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Infection of Potato Plants with Potato Leafroll Virus Changes Attraction and Feeding Behaviour of Myzus Persicae A

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Infection of Potato Plants with Potato Leafroll Virus Changes Attraction and Feeding Behaviour of Myzus Persicae A DOI: 10.1111/j.1570-7458.2007.00607.x Blackwell Publishing Ltd Infection of potato plants with potato leafroll virus changes attraction and feeding behaviour of Myzus persicae A. E. Alvarez1,2, E. Garzo1,3, M. Verbeek2, B. Vosman2, M. Dicke1 & W. F. Tjallingii1* 1Wageningen University, Laboratory of Entomology, P.O. Box 8031, 6700 EH Wageningen, The Netherlands, 2Plant Research International, P.O. Box 16, 6700 AA, Wageningen, The Netherlands, and 3Centro de Ciencias Medioambientales, CSIC, Departamento de Protección Vegetal, Serrano 115 dpdo, 28006 Madrid, Spain Accepted: 29 May 2007 Key words: Solanaceae, Solanum tuberosum, Homoptera, Aphididae, green peach aphid, plant odours, plant viruses, EPG, probing, PLRV Abstract Potato leafroll virus (PLRV; genus Polerovirus, family Luteoviridae) is a persistently transmitted circulative virus that depends on aphids for spreading. The primary vector of PLRV is the aphid Myzus persicae (Sulzer) (Homoptera: Aphididae). Solanum tuberosum L. potato cv. Kardal (Solanaceae) has a certain degree of resistance to M. persicae: young leaves seem to be resistant, whereas senescent leaves are susceptible. In this study, we investigated whether PLRV-infection of potato plants affected aphid behaviour. We found that M. persicae’s ability to differentiate headspace volatiles emitted from PLRV-infected and non-infected potato plants depends on the age of the leaf. In young apical leaves, no difference in aphid attraction was found between PLRV-infected and non-infected leaves. In fact, hardly any aphids were attracted. On the contrary, in mature leaves, headspace volatiles from virus infected leaves attracted the aphids. We also studied the effect of PLRV-infection on probing and feeding behaviour (plant penetration) of M. persicae using the electrical penetration graph technique (DC system). Several differences were observed between plant penetration in PLRV-infected and non-infected plants, but only after infected plants showed visual symptoms of PLRV infection. The effects of PLRV-infection in plants on the behaviour of M. persicae, the vector of the virus, and the implications of these effects on the transmission of the virus are thoroughly discussed. such a way that interactions between host and vector are Introduction influenced. Vector activity and behaviour are important Potato leafroll virus (PLRV) (genus Polerovirus, family determinants of the rate and extent of epidemic virus Luteoviridae) is a persistently transmitted circulative virus development (Jeger et al., 1998, 2004). Changes in the that depends on aphids for dispersal and transmission to attraction between the aphid vector and the infected plant host plants. Potato leafroll virus is restricted to the phloem. and changes in the benefits obtained by the aphid from this Aphids acquire PLRV during ingestion of phloem sap from relationship will certainly influence the probability of virus infected plants and they inoculate it into new plants during dispersal. salivation into the phloem sieve elements. The green peach In some plant–virus–aphid interactions, the presence of aphid, Myzus persicae (Sulzer) (Homoptera: Aphididae), viruses negatively affects the performance of the vector. On is the most efficient vector of PLRV. In this triangular wheat, the presence of barley yellow dwarf virus (BYDV) relationship, direct interactions occur between virus, host, reduces the concentration of total amino acids in the and vector. Moreover, virus infections can change hosts in phloem. BYDV-infection also leads to a less efficient use of phloem sap by the aphid Sitobion avenae (F.) (Fiebig et al., 2004). A. E. Alvarez and E. Garzo contributed equally to this article. *Correspondence: W. F. Tjallingii, Wageningen University, Benefits for the vector that favour the transmission of Laboratory of Entomology, P.O. Box 8031, 6700 EH Wageningen, viruses have been described for various plant–pathogen– The Netherlands. E-mail: [email protected] vector combinations. Belliure et al. (2005) showed that © 2007 The Authors Entomologia Experimentalis et Applicata 125: 135–144, 2007 Journal compilation © 2007 The Netherlands Entomological Society 135 136 Alvarez et al. Frankliniella occidentalis (Pergande) benefits indirectly from EPG waveforms have been correlated with aphid activities the tomato spotted wilt virus, which it transmits, through as well as with tissue locations of the stylet tips (Tjallingii, effects of the virus on host-plant characteristics. They hypo- 1978; Kimmins & Tjallingii, 1986; Tjallingii & Hogen thesized that infection with the virus has a negative effect on Esch, 1993). Strategies