriola and L. virosa accessions in the Center for Genetic Resources, The Netherlands (CGN) collection were reported resistant to Nr:1 (Anonymous, 2008). Dominant resistance to Nr:0 and Nr:1 was claimed in L. serriola accession 10G.913571 (Thabuis et al., 2011).

The potential for the breakdown or failure of resistance conferred by the Nr gene was recognized shortly after release of Nr:0-resistant cultivars (Arend, 2003) and subsequently realized in Europe where the Nr gene was widely deployed (Thabuis et al., 2011). Although the gene has not been widely deployed in the United States as a result of different market requirements and numerous production niches (Davis et al., 1997), alternative sources of resistance to Nr:0 conditioned by other genes or mechanisms are desirable to prolong the effective life of Nr:0-resistant lettuce cultivars. Two potentially unique sources of resistance to Nr:0 were found in a survey of ≈1200 cultivated and wild lettuce accessions (McCreight, 2008). Our objectives were to characterize and determine the inheritance of resistance to Nr:0 in Lactuca serriola accession PI 491093 and L. virosa accession PI 274378.

Materials and Methods

This work was done using controlled infestations in greenhouses (13 experiments) and field cages (one experiment) and natural infestations in open fields (two experiments) in Salinas, CA. Eight of the experiments determined inheritance of resistance in PI 491093 (three) and PI 274378 (five); eight experiments evaluated the resistance phenotype of PI 491093.

Plant materials.

The nine lettuce aphid-susceptible, resistant, or partially resistant accessions and cultivars used in these experiments were from various sources (Table 1). The seeds used in this research were produced in insect-free greenhouses at Salinas, CA. ‘Salinas’ served as the susceptible control (Ryder, 1979a). IVT 280 (Eenink and Dieleman, 1983), and ‘Barcelona’, which carries the Nr gene from IVT 280, served as resistant controls. Lettuce aphid-resistant ‘Dynamite’ (Arend et al., 1999) was included in one test for comparison with ‘Barcelona’.

Table 1.

Plant materials used in experiments to determine the inheritance of lettuce aphid resistance in PI 491093 and PI 274378.

Table 1.

Crosses for genetic studies were made in a greenhouse using standard procedures for hand pollination of lettuce (Ryder, 1979b). PI 491093 was crossed with L. sativa cultivars Barcelona and Salinas. PI 274378 was crossed with four L. virosa accessions: completely resistant IVT 280, partially resistant CGN05332 (McCreight, unpublished data), susceptible PI 273597 (McCreight, unpublished data), and partially resistant PI 274375 (McCreight, unpublished data).

Lettuce aphid strain.

Lettuce aphids were collected from a lettuce field at the USDA-ARS research station, Salinas, CA, in 2001 and reared on lettuce plants, usually ‘Parris Island’ and ‘Salinas’, in large, insect-proof, screened cages in a greenhouse. The colony was periodically supplemented with field-collected lettuce aphids through the duration of the testing to ensure representation of populations in commercial fields and on one occasion was completely re-established when infested by parasitoids. Resistance in IVT 280 and ‘Barcelona’ was always expressed against the lettuce aphids used in these studies; they may thus be regarded as Nr:0 (Thabuis et al., 2011).

Greenhouse tests.

Seeds of each entry were sown in coarse, washed sand in 10 cm × 10 cm × 10-cm plastic pots and covered with Tencate Mirafi® geosynthetic fabric (<http://www.tencate.com/>) through germination in a greenhouse. Seedlings were transplanted at the one to two true leaf stage into 7.6 cm × 7.6 cm × 7.6-cm plastic pots filled with a 1 potting mix:1 sand mixture (by volume). Plants were watered daily, fertilized weekly with 119 15N–2.2P–12.5K–5Ca–2Mg (Peters Excel Cal-Mag; Scotts-Sierra Horticultural Products, Marysville, OH) at a rate of 3.6 g·L−1 to deliver 540 mg·L−1 N, and grown under the natural photoperiod at 4 to 20 °C (winter) and 10 to 40 °C (summer).

Plants were infested with 24 h or less or 24- to 48-h-old nymphs of lettuce aphid (five or 10 nymphs per plant). Infested plants were placed in insect-proof cages (≈63 cm × 63 cm × 63 cm) with one entry per cage. Total numbers of aphids (nymphs + alates) were counted periodically from as early as 2 d through 111 d post-infestation (dpi).

Caged field test.

Seedlings from seeds sown in the greenhouse as described previously were transplanted to standard lettuce beds in a field and included ‘Salinas’, ‘Barcelona’, PI 491093, and IVT 280. Plants were spaced 30 cm apart along the center of the bed and drip-irrigated as needed. Tests were arranged in randomized complete blocks with five replications. Plants were individually enclosed in aphid-proof cages (≈46 cm × 46 cm × 46 cm) at the time of transplanting. One plant of each entry in each replication was infested with five aphids at the time of transplanting and at 2 and 4 weeks post-transplanting. Numbers of aphids were counted at 7-d intervals through 28 dpi. Other aphid species present were also counted.

