Variation in Resistance Mechanisms to the Green Peach Aphid Among Different Prunus persica...

PLANT RESISTANCE

Variation in Resistance Mechanisms to the Green Peach Aphid AmongDifferent Prunus persica Commercial Cultivars

J. A. VERDUGO,1,2 T. MENDEZ,1 S. A. ORTIZ–MARTINEZ,1 R. CUMSILLE,1 AND C. C. RAMIREZ1,3

J. Econ. Entomol. 105(5): 1844Ð1855 (2012); DOI: http://dx.doi.org/10.1603/EC12100

ABSTRACT Peaches and nectarines are frequently attacked by the green peach aphid Myzuspersicae (Sulzer), with signiÞcant negative impacts on fruit production. The genetic variability ofresistance to this aphid among commercial cultivars of Prunus persica (L.) Batsch and Prunus persicavarietynectarinawas evaluated in this study. In total, 16 cultivars ofP. persicawere selected to evaluatethe occurrence and population growth rate of M. persicae in commercial orchards, as well as inno-choice and probing behavior laboratory assays. The results showed variability between cultivarsin resistance and susceptibility to M. persicae, with three cultivars exhibiting different signatures ofresistance. The peach cultivar ÔElegant LadyÕ exhibited a low occurrence of aphids in the orchard, alow rate of growth, moderate leaf-rejection in a no-choice test and a higher number and longer periodof salivation into sieve elements, suggesting resistance at the phloematic level. The nectarine cultivarÔAugust RedÕ also exhibited low aphid occurrence in the orchard, a low rate of growth, and resistanceat the prephloem and phloem levels. Finally, the nectarine ÔJuly Red-NS92� exhibited a low occurrenceof aphids in the orchard, a higher number of rejections in no-choice assays and no ingestion of phloemduring the probing behavior experiments, suggesting prephloematic resistance. The rest of thecultivars studied exhibited clear susceptibility. Hence, different resistance mechanisms are apparentamong the studied cultivars. The information gathered in this study regarding the resistance to M.persicaemay assist breeding programs aimed at increasing aphid resistance to peaches and nectarines.

KEY WORDS resistance, performance, probing, no-choice, aphid

Peaches (Prunus persica (L.) Batsch) and nectarines(Prunus persica variety nectarina) are two of the mostimportant fruits in the world. There is a continuousdevelopment of new cultivars with the characteristicsrequired by producers and consumers (Sherman et al.1996, Infante et al. 2008). However, as with all treefruits, peaches and nectarines are affected by a num-ber of pathogens and insect pests whose inadequatecontrol may affect fruit yields up to 2 yr. One of themost important pests of peaches and nectarines world-wide is the green peach aphidMyzus persicae (Sulzer)(Hemiptera: Aphididae), which is a generalist aphidthat uses P. persica trees as a primary host and speciesfrom �40 plant families as secondary hosts (Blackmanet al. 2000). The green peach aphid produces leafcurling and stunting and devitalization in stems andreduces fruit quality by altering the fruit growth pat-tern (Pascal et al. 2002, Penvern et al. 2010). In addi-tion, this aphid species is responsible for transmittingthe Plum pox potyvirus to P. persica (Isac et al. 1998).A wide range of insecticide resistance mechanismshave also been reported in this aphid species (Field et

al. 1988, Moores et al. 1994, Blackman et al. 1995,Foster et al. 1998, MartinezÐTorres et al. 1999, Bass etal. 2011). Thus, breeding programs would gain frominformation regarding resistance variation to M. per-sicae among different commercial peach and nectar-ine cultivars.

Peach and nectarine resistance mechanisms toaphids, as well as to other pests and diseases, have beenintensively studied (Kervella et al. 1998; Monet et al.1998; Pascal and MonteuxÐCaillet 1998; Sauge et al.1998a,b, 2011; Lambert and Pascal 2011). Studies ad-dressing peach and nectarine resistance toM. persicaehave used performance experiments based on the in-trinsic rate of natural increase rm (Le Roux et al. 2007),monitoring of probing behavior (EPG) (Sauge et al.1998a, Pompon et al. 2010) and no-choice testing(Sauge et al. 1998b, Margaritopoulos et al. 2005). EPGstudies have produced reliable information concern-ing the location of the resistance mechanisms. Forexample, these types of experiments located the re-sistance mechanism of the ÔMalo KonareÕ peach cul-tivar in the vascular system and found it to provideantibiosis resistance, whereas antixenosis was sug-gested for the ÔWeeping Flower PeachÕ cultivar (Mo-net and Massonie 1994, Monet et al. 1998, Sauge et al.1998a,b). Similarly, by monitoring probing behavior ofM. persicae on the ÔRubiraÕ cultivar, antixenosis wasfound to be reinforced by induced resistance (Sauge

1 Instituto de Biologõa y Biotecnologõa Vegetal, Universidad deTalca, 2 Norte 685, Talca, Chile.

2 Gembloux Agro-Bio Tech, Universite de Liege, UnitedÕEntomologie Fonctionnelle et Evolutive, Passage des Deportes 2,5030 Gembloux, Belgium.