for controlling plant viruses depend induced defences against the thrips vector. Aphis gossypii highly on the understanding of the virus–plant–vector Glover transmits zucchini yellow mosaic virus (ZYMV) interactions. The partial plant resistance present in potato to Cucurbita pepo L. and it lives longer and produces more cultivar Kardal slows down aphid population growth on offspring than on non-infected plants (Blua et al., 1994). young plants and, consequently, limits acquisition and In contrast to the negative effects mentioned above (Fiebig dissemination of PLRV. The resistance to aphids in Kardal et al., 2004), BYDV has been reported to benefit its vector is phloem located and occurs in young apical leaves, it S. avenae (F.) by disrupting the development of a braconid declines in mature and senescent leaves (Alvarez et al., parasitoid within the aphid vector (Christiansen-Weniger 2006). Here, we investigated whether infection with PLRV et al., 1998). BYDV-infection of wheat plants increases the changed the host plant to the advantage of the aphid attractiveness to the aphid Rhopalosiphum padi (L.) as a through improving probing and feeding behaviour in result of producing more volatiles than non-infected plants young apical leaves of cv. Kardal. We were especially (Jiménez-Martínez et al., 2004). interested in changes regarding vector attraction. Castle & Berger (1993) found that M. persicae performance Our specific aim was to study (i) the effects of PLRV- improves in terms of growth rate, reproduction, and longevity infection of potato plants on vector attraction by using an on cultivated Solanum tuberosum L. (Solanaceae) plants olfactometer assay for apical and mature leaves, and (ii) the when infected by PLRV (vector-borne virus) as compared impact of PLRV-infection on plant resistance, as expressed to virus-free potato plants, plants infected by potato virus by feeding behaviour, by using the EPG technique. We Y (PVY, stylet-borne virus that can be briefly associated to hypothesized that the better performance of M. persicae aphids but also mechanically transmitted), or potato virus previously found on PLRV-infected potatoes plants was X (PVX, vector-independent mechanically transmitted due to structural or chemical changes in plant tissues that virus). It was also found that more M. persicae individuals enhanced probing and feeding behaviour. settled on PLRV-infected leaves of S. tuberosum L. than on leaves of virus-free, PVY-infected, or PVX-infected leaves Materials and methods (Castle et al., 1998). Eigenbrode et al. (2002) reported that M. persicae preferred PLRV-infected to either non- Plants and aphids infected potato plants, PVY-infected plants, or PVX-infected Virus-free potato plants (S. tuberosum L. cv. Kardal) were plants. They found an increased emission of several volatiles propagated in vitro (Alvarez et al., 2006). After 2 weeks, by PLRV-infected plants when compared to non-infected the rooted plantlets were transferred to soil in a glasshouse plants. These volatiles may act as attractants and arrestants at 22 ± 2 °C, about 70% r.h., and an L16:D8 photoperiod. of M. persicae. Srinivasan et al. (2006) found that the A new colony of M. persicae was established on radish preference of M. persicae for PLRV-infected Solanum Raphanus sativus L. starting with a single virginoparous spp. plants over non-infected plants relies primarily on apterous aphid from a colony maintained at the Laboratory olfactory cues rather than on visual cues. The role of plant of Entomology, Wageningen University, Wageningen, The volatiles in host recognition and settling behaviour by aphids Netherlands. The colony was reared in a climate chamber has been reviewed by Pickett et al. (1992). Vargas et al. at 22 ± 2 °C, 30–40% r.h., and an L16:D8 photoperiod. (2005) have recently shown that alate virginoparae of the tobacco-adapted subspecies Myzus persicae nicotianae Virus infection recognized and chose their host plant more efficiently One week after transfer to soil, nine potato plants were than the generalist Myzus persicae s.s., on the basis of exposed to 15 viruliferous M. persicae nymphs during 96 h olfactory and visual cues and factors present at cuticular (treatment) and nine potato plants were exposed to 15 and subcuticular levels. virus-free nymphs during the same time (control). After In addition to olfactory cues, aphids must insert their 96 h, aphids and nymphs were gently removed with a brush. mouthparts into plant tissues (probing) in order to select Three Physalis floridana Rybd. plants, very susceptible to a suitable host and find the phloem. Therefore, knowledge M. persicae and PLRV, were also exposed to 15 viruliferous of mechanical or biochemical cues in host plants during nymphs during 96 h as a positive control. Viruliferous probing by aphids is crucial. The electrical penetration aphids had been obtained by placing apterous adult aphids
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