Open-field tests.

There were two naturally infested, open-field tests. The first test was started from seed, and entries were planted on standard lettuce beds, two entries per bed (one per seed line) and thinned to one plant per 30-cm; each experimental unit was 3.0 m long. The test included ‘Salinas’, ‘Barcelona’, PI 491093, IVT 280, seven families of F2 Salinas × PI 491093, and one family of F2 Barcelona × PI 491093. The entries were arranged in a randomized complete block design with four replications. Natural infestation of the control cultivar Salinas by lettuce aphid was monitored weekly in both tests. When lettuce aphids were numerous on ‘Salinas’, three plants were randomly selected from each plot and taken to the laboratory where only lettuce aphids were counted.

The second open-field test was transplanted as described previously for the caged field test; included ‘Salinas’, ‘Barcelona’, PI 491093, and IVT 280; and was located in a commercial lettuce production area, 8.9 km away from the caged field test. The entries were arranged in a randomized complete block design with three replications. Each replication included three plants of IVT 280 and five plants each of the other three entries. Natural infestation of the control cultivar Salinas by lettuce aphid was monitored weekly, and when aphids were numerous on ‘Salinas’ (40 dpi), the plants were taken to the laboratory where all aphids were counted. Lettuce aphid counts were totaled separately from other aphid species.

Data analysis.

Statistical analyses and means comparisons were done using JMP 8.0.1 (SAS Institute, Cary, NC). Greenhouse data were analyzed as complete random designs. Caged and open-field data were analyzed as randomized complete block designs.

Results and Discussion

Inheritance of partial resistance in PI 491093.

Mean numbers of lettuce aphids on ‘Salinas’ at 14 and 40 dpi were significantly (P = 0.05) higher than on PI 491093 and six F1 progenies from crosses of PI 491093 with ‘Salinas’ and ‘Barcelona’ (Table 2). Numbers of lettuce aphid on the three F1 Salinas × PI 491093 progenies were not significantly higher than the numbers on three F1 Barcelona × PI 491093 progenies (Table 2). These data suggest that resistance to lettuce aphid in PI 491093 is dominant to susceptibility. Although the F1 data suggest that resistance in PI 491093 is comparable to that in IVT 280, F2 data reveal the difference in their gene expression. In the greenhouse experiment on the F2 Salinas × PI 491093, mean numbers of lettuce aphids on ‘Salinas’ were many fold and significantly (P = 0.05) higher than on PI 491093 and their F2 at 15 and 36 dpi (Table 2). There was a considerable overlap in aphid distributions on the parents and their F2 at 15 dpi (Fig. 1A), but by 36 dpi, lettuce aphids on the susceptible ‘Salinas’ increased significantly and resulted in higher densities per plant than on PI 491093 and their F2 (Fig. 1B). The wide range in number of lettuce aphids per plant of PI 491093 indicates that the resistance is partial in contrast to the complete resistance in IVT 280 (Eenink and Dieleman, 1983). The F2 segregated 87 partially resistant:33 susceptible at 36 dpi when the break point for partial resistant vs. susceptible was set at 73 (= mean + se of the F2; Table 2) lettuce aphids per plant, an acceptable fit to the expected 3:1 ratio for a single dominant gene (χ2 = 0.40, P = 0.54).

Table 2.

Mean ± se numbers of lettuce aphids per plant of ‘Salinas’, ‘Barcelona’, PI 491093, IVT 280, and their F1 and F2 offspring in two greenhouse tests at different days post-infestation and on two dates in a naturally infested, open field test, Salinas, CA.

Table 2.
Fig. 1.
Fig. 1.

Frequency distributions of numbers of lettuce aphids per plant of susceptible ‘Salinas’, partially resistant PI 491093 and F2 Salinas × PI 491093 at 15 dpi (A) and 36 dpi (B); infested with five 24- to 48-h-old nymphs per plant in the greenhouse. dpi = days post-infestation.

Citation: HortScience horts 47, 2; 10.21273/HORTSCI.47.2.179

In the naturally infested field test of the F2 Salinas × 491093 and the F2 Barcelona × 491093, ‘Salinas’ had significantly (P = 0.05) higher aphid density than PI 491093, ‘Barcelona’, and IVT 280 on 8 July and 20 July (Table 2). ‘Salinas’ differed significantly from three of the seven F2 Salinas × PI 491093 progenies and the F2 Barcelona × PI 491093 (Table 2) on 8 July. Mean numbers of lettuce aphids increased on all entries except IVT 280 by 20 July, and ‘Salinas’ had significantly higher aphid density than all seven of the F2 Salinas × PI 491093 progenies. Mean number of aphids on F2 Barcelona × PI 491093 was 1.0; this was significantly lower than on the F2 Salinas × PI 491093 progenies, which ranged from 14.8 to 23.7.