3 Corresponding author, e-mail: [email protected].

0022-0493/12/1844Ð1855$04.00/0 � 2012 Entomological Society of America

et al. 1998b, 2002). Genes conferring monogenic re-sistance to this aphid have been described for theWeeping Flower Peach and Rubira cultivars (Monetand Massonie 1994, Lambert and Pascal 2011). How-ever, studies on the wild Prunus species, P. davidiana,suggested that this cultivar appears to have a phloem-based resistance mechanism (Sauge et al. 1998a,b).Hence, the resistance mechanism of Prunus toM. per-sicae is likely different depending on the cultivar orspecies. Information regarding resistance patterns ofcurrently used commercial cultivars of peaches andnectarines would provide knowledge on aphid man-agement for commercial cultivars in general and tobreeding programs that include commercial cultivars.

In Chile,M. persicae produces serious damage to P.persica (peaches and nectarines) plantations (Rosaleset al. 1998, Reyes et al. 2003). The implementation ofIntegrated Fruit Production (IFP), which was ad-opted to reduce the quantity of chemical inputs usedto protect crops from the green peach aphid (Grechiet al. 2008), is a promising alternative to the conven-tional pest management system because, althoughdamage and disease is higher than in the conventionalsystem, the aphid remains under the tolerable thresh-old for economic damage (Cooper et al. 2001). IFP issuitable in cases in which resistance variation of com-mercial cultivars is known.

This study aimed to determine the variation in re-sistance mechanisms to attack by the M. persicae onseveral commercial cultivars of P. persica, includingpeaches and nectarines commonly planted in centralChile. Because measuring herbivore response in termsof performance, preference or probing behavior is anintegrative and functionally relevant estimate of re-sistance (Leimu and Koricheva 2006), herein we re-port results on 1) the occurrence of M. persicae incommercial orchards, 2) performance variation (pop-ulation growth rate) of M. persicae on these cultivarsduring two seasons in the orchards, and 3) laboratoryassays assessing the rejection of M. persicae for these

cultivars, which included no-choice experiments andprobing behavior recordings.

Materials and Methods

AphidOccurrence onP. persicaOrchards.BetweenAugust 2007 and March 2008, 15 orchards of variouspeach and nectarine cultivars were monitored to as-sess the presence of the M. persicae (Table 1). Thesecultivars are widely cultivated in central Chile, andtheir fruit is exported mostly as fresh fruit to severalmarkets. The orchards were located in the Quinta deTilcoco district, the Cachapoal province, and theOÕHiggins Region in Chile. For each cultivar, 100 ran-domly selected trees (planted with 3.5 m betweenrows and 2 m between trees within rows) were sam-pled every 15 d after a diagonal transect line. Onebranch per tree was visually assessed for the presenceof aphids. The occurrence of aphids was estimated asthe mean proportion of aphid-infested trees. In to-tal, 16 sampling dates were undertaken. The datawere obtained from orchards under Good Agricul-tural Practices (GAP) certiÞcation. These orchardswere under conventional pest management, andaphid occurrence was a result of natural aphid ar-rival in the orchards.Experimental Plants. All of the experiments were

performed with the commercial cultivars of P. persicaused for the aphid occurrence study (see above). Theage of trees used varied from 6 to 11 yr old, and all treeswere grown on ÔNemaguardÕ rootstocks. Differentpeach and nectarine cultivars were used for differenttypes of assays, as listed in Table 1. The selection ofthese cultivars reßected their current use by mostChilean growers (Gratacos 2004) and their availabilityin the commercial orchards during the study period.PerformanceVariation.During the spring and sum-

mer of 2009Ð2010 and 2010Ð2011, 10 orchards of var-ious P. persica cultivars were selected for performanceassays (Table 1). Within each orchard, Þve contiguous

Table 1. Cultivars of P. persica used to study occurrence of aphids in orchards and performance, probing behaviour, and no-choiceof M. persicae

CultivarOccurrencein orchardsa

PerformanceProbing behaviour

(EPG)No-choice

ÔFlavor CrestÕ Peach X X X XÔCal RedÕ Peach X X X XÔSeptember SunÕ Peach X X X XÔElegant LadyÕ Peach X X X XÔWhite LadyÕ Peach X X X XÔDU23Õ Peach X X X XÔFlame CrestÕb Peach X XÔSweet SeptemberÕb Peach X XÔRyan SunÕ Peach XÔSummer Free-N18Õ Nectarine X X X XÔAugust PearlÕ Nectarine X XÔJuly Red-NS92Õ Nectarine X X X XÔArtic SnowÕ Nectarine X X XÔSummer BrightÕ Nectarine X X XÔAugust RedÕ Nectarine X X X XÔFire BrightÕ Nectarine X

a Studies performed during season 2007Ð2008.b These cultivars were used only in no-choice because insecticides applications in the Þeld could not be avoided.

October 2012 VERDUGO ET AL.: RESISTANCE OF P. persica TO THE GREEN PEACH APHID 1845

individual trees, planted in the same row, were se-lected for experimentation and excluded from theapplication of pesticides. To avoid the effect of pes-ticide drift resulting from regular sprays on the assays,three additional adjacent rows contiguous to the se-lected trees were also excluded from pesticide appli-cation. In each of the Þve trees of each cultivar, threebranches (�30 cm) with at least Þve extended leaveswere selected and marked. The insects used for per-formance assessment were adults of M. persicae orig-inating from a multiclonal stock colony composed ofa set of individuals randomly collected the same dayof the assays from the 10 different P. persica cultivars.This approach ensured the availability of a wide ge-netic variation in the aphid populations. On each ofthe selected tree branches, 10 wingless adults from thestock colony were placed on the adaxial side of a leaf,while the rest of the branch was protected with meshbags from natural enemies and from the releasedaphids. All branches were removed after 7 d and trans-ferred to the laboratory for aphid counting. The num-ber of aphids on three branches was averaged to ob-tain one value per tree (n � 5). Performance of M.persicae in each cultivar was calculated using popula-tion growth rate (PGR), which allows an estimationof the developmental rate and nymphal mortality (Go-telli 2001), which is calculated as (ln N2 � ln N1)/(t2�t1), where N1 is the initial number of aphids, N2

