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(Hemiptera: Aphididae) in Red Raspberry View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by ScholarsArchive@OSU PLANT RESISTANCE Location of the Mechanism of Resistance to Amphorophora agathonica (Hemiptera: Aphididae) in Red Raspberry 1 2 3 4 D. M. LIGHTLE, M. DOSSETT, E. A. BACKUS, AND J. C. LEE J. Econ. Entomol. 105(4): 1465Ð1470 (2012); DOI: http://dx.doi.org/10.1603/EC11405 ABSTRACT The aphid Amphorophora agathonica Hottes (Hemiptera: Aphididae) is an important virus vector in red (Rubus idaeus L.) and black (Rubus occidentalis L.) raspberries in North America. Raspberry resistance to A. agathonica in the form of a single dominant gene named Ag1 has been relied upon to help control aphid-transmitted plant viruses; however, the mechanism of resistance to the insect is poorly understood. Aphid feeding was monitored using an electrical penetration graph on the resistant red raspberry ÔTulameenÕ and compared with a susceptible control, ÔVintageÕ. There were no differences in pathway feeding behaviors of aphids as they moved toward the phloem. Once in the phloem, however, aphids feeding on resistant plants spent signiÞcantly more time salivating than on susceptible plants, and ingested signiÞcantly less phloem sap. This suggests that a mechanism for resistance to A. agathonica is located in the phloem. Reduced ingestion of phloem may result in inefÞcient acquisition of viruses and is a likely explanation for the lack of aphid-transmitted viruses in plantings of resistant cultivars. KEY WORDS electrical penetration graph, plant resistance, feeding behavior, antixenosis Aphid-transmitted viruses are an important problem (Hemiptera: Aphididae) in Europe (Isaacs and Trefor for red (Rubus idaeus L.) and black (Rubus occiden- Woodford 2007). Resistance to A. agathonica is con- talis L.) raspberry production in North America. Vi- ferred by the Ag1 gene, which was originally found in ruses such as Raspberry leaf mottle virus (family Clos- ÔLloyd GeorgeÕ and has since been used widely in teroviridae, genus Closterovirus, RLMV), Raspberry breeding (Daubeny 1966). Ag1, a single dominant latent virus (family Reoviridae, genus Reovirus, gene, has been effective for Ͼ50 yr, and resistance has RpLV), and Rubus yellow net (family Caulimoviridae, not been overcome by the most common biotype of A. genus Badnavirus, RYNV) in red raspberry and Black agathonica, although an Ag1-breaking biotype of A. raspberry necrosis virus (family Secoviridae, genus un- agathonica has been reported in British Columbia assigned Secoviridae species, BRNV) in black rasp- (Daubeny and Anderson 1993). Despite reliance upon berry, cause a decline in cane health and fruit quality, this gene, the mechanism of resistance is not entirely resulting in a shortened life of the infected planting- understood. s(Halgren et al. 2007, Tzanetakis et al. 2007, Quito- Kennedy and Schaefers (1974b) presented evi- Avila et al. 2011). In North America, the most impor- dence that Ag1 plants were resistant through antix- tant vector of these viruses is the large raspberry enosis, or aphid nonpreference for the host, which led aphid, Amphorophora agathonica Hottes (Hemiptera: to host rejection and eventual aphid death. In choice Aphididae). A. agathonica is distributed throughout trials, aphid colonies became established only on sus- the United States and Canada and colonizes only Ru- ceptible cultivars, whereas in no-choice trials, aphids bus species (Blackman and Eastop 2000). experienced decreased survival and high desertion Host plant resistance has long been recognized as an rates on resistant cultivars compared with susceptible effective method for reducing virus spread (van Em- cultivars (Kennedy and Schaefers 1974b). However, den 2007). Indeed, this practice has played a major phloem contact was not entirely avoided because his- role in reducing the spread of viruses in resistant red tological studies of stylet sheath pathways showed that raspberry by A. agathonica in North America and by aphids on resistant plants reached the phloem sieve the closely related Amphorophora idaei Bo¨rner elements (Kennedy 1974). Furthermore, Kennedy and Schaefers (1975) showed that the ingestate from resistant plants was more dilute than on susceptible 1 Corresponding author: Oregon State University, 4017 Ag & Life Sciences Bldg., Corvallis, OR 97330 (e-mail: [email protected]). plants based on honeydew and whole-body homoge- 2 PaciÞc Agri-Food Research Centre, Agriculture and Agri-Food nate analysis. They hypothesized that in addition to Canada, 6947 #7 Hgwy., Agassiz, BC, Canada V0M 1A0. antixenotic mechanism, there was a nutritional role to 3 USDAÐARS, Crop Diseases, Pests and Genetics Research Unit, the resistance against A. agathonica. Yet, questions 9611 Riverbend Ave., Parlier, CA 93619. 