Frequency distributions of lettuce aphid from the F2 field tests further revealed the difference in dominance and, possibly, the number of resistant alleles between the L. virosa-derived (IVT 280) resistance conditioned by the single dominant gene, Nr, and the resistance in PI 491093 (Fig. 2). Numbers of lettuce aphids on susceptible ‘Salinas’ ranged from zero (one plant) to 100 (Fig. 2). Distributions of IVT 280 (all zero lettuce aphids per plant) and ‘Barcelona’ (zero to two lettuce aphids per plant) were similar to each other. Numbers of lettuce aphids per plant of PI 491093 ranged from zero (16 plants) to 17 (one plant). The small sample of the F2 Barcelona × PI 491093 segregated 20 completely resistant:three partially resistant where, based on the range of ‘Barcelona’, completely resistant ranged from zero to two lettuce aphids per plant and partially resistant had three or more lettuce aphids per plant, an acceptable fit to the expected 3:1 ratio for a single dominant gene (χ2 = 1.17, P = 0.28) with Yates correction (Yates, 1931). Mean number of lettuce aphids per plant for the seven F2 Salinas × PI 491093 progenies was 19.7 ± 1.8; the combined data ranged from zero (36 plants) to 106 (one plant) lettuce aphids per plant (Fig. 2). The combined F2 families in this naturally infested field test segregated 120 partially resistant:54 susceptible when the break point for partial resistant vs. susceptible was set at 22 (= mean + se of the combined F2) lettuce aphids per plant, an acceptable fit to a three partially resistant:one susceptible (χ2 = 3.38, P = 0.07).

Fig. 2.
Fig. 2.

Frequency distributions of numbers of lettuce aphids per plant in a naturally infested, open field; completely resistant ‘Barcelona’ and IVT 280, susceptible ‘Salinas’, partially resistant PI 491093, F2 Barcelona × PI 491093, and F2 Salinas × PI 491093 (composite of seven families).

Citation: HortScience horts 47, 2; 10.21273/HORTSCI.47.2.179

These results suggest that resistance to lettuce aphid strain Nr:0 is likely conferred by multiple alleles. IVT 280 is the source of Nr, which confers complete resistance and is dominant to partial resistance in other L. virosa accessions as previously reported (Eenink and Dieleman, 1983). The F2 Barcelona × PI 491093 segregation had no susceptible segregants, which indicates that complete resistance in ‘Barcelona’ is allelic to partial resistance in PI 491093. Partial resistance in PI 491093 was dominant to susceptibility in ‘Salinas’. We propose the revised gene symbols for resistance to lettuce aphid strain Nr:0: Nr:0C for complete resistance and Nr:0P for partial resistance, which was originally designated as nr (Eenink and Dieleman, 1983) but may now be regarded as the symbol for susceptibility to all strains of lettuce aphid. The dominance relationships among these three alleles are Nr:0C (in IVT 280, ‘Barcelona’) > Nr:0P (in PI 491093) > nr (in susceptible genotypes).

Inheritance of resistance in PI 274378.

Mean numbers of lettuce aphids on susceptible ‘Salinas’ and PI 273597 were significantly higher in three tests done in different seasons of the year than on resistant ‘Barcelona’, PI 2742378, IVT 280, and reciprocal F1 progenies from crosses of PI 273597 and PI 274378 with IVT 280 and F1 PI 274378 × CGN05332 (Table 3). There were no significant differences in number of lettuce aphids per plant between ‘Salinas’ and PI 273597 (L. virosa). Resistance to lettuce aphid in PI 274378 was dominant in the F1 PI 274378 × CGN05332 (Spring test) and was comparable to IVT 280 and ‘Barcelona’.

Table 3.

Mean numbers ± se of lettuce aphids per plant at various days post-infestation in three greenhouse tests that included ‘Salinas’, ‘Barcelona’, PI 273597, PI 2742378 and IVT 280, and PI 274375, and F1 and F2 progenies from crosses among the L. virosa accessions; each plant infested with five 24- to 48-h-old nymphs; greenhouse; Salinas, CA.

Table 3.

CGN05332 exhibited partial resistance in a separate greenhouse test with ‘Salinas’; their respective mean number of lettuce aphids per plant 28 dpi were 6.8 ± 1.6 and 40.3 ± 10.0. The F2 PI 274378 × CGN05332 did not segregate; mean numbers of aphids per plant 14 and 21 dpi were less than 1.0 (Table 3); at 28 dpi, no aphids were on 114 plants, one plant had a single aphid, and one plant had seven aphids. These data are comparable with the F2 Barcelona × PI 491093 data. Likewise, the F2 IVT 280 x PI 274378 did not segregate and mean numbers of aphids per plant 14 and 21 dpi were also less than 1.0 (Table 3). These data demonstrate that complete resistance to lettuce aphid in PI 274378 is not the result of a unique new gene, but is allelic with the Nr:0C gene in IVT 280.

Nature of resistance in PI 491093.