is the Þnal number of aphids, and (t2 � t1) is thenumber of days of the experiment (7 d).No-ChoiceTest.Young shoots with at least 10 leaves

were collected from 14 P. persica cultivars (Table 1),placed into pots with 300 ml of water and maintainedunder controlled conditions (20�C � 2 and a photo-period of 16:8 [L:D] h) in a growth chamber. One leaffrom each cultivar was extracted from the shoot, andthe petioles were covered with humid cotton to avoiddehydration. Each leaf was placed in a petri dish (10cm diameter), and 10 wingless adult aphids of M.persicae were gently placed on the adaxial side of theleaves.TheM.persicae individuals thatwereusedwereobtained from a multiclonal stock colony maintainedon sweet-pepper Capsicum annumm L. for at leastthree parthenogenetic generations before the no-choice tests. The number of individual aphids on theleaves, aphids walking outside the leaves and deadaphids were registered at 1, 2, 3, 6, 12, and 24 h afterthe start of the experiments. In total, 15 replicates percultivar were conducted.Aphid Probing Behavior. The electron penetration

graph (EPG-DC) technique was used to assess theprobing behavior of M. persicae on the P. persica cul-tivars. In this technique, the insect and the plant areboth part of an electrical circuit. EPG ampliÞes voltageßuctuations resulting from the insect-plant interac-tion, producing waveforms that are stored and ana-lyzed. Different types of signals are emitted depend-ing on the location and activities performed by theaphid stylet inside the plant tissue (Tjallingii and Esch1993, Alvarez et al. 2006). Acceptance (e.g., sustainedphloem ingestion) or rejection (e.g., no penetration ofstylet) may reßect differences in the levels of resis-

tance among cultivars (Sauge et al. 2006). Using theEPG technique, it is also possible to recognize differ-ent waveforms, such F, which reßects stylet difÞcul-ties during penetration at the epidermis/mesophylllevel; C, which indicates intercellular penetration bythe stylet; E1, which is associated with salivary secre-tion into the sieve elements; E2, which indicates sapingestion; and pd, which corresponds to potentialdrops because of intracellular stylet tip punctureswhen the stylet passes through membrane cells. Thesedrops can be divided into subphases I, II-1, II-2, II-3,and III (Powell 2005, Tjallingii 2006, Tjallingii et al.2010). These waveforms are usually recorded as thenumber of events or their duration, which allows thecomputation of many nonsequential or sequential be-havioral parameters (Van Helden and Tjallingii 2000).These parameters are used to estimate the relativeimportance of prephloematic, phloematic, or all tissuefactors affecting aphid probing behavior and accord-ingly reßecting different levels of plant resistance.

EPGs were performed on branches free of aphids ofdifferent P. persica cultivars (Table 1), which werecollected from the orchards mentioned above andtransported to the laboratory. To keep the leaves freshduring the EPGs, the stems of the experimentalbranches (�15 cm) were submerged in a Pasteurpipette modiÞed to contain water. The aphids usedwere obtained from a multiclonal stock-colony of M.persicae rearedonsweetpepperandmaintainedundercontrolled conditions at 20�C � 2 and a photoperiodof 16:8 (L:D) h. For the EPGs, each aphid was initiallyimmobilized with the help of a vacuum pump, and anelectrode (4 cm of gold wire and 18 �m diameter) wasattached to the dorsum with a silver conductive ad-hesive (colloidal silver, Ted Pella, Inc., Redding, CA).Another electrode (2 mm copper wire) was intro-duced into the Pasteur pipette containing P. persicabranches. Before each recording, the aphids werestarved for 15 min and then connected to the ampliÞerGiga 4. Both electrodes were then connected to a DCcircuit and recorded continuously for 4 h. The voltageßuctuations were recorded using the program PROBE3.4 (F. Tjallingii, Laboratory of Entomology, Wage-ningen University, Netherlands). Six to 18 replicationswere performed for each cultivar over 4 h. For the dataanalysis, the Excel Workbook for the automatic cal-culation of EPG parameters was used (Sarria et al.2009). This workbook produced sets of parametersaccording to the factors involved (e.g., epidermal fac-tor, prephloem factors, xylem factors, phloem factors,and all tissues factors), which can be further analyzed.Statistical Analysis. Aphid occurrence data were

analyzed with KruskalÐWallis analysis of variance(ANOVA) on ranks. Performance data from summer2009 and spring 2010 were analyzed with one-wayANOVA for repeated measures of ranked data, withyears as repeated measures. The no-choice test wascompared with a generalized linear model with a Pois-son distribution using STATISTICA 10.0 (StatSoft2004). For EPG, multivariate analyses of variance(MANOVA) to determine whether a signiÞcant dif-ference existed among cultivars were performed for

1846 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 105, no. 5

each set of parameters, followed by Tukey test formultiple comparisons. EPG parameters with non-nor-mal distribution were normalized using ln (x � 1).Parameters that could not be normalized were ana-lyzed with KruskalÐWallis nonparametric ANOVA,followed by multiple comparisons. Given thatKruskalÐWallis tests, unlike MANOVA, do not includepossible correlations between parameters, correla-tions were independently assessed. To assess whetherany of these EPG parameters correlated with PGR ofaphids, a multiple regression analysis using these pa-rameters as predictor variables and the PGR of aphidsas the dependent variable was performed. In addition,

EPG parameters differing among cultivars (Table 2)were subjected to principal component analysis(PCA) to separate susceptible from resistant cultivarsand to Þnd which of these parameter were more as-sociated with resistance . These analyses were per-formed using SPSS 11.5 for Windows (SPSS 2001).