4 USDAÐARS, Horticultural Crops Research Unit, 3450 SW Campus about the resistance mechanism of Ag1 remain. It is Way, Corvallis, OR 97331. unlikely that a substantial nutritional deÞcit exists in 1466 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 105, no. 4 Ag1 raspberries because several other aphid species, tested to verify that they were resistant to the aphid including Aphis rubicola Oestlund (Hemiptera: Aphi- clones used in this study. Two Tulameen plants were didae) and the closely related A. idaei, will readily feed placed in one mesh aluminum cage (35.5 by 35.5 by on Ag1 plants without an impact on survival or ability 35.5 cm) and two Vintage plants were placed in a to colonize these plants (Kennedy et al. 1973, Ken- second cage. Twenty adults and 20 nymphs were nedy and Schaefers 1975). evenly distributed in each cage. The plants and aphids Insight on potential mechanisms of resistance can were maintained in this insect cage in a greenhouse at be obtained by studying the feeding behaviors of a photoperiod of 16:8 (L:D) h and 21ЊC daytime and aphids on resistant and susceptible plants. The elec- 15.5ЊC nighttime temperatures. After 2 wk, the aphid trical penetration graph (EPG) technique has been populations in each cage were counted. This proce- invaluable in measuring the feeding behavior of aphids dure was replicated three times. and other hemipterans (Walker 2000). In EPG, the Aphid Settling Behavior. To test whether resistant insect is wired into an electrical circuit with a host plants may affect aphid settling behaviors or tendency plant. The insectÕs stylets then act as a switch, com- of an aphid to immediately leave the plant (Pelletier pleting the circuit when the stylets are inserted into and Giguere 2009), aphids were observed for differ- the plant. Changes in output voltage over time, known ences in behavior on Tulameen or Vintage leaves. as waveforms, represent different activities, such as Adult aphids were starved in a petri dish for1htobe phloem salivation or ingestion, within the plant. The consistent with the 1-h handling time aphids under- objective of this study was to compare the feeding went in the electronic monitoring protocol (see be- behavior of A. agathonica on resistant and susceptible low), then placed individually on a trifoliate leaf cut- hosts using EPG to determine which plant tissues were ting from a resistant or susceptible plant. Leaf cuttings most important for resistance. were obtained by excising the leaf with a razor blade and immediately submerging the petiole in water, which reduces the likelihood that the resistance prop- Materials and Methods erties are lost (Kennedy and Schaefers 1974a). The Plants and Insects. The raspberry cultivars selected aphidsÕ position (on top of or under leaf, on stem, for this study were the resistant ÔTulameenÕ and sus- desertion of plant) and activity (walking, settled) was ceptible ÔVintage,Õ a new release from the USDA Hor- recorded every 5 min for 1 h. Observations on aphids ticultural Crops Research Unit and Oregon State Uni- in each treatment were replicated 15 times. versity cooperative breeding program. Tulameen was Electronic Monitoring. The EPG system used for selected for aphid resistance conferred by gene Ag1 this study was the AC-DC EPG developed by Backus (Daubeny and Anderson 1991, Daubeny and Kempler and Bennett (2009). Before the beginning of moni- 2003). Vintage and Tulameen plants were obtained as toring, adult aphids were starved for 1 h, during which hardened-off tissue culture plugs from Sakuma Broth- time the aphids were immobilized and attached to the ers (Burlington, WA). Randomly sampled individuals insect electrode via a 1Ð2-cm long, 25.4-␮m-diameter of each cultivar tested negative for the presence of all gold wire using silver conductive glue (1 part school known aphid-transmitted raspberry viruses. Plugs glue:1 part water:1 part silver ßake by weight). A were grown individually in 10-cm pots (Dura-Pot, second copper electrode was inserted into the soil at Lake Oswego, OR) of Sunshine Professional Growing the base of the plant. Direct current (DC) signal (40 Mix (Sun Gro Horticulture, Bellevue, WA) amended mV) was applied to the plant and data were collected with 8 g/gal of 21Ð2Ð11 NÐPÐK fertilizer (Apex, Boise, using a giga-Ohm (109) input resistor. The data sample ID). The plants were grown in a greenhouse at a rate was 100 Hz. EPG recordings were acquired using photoperiod of 16:8 (L:D) h and 21ЊC daytime and a DI-710 and Windaq Acquisition Software (Dataq 15.5ЊC nighttime temperatures, and used when they Instruments Inc., Akron, OH). were Ϸ30 cm tall. Recordings began every evening at 1800 hours and Six apterous parthenogenic female A. agathonica lasted for 12 h. Recordings were conducted overnight were collected from commercial red raspberry Þelds to reduce interference resulting from laboratory ac- in Whatcom Co., WA, in July 2010 and offspring from tivities during the daytime. The plants and aphids were these females were combined into a single colony. set up in the laboratory in a metal Faraday cage to This aphid colony was maintained in a Percival growth reduce extraneous electrical noise. The temperature chamber at 18 Ϯ 2ЊC under ßuorescent growth lights ranged from 20 to 24ЊC, and ambient light was pro- at a photoperiod of 16:8 (L:D) h.
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