Partial resistance permits lettuce aphids to reproduce; the numbers of aphids per plant ranges over a wide range as these and previous (Eenink and Dieleman, 1983) data show. Numbers of live lettuce aphids were counted at different intervals starting 2 dpi for periods ranging up to 40 dpi in tests in which plants of PI 491093, ‘Barcelona’, ‘Dynamite’, IVT 280, and ‘Salinas’ were infested with 10 24-h-old nymphs (Fig. 3A–C). Numbers of live aphids declined on susceptible, partially resistant, and completely resistant genotypes by 2 dpi in the three tests (Fig. 3A–C). The reduction was minimal or approximately one-third on susceptible and partially resistant genotypes; reduction was more severe on resistant genotypes, from approximately half to 100%. After a short lag time, numbers of aphids on susceptible and partially resistant genotypes increased with a much greater increase on susceptible ‘Salinas’. In one test, the numbers of aphids per plant on PI 491093 were virtually indistinguishable from completely resistant genotypes from 14 through 40 dpi (Fig. 3B). In another test, mean numbers of aphids remained approximately five per plant except for a period ≈14 dpi (Fig. 3C).

Fig. 3.
Fig. 3.

Mean numbers of lettuce aphids per plant on resistant and susceptible lettuce at various days post-infestation. Plants infested with 10 24-h-old nymphs per plant (A–C) or a single 24-h-old nymph per plant (D–F) in the greenhouse.

Citation: HortScience horts 47, 2; 10.21273/HORTSCI.47.2.179

In three similar tests, plants were infested with a single 24-h nymph. The initial count was made 10 to 20 dpi and the final count was made from 21 to 111 dpi (Fig. 3D–F). In one test (Fig. 3D) there was no significant difference between ‘Salinas’ and PI 491093 for number of aphids at 10 dpi, but by 21 dpi, PI 491093 had significantly fewer aphids than ‘Salinas’, although the mean number of aphids per plant on either was very low. Numbers of lettuce aphids on ‘Salinas’ and PI 491093 followed similar patterns through ≈30 dpi (Fig. 3E–F), although the numbers on PI 491093 were significantly lower than on ‘Salinas’ but not significantly greater than on IVT 280 or ‘Barcelona’ through the end of the tests.

Numbers of lettuce aphids per plant were significantly higher on ‘Salinas’ than ‘Barcelona’, IVT 280, and PI 491093 in a caged field test (Table 4). ‘Barcelona’ and IVT 280 were essentially aphid-free, whereas mean numbers of aphids on PI 491093 ranged from 17.4 when infested immediately after transplanting to 1.6 when infested 4 weeks post-transplanting. Partial resistance provided a marked and significant level of protection against lettuce aphid infestation in this test. The cages were not completely insect-proof as indicated by high numbers of other aphid species on the plants regardless of their aphid resistance genotype (Table 4). These data confirm the specificity resistance in lettuce aphid as previously reported (Reinink et al., 1995). Other crops have been noted as hosts of different aphid species, whereas their resistance to aphids is species- or biotypes-specific (Dogimont et al., 2010). A given lettuce genotype may possess resistance to more than one aphid (Reinink and Dieleman, 1989).

Table 4.

Mean numbers ± se of lettuce aphid and other unidentified aphid spp. on lettuce aphid-susceptible ‘Salinas’, partially resistant PI 491093, and completely resistant ‘Barcelona’, and IVT 280 at 28 d post-infestation after three infestation dates of plants in field cages (No. = 5) and in a naturally infested open field; 2008.z

Table 4.

Partial resistance in PI 491093 provided protection against natural infestation by lettuce aphid in a replicated, naturally infested field test. ‘Salinas’ had significantly greater numbers of lettuce aphids than PI 491093, ‘Barcelona’, and IVT 280 (Table 4). Other aphid species were present at very low levels.

Partial resistance to lettuce aphid in L. serriola accession PI 491093 is dominant to susceptibility in L. sativa cultivars, e.g., ‘Salinas’. Partial resistance is controlled by a single dominant gene that appears to be identical to the gene in L. virosa accession IVT 273 and allelic to the gene for complete resistance in L. virosa accession IVT 280, the source of resistance for all currently available lettuce aphid-resistant lettuce cultivars. Transfer of complete resistance from IVT 280 was a lengthy, complicated process that involved interspecific crosses to introgress a unique gene from a tertiary gene pool into cultivated lettuce (Arend et al., 1999; Eenink et al., 1982a; Lebeda et al., 2007).

Partial resistance to lettuce aphid provides a level of protection that is of potential value to lettuce production. Greenhouse data suggest increased expression or effectiveness of partial resistance with plant growth. Partial resistance may, either alone or as a component of integrated pest management, delay or prevent emergence of resistance-breaking strains where complete resistance has not been widely deployed. Lactuca serriola is in the primary gene pool for cultivated lettuce; transfer of partial resistance from PI 491093 is, therefore, expected to be easier than transfer from the tertiary gene pool.