Results

Aphid Occurrence in P. persica Orchards. The P.persica cultivars that were monitored, includingpeaches and nectarines, exhibited relatively similarproportions of aphid occurrence, with �1 to 3% of

Table 2. Summary results of M. persicae probing behaviour on 11 cultivars of P. persica

EPG parameterÔAugust RedÕ

(N � 10)

ÔSummer Free-N18Õ

(N � 7)

ÔArtic SnowÕ(N � 9)

ÔFlavor CrestÕ(N � 9)

ÔSummer BrightÕ(N � 6)

ÔSeptember SunÕ(N � 7)

Prephloem factors1. Duration of nonprobe period

before the Þrst E (min)45.2 � 32.5a 41.6 � 39.4ab 28.1 � 25.5ab 43.2 � 45.2ab 24.3 � 28.4ab 44.8 � 22.3ab

2. Mean duration of pd (s) 3.9 � 0.5a 4.0 � 0.4ab 4.0 � 0.7a 4.0 � 0.8ab 4.1 � 0.5ab 4.4 � 0.8ab3. Total duration of F (s) 2781.3 � 2603.4c 3583.3 � 4858.5bc 381.2 � 434.1abc 386.7 � 747.5abc 916.7 � 2240.0abc 261.8 � 444.9abc4. Mean duration of F (s) 1413 � 2291.6b 966.2 � 1195.5ab 67.6 � 64.2ab 307.4 � 763.3ab 915.5 � 2240.6ab 117.1 � 204.6ab5. Mean duration of subphases

II-2 of pd (s)1.4 � 0.2a 1.2 � 0.2ab 1.4 � 0.3ab 1.4 � 0.4ab 1.6 � 0.2a 1.5 � 0.3ab

6. Mean duration of subphasesII-3 of pd (s)

1.2 � 0.3ab 1.2 � 0.2ab 1.4 � 0.3a 1.2 � 0.3ab 1.6 � 0.2ab 1.4 � 0.2ab

Phloem factors7. Number of E1 0.3 � 0.5a 2.3 � 2.9ab 1 � 0.5ab 3.3 � 2.6ab 3.5 � 4.3ab 2.4 � 2.1ab8. Duration of Þrst E (s) 422.9 � 1306.1ab 105.7 � 104.7ab 71.5 � 58.3ab 67.2 � 67.7ab 180.4 � 187.8ab 141.6 � 195.6ab9. Total duration of E1 (s) 17.8 � 32.0b 684.0 � 1026.4ab 74.3 � 59.9ab 325.4 � 385.1ab 431.6 � 504.2ab 485.3 � 518.1ab

All tissue factors10. Total duration of pd (s) 354.8 � 160.9ab 403.2 � 210.5abc 282.2 � 152.9a 455.0 � 277.0abc 287.1 � 151.8ab 281.8 � 122.3a11. Time from the beginning of

the Þrst probe to Þrst pd(min)

496.3 � 939.8ab 988.7 � 2019.6ab 593.5 � 660.0ab 1599.4 � 2447.1b 450.2 � 780.3ab 666.2 � 891.7ab

12. Total duration of nophloematic phase (min)

64.9 � 106.2b 201.3 � 109.8ab 212.1 � 79.5 180.3 � 102.4ab 228 � 19.7a 163.2 � 111.7ab

13. Time from start of EPG toÞrst E2 (min)a

233.2 � 21.4ab 192.7 � 80.8ab 239.9 � 0.0ab 187.9 � 79.6ab 230.1 � 24.3b 239.1 � 0.1ab

14. Time from Þrst probe toÞrst E2 (min)a

230.0 � 31.6ab 189.3 � 86.5ab 239.9 � 0.0ab 182.5 � 87.2ab 230.0 � 24.4b 239.1 � 0.1ab

15. Time from the beginning ofthe probe reaching the ÞrstE2 to that E2 (min)a

222.5 � 55.2ab 174.3 � 112.1ab 239.9 � 0.0ab 165.1 � 112.1ab 205.1 � 85.4b 239.1 � 0.1ab

16. Average duration of pdduring third hour

2.3 � 2.0a 3.9 � 0.5ab 2.9 � 1.8a 3.5 � 1.5ab 3.2 � 1.6ab 4.2 � 0.9ab

ÔJuly Red-NS92Õ(N � 7)

ÔDU23Õ(N � 9)

ÔCal RedÕ(N � 19)

ÔWhite LadyÕ(N � 8)

ÔElegant LadyÕ(N � 8)

Prephloem factors1. Duration of nonprobe period before

the Þrst E (min)65.1 � 73.9ab 38.3 � 29.3ab 22.2 � 22.8ab 59.8 � 74.1ab 14.8 � 24.5b