Literature Cited

  • Anonymous2004Australian Vegetable and Potato Growers Federation. Lettuce aphid outbreak update. <http://www.ausveg.com.au/assets/contentitems/public/1268/LettuceAphidFAQsConsumers.pdf>.

  • Anonymous2008Resistance to the lettuce leaf aphid Nasonovia ribisnigri. Disclosure Number IPCOM000176078D dated 4 Nov. 2008. IP.com Prior Art Database Disclosure. <http://ip.com/IPCOM/000176078>.

  • ArendA.J.M.d.2003The possibility of Nasonovia ribisnigri resistance breaking biotype development due to plant host resistance: A literature study p. 75–81. In: Hintum T.J.L.v. A. Lebeda D.A. Pink and J.W. Schut (eds.). EUCARPIA leafy vegetables 2003. Proc. of the EUCARPIA Meeting on Leafy Vegetables Genetics and Breeding Noordwijkerhout The Netherlands 19–21 Mar. 2003. Centre for Genetic Resources Wageningen The Netherlands

  • ArendA.J.M.d.EsterA.SchijndelJ.T.v.1999Developing an aphid-resistant butterhead lettuce “Dynamite”. Eucarpia Leafy vegetables '99. Palacky University Olomouc Czech Republic. p. 149–157.

  • BarberM.D.MooresG.D.TatchellG.M.ViceW.E.DenholmI.1999Insecticide resistance in the currant-lettuce aphid, Nasonovia ribisnigri (Homoptera: Aphididae) in the UKBul. Ent. Res.891723

    • Search Google Scholar
    • Export Citation
  • BluaM.J.1997Vectors p. 51–54. In: Davis R.M. K.V. Subbarao R.N. Raid and E.A. Kurtz (eds.). Compendium of lettuce diseases. APS Press St. Paul MN.

  • ChaneyB.1999Lettuce aphid update. Monterey County Crop Notes. University of California Cooperative Extension Salinas CA. April:1 7.

  • DavisR.M.SubbaraoK.V.RaidR.N.KurtzE.A.1997Compendium of lettuce diseases. APS Press St. Paul MN.

  • DogimontC.BendahmaneA.ChovelonV.BoissotN.2010Host plant resistance to aphids in cultivated crops: Genetic and molecular bases, and interactions with aphid populationsComptes Rendus Biologies333566573

    • Search Google Scholar
    • Export Citation
  • EeninkA.H.DielemanL.F.1983Inheritance of resistance to the leaf aphid Nasonovia ribis-nigri in the wild lettuce species Lactuca virosaEuphytica32691695

    • Search Google Scholar
    • Export Citation
  • EeninkA.H.GroenwoldR.DielemanF.L.1982aResistance of lettuce (Lactuca) to the leaf aphid Nasonovia ribisnigri. 1. Transfer of resistance from L. virosa to L. sativa by interspecific crosses and selection of resistant breeding linesEuphytica31291300

    • Search Google Scholar
    • Export Citation
  • EeninkA.H.DielemanF.L.GroenwoldR.1982bResistance of lettuce (Lactuca) to the leaf aphid Nasonovia ribis nigri. 2. Inheritance of the resistanceEuphytica31301304

    • Search Google Scholar
    • Export Citation
  • ForbesA.R.MacKenzieJ.R.1982The lettuce aphid, Nasonovia ribisnigri (Homoptera: Aphididae) damaging lettuce crops in British ColumbiaJ. Ent. Soc. British Columbia792831

    • Search Google Scholar
    • Export Citation
  • LauritzenE.2011Monterey County Crop report 2010. Office of the Agricultural Commissioner Monterey County CA. <http://ag.co.monterey.ca.us/>.

  • LebedaA.RyderE.J.GrubeR.DolezalovaI.KriskovaE.2007Lettuce (Asteraceae; Lactuca spp.) p. 377–472. In: Singh R.J. (ed.). Genetic resources chromosome engineering and crop improvement. CRC Press New York NY.

  • LiuY.-B.2004Distribution and population development of Nasonovia ribisnigri (Homoptera: Aphididae) in iceberg lettuceJ. Econ. Entomol.97883890

    • Search Google Scholar
    • Export Citation
  • LiuY.-B.2005Ultralow oxygen treatment for postharvest control of Nasonovia ribisnigri (Homoptera: Aphididae) on iceberg lettuceJ. Econ. Entomol.9818991904

    • Search Google Scholar
    • Export Citation
  • LiuY.-B.McCreightJ.D.2006Responses of Nasonovia ribisnigri (Homoptera: Aphididae) to susceptible and resistant lettuceJ. Econ. Entomol.99972978

    • Search Google Scholar
    • Export Citation
  • McCreightJ.D.2008Potential sources of genetic resistance in lettuce to the lettuce aphid, Nasanovia ribisnigri (Mosely) (Homoptera: Aphididae)HortScience4313551358

    • Search Google Scholar
    • Export Citation
  • MouB.2009Nutrient content of lettuce and its improvementCurrent Nutr. Food Sci.5242248

  • PainterR.H.1980Breeding plants resistant to insects. John Wiley & Sons New York NY.

  • PalumboA.D.2000Seasonal abundance and control of the lettuce aphid Nasonovia ribisnigri on head lettuce in Arizona. <http://ag.arizona.edu/pubs/crops/az1177-1171m.pdf>. In: Byrne D.N. and P. Baciewicz (eds.). 2000 vegetable report. University of Arizona College of Agriculture 2000 and Life Sciences. <http://ag.arizona.edu/pubs/crops/az1177/>.

  • ReininkK.DielemanF.L.1989Resistance in lettuce to the leaf aphids Macrosiphum euphorbiae and Uroleucon sonchiAnn. Appl. Biol.115489498

    • Search Google Scholar
    • Export Citation
  • ReininkK.DielemanF.L.GroenwoldR.1995Inheritance of partial resistance to the leaf aphids Macrosiphum euphorbiae and Uroleucon sonchi in lettuceAnn. Appl. Biol.127413424

    • Search Google Scholar
    • Export Citation
  • RyderE.J.1979a‘Salinas’ lettuceHortScience14283284

  • RyderE.J.1979bLeafy salad vegetables. AVI Publ. Co. Westport CT.

  • RyderE.J.2002The new salad crop revolution p. 408–412. In: Janick J. and A. Whipkey (eds.). Trends in new crops and new uses. ASHS Press Alexandria VA.

  • StufkensM.A.W.NicholS.E.BulmanS.R.DraytonG.M.2004Incursion of the lettuce aphid into Tasmania—Could it have blown over from New Zealand?New Zealand Plant Protection57340(abstr.).

    • Search Google Scholar
    • Export Citation
  • StufkensM.A.W.TeulonD.A.J.2003Distribution, host range and flight pattern of the lettuce aphid in New ZealandNew Zealand Plant Protection562732

    • Search Google Scholar
    • Export Citation
  • StufkensM.A.W.TeulonD.A.J.BulmanS.R.2002Nasonovia ribisnigri, a new aphid pest found on lettuces (Lactuca sativa L.) and Ribes spp. in CanterburyNew Zealand Plant Protection55437(abstr.).

    • Search Google Scholar
    • Export Citation
  • StufkensM.A.W.WallaceA.R.2004Effectiveness and persistence of six insecticides for control of lettuce aphid on field lettuce in Canterbury New Zealand. New Zealand Plant Protection Volume 57 2004. Proc. of a conference Hamilton New Zealand 10–12 Aug. 2004. p. 233–238

  • ThabuisA.P.P.TeekensK.C.Van HerwijnenZ.O.2011Lettuce that is resistant to the lettuce aphid Nasonovia ribisnigri biotype 1. World Intellectual Property Organization. PCT/EP2010/067588

  • USDA2011aEconomic Research Service U.S. Lettuce Statistics. <http://usda.mannlib.cornell.edu/MannUsda/viewDocumentInfo.do?documentID=1576>.

  • USDA2011bARS National Genetic Resources Program. Germplasm Resources Information Network—(GRIN) [online database]. National Germplasm Resources Laboratory Beltsville MD. <http://www.ars-grin.gov/cgi-bin/npgs/swish/accboth?query=PI+273597>.

  • USDA2011cARS National Genetic Resources Program. Germplasm Resources Information Network—(GRIN) [online database]. National Germplasm Resources Laboratory Beltsville MD. <http://www.ars-grin.gov/cgi-bin/npgs/acc/display.pl?1205938>.

  • USDA2011dARS National Genetic Resources Program. Germplasm Resources Information Network—(GRIN) [online database]. National Germplasm Resources Laboratory Beltsville MD. <http://www.ars-grin.gov/cgi-bin/npgs/acc/display.pl?1205936>.

  • USDA2011eARS National Genetic Resources Program. Germplasm Resources Information Network—(GRIN) [online database]. National Germplasm Resources Laboratory Beltsville MD. <http://www.ars-grin.gov/cgi-bin/npgs/acc/display.pl?1386029>.

  • YatesF.1931Contingency tables involving small numbers and the χ2 testSuppl. J. Royal Stat. Soc.1215235

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Contributor Notes

Funded in part by a grant from the California Leafy Greens Research Program.We thank Patti Fashing and Jeff Wasson for assistance in the field tests.USDA is an equal opportunity provider and employer.Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the U.S. Department of Agriculture.

To whom reprint requests should be addressed; e-mail jim.mccreight@ars.usda.gov.

  • View in gallery

    Frequency distributions of numbers of lettuce aphids per plant of susceptible ‘Salinas’, partially resistant PI 491093 and F2 Salinas × PI 491093 at 15 dpi (A) and 36 dpi (B); infested with five 24- to 48-h-old nymphs per plant in the greenhouse. dpi = days post-infestation.