2. Mean duration of pd (s) 4.5 � 0.7ab 4.6 � 0.8ab 4.8 � 0.8ab 5.1 � 0.5b 5.1 � 0.6b3. Total duration of F (s) 0.0 � 0.0a 318.6 � 912.5ab 800.3 � 1567.4abc 1.9 � 5.2a 1.3 � 3.7a4. Mean duration of F (s) 0.0 � 0.0b 165.8 � 454.8ab 167.2 � 321.1ab 1.9 � 5.2b 0.7 � 1.8b5. Mean duration of subphases II-2 of

pd (s)1.2 � 0.2a 1.3 � 0.2ab 1.2 � 0.2ab 1.3 � 0.3ab 1.9 � 0.9b

6. Mean duration of subphases II-3 ofpd (s)

1.5 � 0.4ab 1.2 � 0.2ab 1.5 � 0.3ab 1.4 � 0.3b 1.6 � 0.3b

Phloem factors7. Number of E1 4.6 � 10.8ab 2.6 � 2.4ab 2.4 � 1.7ab 4.8 � 3.8b 7.6 � 8.0b8. Duration of Þrst E (s) 2.4 � 5.2a 132.8 � 143.5ab 199.6 � 398.1b 71.8 � 132.9ab 45.5 � 34.8ab9. Total duration of E1(s) 128.7 � 273.2ab 449.9 � 529.1ab 364.7 � 538.3ab 564.8 � 738.4ab 1465.1 � 2256.7a

All tissue factors10. Total duration of pd (s) 348.3 � 237.2ab 697.1 � 209.5c 606.7 � 220.4bc 504.7 � 244.7abc 393.5 � 235.1abc11. Time from the beginning of the

Þrst probe to Þrst pd (min)1527.0 � 3620.1ab 453.7 � 856.3ab 77.2 � 68.1a 448.0 � 571.9ab 90.8 � 571.9ab

12. Total duration of no phloematicphase (min)

66.3 � ab 174.8 � 101ab 194.5 � 87.2a 198.6 � 81.9ab 181.9 � 82.8ab

13. Time from start of EPG to Þrst E2(min)a

239.8 � 0.2ab 204.5 � 76.4ab 210.3 � 70.3ab 195.7 � 74.0ab 101.4 � 92.1a

14. Time from Þrst probe to Þrst E2(min)a

239.8 � 0.2ab 204.5 � 76.4ab 240.0 � 72.3ab 175.3 � 88.1ab 100.7 � 92.7a

15. Time from the beginning of theprobe reaching the Þrst E2 to thatE2 (min)a

239.8 � 0.2ab 190.9 � 97.2ab 194.3 � 91.1ab 130.7 � 117.0ab 77.9 � 100.9a

16. Average duration of pd duringthird hour

2.3 � 2.2a 4.5 � 0.8ab 3.7 � 1.7ab 5.2 � 0.6b 4.8 � 0.5b

a Parameter including total duration of the recording when the E2 waveform was not observed during the recording.


buds infected by aphids (Fig. 1), although there wassigniÞcant variation among cultivars (H � 24.76; P �0.037). Only the nectarine cultivars ÔAugust RedÕ andÔSummer BrightÕ exhibited a higher proportion of in-festation, with over 20% occurrence. It is important tomention that the presence of the parasitoids Aphidiuscolemani and Aphidius rhopalosiphi (Hymenoptera:Braconidae) was detected in low abundances in somecultivars, but their prevalence could not be assessed.Performance Variation. M. persicae displayed sig-

niÞcant variation in PGR on different P. persica cul-

tivars (F� 5.32; df � 9,39; P 0.001), with signiÞcanteffects for year (F� 7.49; df � 1,39; P 0.001) and theyear cultivar interaction (F� 10.65; df � 9,39; P0.001). Only ÔFlavor Crest,Õ ÔSeptember Sun,Õ andÔWhite LadyÕ exhibited a different PGR betweenyears (Fig. 2). However, independent of the year(Fig. 3), the cultivars White Lady, ÔCal Red,Õ ÔJulyRed-N92,Õ ÔDu23,Õ and September Sun exhibited sim-ilar high PGRs, while ÔAugust RedÕ and ÔSummerFree-N18� cultivars exhibited similar low PGRs(Fig. 3).

Fig. 1. Aphid occurrence on commercial cultivars of P. persicae in central Chile (OÕHiggins Region) during thespringÐsummer season of 2008Ð2009. Bars indicate the 95% CI. Different letters above bars represent signiÞcant differences(P 0.05) among cultivar based on multiple comparison test after KruskalÐWallis.

Fig. 2. Population growth rate (PGR, mean � SE) of the aphidM. persicae on 10 P. persica cultivars as measured in Þeldassays for two consecutives years. Asterisks indicate signiÞcant difference (P 0.05) between years within cultivar basedon Tukey multiple comparison test after ANOVA for repeated measures.


No-Choice Test. After 24 h, there were signiÞcantdifferences among cultivars in the number of aphidsoff of the leaves (GLM, Poisson: Wald �2 � 35.4; df �14; P� 0.001; Fig. 4). ÔJuly Red-NS92� had the highestnumber of aphids off of the leaves, although ÔArticSnow,Õ ÔSummer Bright,Õ ÔSweet September,Õ and ÔAu-gust PearlÕ had also higher values of rejection. FlavorCrest and Summer Free-N18 had the lowest numberof aphids off of their leaves (Fig. 4). All other cultivarsexhibited values between these contrasting cultivars.