  • View in gallery

    Frequency distributions of numbers of lettuce aphids per plant in a naturally infested, open field; completely resistant ‘Barcelona’ and IVT 280, susceptible ‘Salinas’, partially resistant PI 491093, F2 Barcelona × PI 491093, and F2 Salinas × PI 491093 (composite of seven families).

  • View in gallery

    Mean numbers of lettuce aphids per plant on resistant and susceptible lettuce at various days post-infestation. Plants infested with 10 24-h-old nymphs per plant (A–C) or a single 24-h-old nymph per plant (D–F) in the greenhouse.

  • Anonymous2004Australian Vegetable and Potato Growers Federation. Lettuce aphid outbreak update. <http://www.ausveg.com.au/assets/contentitems/public/1268/LettuceAphidFAQsConsumers.pdf>.

  • Anonymous2008Resistance to the lettuce leaf aphid Nasonovia ribisnigri. Disclosure Number IPCOM000176078D dated 4 Nov. 2008. IP.com Prior Art Database Disclosure. <http://ip.com/IPCOM/000176078>.

  • ArendA.J.M.d.2003The possibility of Nasonovia ribisnigri resistance breaking biotype development due to plant host resistance: A literature study p. 75–81. In: Hintum T.J.L.v. A. Lebeda D.A. Pink and J.W. Schut (eds.). EUCARPIA leafy vegetables 2003. Proc. of the EUCARPIA Meeting on Leafy Vegetables Genetics and Breeding Noordwijkerhout The Netherlands 19–21 Mar. 2003. Centre for Genetic Resources Wageningen The Netherlands

  • ArendA.J.M.d.EsterA.SchijndelJ.T.v.1999Developing an aphid-resistant butterhead lettuce “Dynamite”. Eucarpia Leafy vegetables '99. Palacky University Olomouc Czech Republic. p. 149–157.

  • BarberM.D.MooresG.D.TatchellG.M.ViceW.E.DenholmI.1999Insecticide resistance in the currant-lettuce aphid, Nasonovia ribisnigri (Homoptera: Aphididae) in the UKBul. Ent. Res.891723

    • Search Google Scholar
    • Export Citation
  • BluaM.J.1997Vectors p. 51–54. In: Davis R.M. K.V. Subbarao R.N. Raid and E.A. Kurtz (eds.). Compendium of lettuce diseases. APS Press St. Paul MN.

  • CGN2011The Centre for Genetic Resources The Netherlands. <http://www.cgn.wur.nl/UK/CGN+Plant+Genetic+Resources/Search+and+…mplasm/On+line+search/Default.htm?page=detail&acnumber=CGN05332>.

  • ChaneyB.1999Lettuce aphid update. Monterey County Crop Notes. University of California Cooperative Extension Salinas CA. April:1 7.

  • DavisR.M.SubbaraoK.V.RaidR.N.KurtzE.A.1997Compendium of lettuce diseases. APS Press St. Paul MN.

  • DogimontC.BendahmaneA.ChovelonV.BoissotN.2010Host plant resistance to aphids in cultivated crops: Genetic and molecular bases, and interactions with aphid populationsComptes Rendus Biologies333566573

    • Search Google Scholar
    • Export Citation
  • EeninkA.H.DielemanL.F.1983Inheritance of resistance to the leaf aphid Nasonovia ribis-nigri in the wild lettuce species Lactuca virosaEuphytica32691695

    • Search Google Scholar
    • Export Citation
  • EeninkA.H.GroenwoldR.DielemanF.L.1982aResistance of lettuce (Lactuca) to the leaf aphid Nasonovia ribisnigri. 1. Transfer of resistance from L. virosa to L. sativa by interspecific crosses and selection of resistant breeding linesEuphytica31291300

    • Search Google Scholar
    • Export Citation
  • EeninkA.H.DielemanF.L.GroenwoldR.1982bResistance of lettuce (Lactuca) to the leaf aphid Nasonovia ribis nigri. 2. Inheritance of the resistanceEuphytica31301304

    • Search Google Scholar
    • Export Citation
  • ForbesA.R.MacKenzieJ.R.1982The lettuce aphid, Nasonovia ribisnigri (Homoptera: Aphididae) damaging lettuce crops in British ColumbiaJ. Ent. Soc. British Columbia792831

    • Search Google Scholar
    • Export Citation
  • LauritzenE.2011Monterey County Crop report 2010. Office of the Agricultural Commissioner Monterey County CA. <http://ag.co.monterey.ca.us/>.

  • LebedaA.RyderE.J.GrubeR.DolezalovaI.KriskovaE.2007Lettuce (Asteraceae; Lactuca spp.) p. 377–472. In: Singh R.J. (ed.). Genetic resources chromosome engineering and crop improvement. CRC Press New York NY.

  • LiuY.-B.2004Distribution and population development of Nasonovia ribisnigri (Homoptera: Aphididae) in iceberg lettuceJ. Econ. Entomol.97883890

    • Search Google Scholar
    • Export Citation
  • LiuY.-B.2005Ultralow oxygen treatment for postharvest control of Nasonovia ribisnigri (Homoptera: Aphididae) on iceberg lettuceJ. Econ. Entomol.9818991904

    • Search Google Scholar
    • Export Citation
  • LiuY.-B.McCreightJ.D.2006Responses of Nasonovia ribisnigri (Homoptera: Aphididae) to susceptible and resistant lettuceJ. Econ. Entomol.99972978

    • Search Google Scholar
    • Export Citation
  • McCreightJ.D.2008Potential sources of genetic resistance in lettuce to the lettuce aphid, Nasanovia ribisnigri (Mosely) (Homoptera: Aphididae)HortScience4313551358

    • Search Google Scholar
    • Export Citation
  • MouB.2009Nutrient content of lettuce and its improvementCurrent Nutr. Food Sci.5242248

  • PainterR.H.1980Breeding plants resistant to insects. John Wiley & Sons New York NY.

  • PalumboA.D.2000Seasonal abundance and control of the lettuce aphid Nasonovia ribisnigri on head lettuce in Arizona. <http://ag.arizona.edu/pubs/crops/az1177-1171m.pdf>. In: Byrne D.N. and P. Baciewicz (eds.). 2000 vegetable report. University of Arizona College of Agriculture 2000 and Life Sciences. <http://ag.arizona.edu/pubs/crops/az1177/>.

  • ReininkK.DielemanF.L.1989Resistance in lettuce to the leaf aphids Macrosiphum euphorbiae and Uroleucon sonchiAnn. Appl. Biol.115489498

    • Search Google Scholar
    • Export Citation
  • ReininkK.DielemanF.L.GroenwoldR.1995Inheritance of partial resistance to the leaf aphids Macrosiphum euphorbiae and Uroleucon sonchi in lettuceAnn. Appl. Biol.127413424

    • Search Google Scholar
    • Export Citation
  • RyderE.J.1979a‘Salinas’ lettuceHortScience14283284

  • RyderE.J.1979bLeafy salad vegetables. AVI Publ. Co. Westport CT.

  • RyderE.J.2002The new salad crop revolution p. 408–412. In: Janick J. and A. Whipkey (eds.). Trends in new crops and new uses. ASHS Press Alexandria VA.

  • StufkensM.A.W.NicholS.E.BulmanS.R.DraytonG.M.2004Incursion of the lettuce aphid into Tasmania—Could it have blown over from New Zealand?New Zealand Plant Protection57340(abstr.).

    • Search Google Scholar
    • Export Citation
  • StufkensM.A.W.TeulonD.A.J.2003Distribution, host range and flight pattern of the lettuce aphid in New ZealandNew Zealand Plant Protection562732

    • Search Google Scholar
    • Export Citation
  • StufkensM.A.W.TeulonD.A.J.BulmanS.R.2002Nasonovia ribisnigri, a new aphid pest found on lettuces (Lactuca sativa L.) and Ribes spp. in CanterburyNew Zealand Plant Protection55437(abstr.).

    • Search Google Scholar
    • Export Citation
  • StufkensM.A.W.WallaceA.R.2004Effectiveness and persistence of six insecticides for control of lettuce aphid on field lettuce in Canterbury New Zealand. New Zealand Plant Protection Volume 57 2004. Proc. of a conference Hamilton New Zealand 10–12 Aug. 2004. p. 233–238

  • ThabuisA.P.P.TeekensK.C.Van HerwijnenZ.O.2011Lettuce that is resistant to the lettuce aphid Nasonovia ribisnigri biotype 1. World Intellectual Property Organization. PCT/EP2010/067588

  • USDA2011aEconomic Research Service U.S. Lettuce Statistics. <http://usda.mannlib.cornell.edu/MannUsda/viewDocumentInfo.do?documentID=1576>.

  • USDA2011bARS National Genetic Resources Program. Germplasm Resources Information Network—(GRIN) [online database]. National Germplasm Resources Laboratory Beltsville MD. <http://www.ars-grin.gov/cgi-bin/npgs/swish/accboth?query=PI+273597>.

  • USDA2011cARS National Genetic Resources Program. Germplasm Resources Information Network—(GRIN) [online database]. National Germplasm Resources Laboratory Beltsville MD. <http://www.ars-grin.gov/cgi-bin/npgs/acc/display.pl?1205938>.

  • USDA2011dARS National Genetic Resources Program. Germplasm Resources Information Network—(GRIN) [online database]. National Germplasm Resources Laboratory Beltsville MD. <http://www.ars-grin.gov/cgi-bin/npgs/acc/display.pl?1205936>.

  • USDA2011eARS National Genetic Resources Program. Germplasm Resources Information Network—(GRIN) [online database]. National Germplasm Resources Laboratory Beltsville MD. <http://www.ars-grin.gov/cgi-bin/npgs/acc/display.pl?1386029>.

  • YatesF.1931Contingency tables involving small numbers and the χ2 testSuppl. J. Royal Stat. Soc.1215235

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