Aphid Probing Behavior. Among the parametersrelated to prephloem factors, MANOVA showed sig-niÞcant differences among cultivars (Wilks lambda �0.2980;F� 1.906; df � 60;P 0.001), with the durationof the nonprobe period before the Þrst phloem phase(E) and mean duration of pd showing signiÞcant dif-ferences among cultivars (Table 2). The duration ofthe nonprobe period before the Þrst E exhibited thelowest value in ÔElegant LadyÕ and the highest value inAugust Red, whereas the mean duration of pd exhib-

Fig. 3. Population growth rate (PGR, mean � SE) of the aphidM. persicae on 10 P. persica cultivars as measured in Þeldassays. PGR values in each cultivars included both years (main effect of cultivars on PGR). Asterisks indicate signiÞcantdifference (P 0.05) between years within cultivar based on Tukey multiple comparison test after ANOVA for repeatedmeasures.

Fig. 4. Number of aphids (mean � SE) of M. persicae off of the leaves of P. persica cultivars after 24 h of no choicelaboratory experiments.


ited the lowest values in August Red and Arctic Snowand the highest values in White Lady and ElegantLady (Table 2). Following the analysis of the param-eters with a nonparametric univariate test, the totalduration of F (H � 35.52; P � 0.0001) and meanduration of F (H � 34.64; P � 0.0001) showed differ-ences among cultivars. These two parameters are as-sociated with stylet difÞculties during penetration atthe epidermis/mesophyll level; both were similarlylower in the July Red-NS92, Elegant Lady, and WhiteLady cultivars, while August Red exhibited the highestvalues (Table 2). Both parameters also correlated sig-niÞcantly with each other (r � 0.99; P 0.05). How-ever, the mean duration of subphases II-2 of pd (H �33.73;P� 0.0002) and mean duration of subphases II-3of pd (H � 26.87; P � 0.0027) were also signiÞcantlydifferent among cultivars (Table 2), with the meanduration of subphase II-2 of pd showing the lowestvalues in August Red, Summer Bright, and July Red-NS92 and the highest values in Elegant Lady. Themean duration of subphase II-3 of pd showed thelowest value in Arctic Snow and the highest values inElegant Lady and White Lady. In addition, the meanduration of subphase II-2 correlated with the meanduration of subphase II-3 (r � 0.61; P 0.05). Theresults for the duration of subphases II-1, II-2, and II-3of pds in all cultivars are shown in Fig. 5.

All parameters related to phloem factors were an-alyzed using a nonparametric univariate test, resultingin values for the number of E1 (H� 24.63; P� 0.006),duration of Þrst E (H � 21.31; P � 0.0191), and totalduration of E1 (H� 22.90; P� 0.01), with signiÞcantdifferences among cultivars (Table 2). The number ofE1 showed the lowest value in August Red and thehighest values in Elegant Lady and White lady. Theduration of the Þrst E exhibited the longest time in CalRed, while July Red-NS92 was the shortest (Table 2).The total duration of E1 showed the lowest values in

August Red and the highest values in Elegant Lady.Correlations were found between the following pa-rameters: the number of E1 with duration of Þrst E(r � 0.85; P 0.05), the number of E1 with totalduration of E1 (r � 0.74; P 0.05), and the durationof Þrst E with total duration of E1 (r� 0.98; P 0.05).It is worth noting that M. persicae did not exhibitphloem ingestion (E2) in July Red-NS92, Arctic Snow,and September Sun during the recording phase.

For the parameters related to all tissue factors,MANOVA showed signiÞcant differences among cul-tivars (Wilks lambda � 0.214; F � 1.53; df � 90; P 0.003; Table 2). Among these parameters, total dura-tion of pd showed the highest values in White Ladyand Elegant Lady and the lowest value in Arctic Snow.Time from the beginning of the Þrst probe to Þrst pdexhibited the highest value in Flavor Crest and thelowest value in Cal Red (Table 2). Following analysisof the parameters using a nonparametric univariatetest, the total duration of the nonphloematic phase(H� 22.83; P� 0.0114), time from start of EPG to ÞrstE2 (H � 17.12; P � 0.0716), time from Þrst probe toÞrst E2 (H � 16.94; P � 0.0756), time from the be-ginning of the probe reaching to Þrst E2 (H � 15.50;P � 0.1148) and average duration of pd during thethird hour (H� 35.7; P� 0.0001) exhibited signiÞcantdifferences among cultivars (Table 2). Total durationof the nonphloematic phase showed the highest valuein Summer Bright, while the lowest value was found inAugust Red. Time from start of EPG to the Þrst E2,time from the Þrst probe to the Þrst E2 and time fromthe beginning of the probe reaching the Þrst E2 ex-hibited the highest value in Artic Snow and the lowestvalue in Elegant Lady. In addition, average duration ofpd during the third hour showed the longest value inthe cultivars White Lady and the shortest values inAugust Red and July Red-NS92. A signiÞcant corre-lation was found for time from the beginning of the

Fig. 5. Duration of subphases within phase II (mean � 95% CI) of stylet intracellular punctures performed byM. persicaerecorded on P. persica cultivars. Cultivars are ordered in decreasing order relative to total duration of pds.


Þrst probe to the Þrst pd and time from the beginningof Þrst probe to the Þrst E2 (r � 0.23; P 0.05).Similarly, time from the start of EPG to the Þrst E2 andtime from the beginning of Þrst probe to the Þrst E2correlated signiÞcantly (r� 0.81; P 0.05). The meanduration of subphase II-1 was the only EPG parameterthat correlated signiÞcantly with PGR (r � 0.32; P 0.001).

The PCA analysis with varimax normalized rotation,including 16 EPG parameters and 11 cultivars, showedfour principal components with 35.6, 21.9, 16.3, and11.5% explained variance and a cumulative variance of85.3% (eigenvalues �1). The PC1 and PC2 compo-nents of scores and loading (Table 3; Fig. 6A,B)showed that the Elegant Lady cultivar was mostlyassociated with a longer total duration of E1 and ahigher number of E1 (high score on PC1). In addition,August Red was associated with a longer total durationand mean duration of F and duration of Þrst E (highscore on PC2). However, July Red-NS92, Arctic Snow,and September Sun were associated with a longer timefrom the beginning of the Þrst probe, longer probeperiods before the Þrst E and a longer time from thestart of EPG to Þrst E2 (high scores on PC1).

Discussion

By estimating its occurrence in peach and nectarineorchards, measuring PGR, monitoring leaf rejection(no-choice test), and monitoring probing behavior inlaboratory assays, we determined an integrated assess-ment of variation in resistance to the aphidM. persicaeamong a set of commercial cultivars of P. persica.Considering the evidence, the resistance or suscepti-bility status of a given peach or nectarine cultivardepends on the data type. Nevertheless, taken to-gether, some cultivars exhibited distinct resistance toM. persicae.

Aphid occurrence in the orchards yielded impor-tant insight into susceptibility rather than resistance.Here, August Red and Summer Bright showed the

highest values of aphid occurrence (Fig. 1), althoughmost of the cultivars exhibited a low occurrence. How-ever, aphid occurrence in the orchards may mask thegenetic variation in resistance to aphids because theorchards studied were under conventional pest man-agement. To determine the status of resistance of eachcultivar, it is useful to evaluate the results from dif-ferent manipulative experiments at the performance,no-choice or probing behavior level. For instance, thecultivar Summer Bright exhibited the highest occur-rence of aphids in the orchards, that is, the highestsusceptibility to aphids. However, a no-choice testshowed an intermediate resistance (Fig. 4) for Sum-mer Bright, while probing behavior assays revealedmoderate susceptibility (Table 2) for this cultivar.Nevertheless, some cultivars exhibited a similar ten-dency both in aphid occurrence in the orchards and inmanipulative experiments. For example, the cultivarElegant Lady exhibited a low aphid occurrence with2.3% of infested buds (Fig. 1), while it ranked as thelowest cultivar in PGR of M. persicae. The no-choiceexperiment showed an intermediate resistance for El-egant Lady (Fig. 4), and EPG data were characterizedby a higher frequency and longer duration of saliva-tion into the sieve elements (waveform E1). Thus,Elegant Lady displays signatures of resistance acrossmost of the studies performed. However, this was notthe case for all cultivars.

An overview of the evidence obtained using themanipulative experiments (performance, no-choice,and EPG) may facilitate the discovery of the mostresistant cultivars. Regarding the performance varia-tion experiments (PGR), two tendencies were appar-ent among cultivars (Fig. 3): White Lady and Cal Redexhibited susceptibility to aphids, while Elegant Ladywas the most resistant to aphids. Because these resultsreßect 7 d of reproduction, such resistance is mostlikely the resultof anantibioticeffect.Theresults fromthe no-choice assay showed a completely differenttrend, with only 20% of aphids rejecting the leavesafter 24 h, which is an indicator of high susceptibility.

Table 3. Factor loadings of the principal components (PC) with varimax normalized based on correlations

EPG parameters PC1 PC2 PC3 PC4

Total duration of F 0.009711 �0.872807 �0.227850 0.174460Duration of nonprobe period before the Þrst E �0.577323 �0.072027 �0.323378 0.494832Mean duration of pd 0.462663 0.504917 0.702332 �0.064875Mean duration of subphases II-2 of pd 0.586910 0.343965 0.484661 �0.361936Mean duration of subphases II-3 of pd 0.457490 0.511040 0.641210 0.159219Mean duration of F �0.089415 �0.920257 �0.248917 0.139960Number of E1 0.765640 0.534075 0.106521 0.105667Duration of Þrst E �0.312332 �0.849457 0.278503 �0.000183Total duration of E1 0.911786 0.127910 0.132964 �0.217121Total duration of pd 0.104961 0.036549 0.683951 �0.037987Time from the beginning of the Þrst probe to Þrst pd �0.174160 0.263109 �0.625230 0.610817Total duration of no phloematic phase 0.161332 0.248573 �0.057717 �0.886570Time from start of EPG to Þrst E2 �0.962316 �0.063160 �0.136158 0.118176Time from Þrst probe to Þrst E2 �0.959549 �0.080112 �0.166855 0.095755Time from the beginning of the probe reaching the

Þrst E2 to that E2 (min)�0.927830 �0.073887 �0.211031 0.126852

Average duration of pd during third hour 0.549277 0.292054 0.429770 �0.348065Proportion 0.356316 0.219060 0.162625 0.114667

Bold no. shows the principal contribution parameters.


However, in these experiments, the aphidÕs rejectionof the July Red-NS92 cultivar was higher, suggesting astrong antixenotic effect.

For the EPG results, varying resistance or suscep-tibility statuses were deÞned according to the plantfactor involved (Table 2). Because EPG parameterscan be useful in identifying the tissues containingputative resistance factors (Tjallingii 1995), a detailedanalysis of the EPG results may help elucidate theantibiotic and antixenotic components of the resis-tance mechanisms. Because EPG data are used toproduce many different nonindependent parameters,which are associated with different resistant factors, aglobal multivariate view may help reduce this com-plexity. The results from the PCA analysis (Fig. 6A,B)suggest that Elegant Lady is a resistant cultivar that isassociated with the variables correlated with frequent

and longer salivation into the sieve elements (E1),which is an indication of phloematic factor acting onresistance. August Red exhibited resistance associatedwith the presence of the styletÕs penetration difÞcul-ties (F) and a longer duration of the Þrst phloemphase, indicating both the presence of prephloematicand phloematic factors. Finally, July Red-NS92showed resistance associated with a lack of phloemingestion (E2) and all tissues parameters, indicatingthe presence of prephloematic factors.

EPG allowed a detailed view of the pattern of cellpunctures within plant tissues (Tjallingii et al. 2010),which may aid in discerning factors involved in resis-tance. Using this information, the mean duration of thesubphases of pds were analyzed. August Red, whichwas found to possess prephloematic resistance,showed a short duration of pds (Table 2; Fig. 5),

Fig. 6. Principal components analysis with varimax normalized rotation for the EPG study ofM.persicaeprobing on severalP. persica cultivars. Panels shows two principal components (PC1 vs. PC2) for (A) scores of cultivars and (B) loading forparameters. EPG parameters are numbered as described in Table 2.


particularly in subphase II-2. It is interesting to notethat M. persicae showed the second lowest perfor-mance in August Red. A short pds may be associatedwith the presence of intracellular metabolites thatinduce the rapid withdrawal of stylets (Powell et al.2006). The role of subphase II-2 is unknown (Tjallingiiet al. 2010). No further conclusion could be drawnfrom this detailed view for the Elegant Lady and JulyRed-NS92 cultivars.

ElegantLadyexhibited resistancemostlybecauseofphloematic factors. It is particularly interesting to notethat in this cultivar, salivation after sieve elementpuncture (E1) correlated negatively with PGR, whichhas been found to occur more frequently in aphid-resistant plants (Klingler et al. 1998, Ramõrez and Ni-emeyer 1999, Tjallingii 2006). A higher number andduration of E1 were also found in other peach culti-vars, such as the wild peach P. davidiana, which ishighly resistant to aphids (Sauge et al. 1998a). How-ever, July Red-NS92, in addition to the lack of phloemingestion and longer time to commit salivation into thesieve element, exhibited strong prephloematic resis-tance, as shown by no-choice assays. However, theperformance experiment showed a positive PGR inthis cultivar, suggesting that despite an initial antix-enotic effect, aphids are likely able to develop inducedsusceptibility under such experimental conditions, asshown in other aphid-plant systems (Karban and Bald-win 1997, Prado and Tjallingii 1997, Gonzales et al.2002).

It is worth noting that the lack of congruence be-tween performance and EPG experiments may bebecause of the large difference in the time windowsinvolved between both assays. However, the studiesperformed allowed the identiÞcation of the putativeorigins of the resistance. Other studies addressing theM. persicae-P. persica interaction have also identiÞedcultivars with contrasting susceptibility or resistancestatuses based on different experiments. A low resis-tance for the peach cultivar ÔGF305,Õ minor resistancefor the ÔSummergrandÕ and Malo Konare cultivars, andmoderate resistance for the Rubira and WeepingFlower Peach cultivars to M. persicae were found(Sauge et al. 1998a,b; Sauge 1998). In addition, acces-sions of the wild species P. davidianawere found to behighly resistant to M. persicae. In these cultivars, re-sistance appears to be based on antibiosis (MaloKonare and P. davidiana) and antixenosis (Rubira andWeeping Flower Peach). The genetic basis of thisresponse has previously been identiÞed (Monet andMassonie 1994, Lambert and Pascal 2011). The com-mercial cultivars studied herein are very likely to pos-sess the same genetic basis; however, additional stud-ies are necessary to determine the presence of such agenetic basis.

Peaches and nectarines did not exhibit a major dif-ference in their resistance to aphids. Nevertheless, thismay not be the case when aphids attack directly onfruits. Nectarine fruits are glabrous and are apparentlymore attacked by aphids than peaches (data notshown). However, a slightly higher resistance wasfound in nectarines because more cultivars of this

variety showed low performance and leaf-rejectionsin no-choice testing. It should be noted that this studyonly assessed constitutive resistance, although in-duced resistance has been shown to occur on differentcultivars of P. persicae and related species (Sauge et al.2006). Further studies should attempt to identify in-duced responses to the attacks ofM. persicae on thesecultivars, which would aid in understanding the re-sistance of P. persica varieties and cultivars to the M.persicae attacks and aid future breeding programs toimprove these cultivarsÕ resistance to pests and dis-eases.

Acknowledgments

Theauthors aregrateful to “Don” GustavoFernandez fromAgricola JHM and Freddy Ascencio for their valuable help inthe Þeld. This research was supported by Fondecyt Grant1100746 awarded to C.R. and by a Ph.D. Grant from theFacultad de Ciencias Agrarias of the Universidad de Talcaawarded to J.V.

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Received 9 March 2012; accepted 19 July 2012.


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