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Detection and Variability of Aster Yellows Phytoplasma Titer in Its Insect Vector, Macrosteles Quadrilineatus (Hemiptera: Cicadellidae)

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Detection and Variability of Aster Yellows Phytoplasma Titer in Its Insect Vector, Macrosteles Quadrilineatus (Hemiptera: Cicadellidae) ARTHROPODS IN RELATION TO PLANT DISEASE Detection and Variability of Aster Yellows Phytoplasma Titer in Its Insect Vector, Macrosteles quadrilineatus (Hemiptera: Cicadellidae) 1 2 3 K. E. FROST, D. K. WILLIS, AND R. L. GROVES J. Econ. Entomol. 104(6): 1800Ð1815 (2011); DOI: http://dx.doi.org/10.1603/EC11183 ABSTRACT The aster yellows phytoplasma (AYp) is transmitted by the aster leafhopper, Mac- rosteles quadrilineatus Forbes, in a persistent and propagative manner. To study AYp replication and examine the variability of AYp titer in individual aster leafhoppers, we developed a quantitative real-time polymerase chain reaction assay to measure AYp concentration in insect DNA extracts. Absolute quantiÞcation of AYp DNA was achieved by comparing the ampliÞcation of unknown amounts of an AYp target gene sequence, elongation factor TU (tuf), from whole insect DNA extractions, to the ampliÞcation of a dilution series containing known quantities of the tuf gene sequence cloned into a plasmid. The capabilities and limitations of this method were assessed by conducting time course experiments that varied the incubation time of AYp in the aster leafhopper from 0 to 9 d after a 48 h acquisition access period on an AYp-infected plant. Average AYp titer was Ϯ measured in 107 aster leafhoppers and, expressed as Log10 (copies/insect), ranged from 3.53 ( 0.07) to 6.26 (Ϯ0.11) occurring at one and 7 d after the acquisition access period. AYp titers per insect and relative to an aster leafhopper chromosomal reference gene, cp6 wingless (cp6), increased Ϸ100-fold in insects that acquired the AYp. High quantiÞcation cycle values obtained for aster leafhoppers not exposed to an AYp-infected plant were interpreted as background and used to deÞne a limit of detection for the quantitative real-time polymerase chain reaction assay. This method will improve our ability to study biological factors governing AYp replication in the aster leafhopper and determine if AYp titer is associated with frequency of transmission. KEY WORDS aster leafhopper, aster yellows, aster yellows phytoplasma, Macrosteles quadrilineatus, qPCR Aster yellows (AY) is a widespread disease of plants For root vegetables, processing problems can result caused by the aster yellows phytoplasma (AYp), a from an inability to obtain clean raw product because small, wall-less prokaryotic organism that is currently of adventitious root growth and associated Þeld soil placed in the provisional genus Candidatus (Lee et al. contamination. 2000, IRPCM Phytoplasma/Spiroplasma working te- Although, more than 24 leafhopper species are amÐPhytoplasma taxonomy group 2004). The AYp has known to acquire and transmit AYp organisms (Mahr an extensive and diverse host range infecting over 350 1989, Christensen et al. 2005), the aster leafhopper, plant species including many common vegetable, or- Macrosteles quadrilineatus Forbes, is considered to be namental, and agronomically important Þeld crops, the primary vector of the AYp because of its preva- and several noncrop plant species (Kunkel 1926; Chi- lence in Midwestern susceptible crops (Drake and ykowski 1965, 1967; Chiykowski and Chapman 1965; Chapman 1965, Hoy et al. 1992). The aster leafhopper Westdal and Richardson 1969; Peterson 1973; Lee et al. is a polyphagous insect species that uses over 300 1998, 2000, 2003; Hollingsworth et al. 2008). The most different plant species for food, oviposition, and shel- common disease phenotypes are vein clearing, chlo- ter and many of these are susceptible to AYp infection, rosis, stunting, twisting and proliferation of plant (Wallis 1962, Peterson 1973). Aster leafhopper host stems, and the development of adventitious roots plant species can be classiÞed into two primary groups (Kunkle 1926, Bloomquist 2002). In vegetable crops, based on utilization patterns to include: 1) feeding these symptoms can lead to yield and quality losses. hosts or 2) feeding and reproductive hosts. Other factors such as plant community composition (Lee and Robinson 1958, Wallis 1962, Schultz 1979), plant 1 Department of Plant Pathology, University of Wisconsin-Madison, 1630 Linden Drive, Madison, WI 53706. physiological state (Peterson 1973) and seasonal or 2 Department of Plant Pathology and U.S. Department of Agricul- geographic location (Lee and Robinson 1958, Wallis ture, Agricultural Research Service, Vegetable Crops Research Unit, 1962, Peterson 1973) can also affect host preferences Russell Laboratories, University of Wisconsin, Madison, WI 53706. of aster leafhopper in the Þeld. In Wisconsin, culti- 3 Corresponding author: Department of Entomology, University of Wisconsin-Madison, 1630 Linden Drive, Madison, WI 53706 (e-mail: vated grains are hosts for overwintering eggs and also [email protected]). serve as early feeding and reproductive hosts for the December 2011 FROST ET AL.: DETECTION AND VARIABILITY OF ASTER YELLOWS 1801 aster leafhopper (Drake and Chapman 1965). In ad- quantify the titer of phytoplasma organisms in their dition to grain crops, the aster leafhopper feeds and is insect host. moderately abundant in mixed broadleaf weeds and Recent research in pathogen-vector interactions grasses that border crop Þelds (Shultz 1979). suggests that the titer of circulative, propagative AYp has been reported to be circulative and prop- pathogens in their insect vectors may inßuence the agative in the aster leafhopper (Maramorosch 1952, likelihood of successful transmission events to a sus- Sinha and Chiykowski 1967, Lee et al. 2000); vector ceptible host plant. For example, Rotenberg et al. competence involves acquisition, pathogen replica- (2009) demonstrated that single thrips (Frankliniella tion, and circulation to result in successful transmis- occidentalis) containing higher titers of Tomato spot- sion to a susceptible host (Matthews 1991). Using ted wilt virus (TSWV) transmitted the virus more indirect methods (see below) and histological studies frequently to susceptible plants. Only a few studies of other fastidious prokaryotic organisms, a model has have reported phytoplasma titer of an insect and its been developed for acquisition and transmission of relationship to transmission success (Bosco et al. AYp. Brießy, the aster leafhopper acquires AYp by 2007a, Galetto et al. 2009). Additionally, the relation- feeding on vascular tissues of infected plants for ex- ship between AYp titer and frequency of transmission tended periods of time (hours to days) (Murral et al. has not been examined for individual aster leafhopper. 1996). The phytoplasma moves from the mouthparts To better understand AYp replication in the aster through the alimentary canal to the lumen of the leafhopper, our objectives were 1) to develop a quan- midgut (Sinha and Chiykowski 1967, Fletcher et al. titative assay to measure AYp titer in individual leaf- 1998). Once in the midgut lumen, the organism moves hoppers, 2) to examine the variability of AYp titer in through the epithelium (Fletcher et al. 1998, Kwon et aster leafhoppers, and 3) to use the assay to charac- al. 1999), circulates in the insect body and replicates terize the temporal dynamics of AYp titer among a in the hemolymph and other insect tissues (Maram- population of AYp-infected insects. orosch 1952a, Sinha and Chiykowski 1967, Fletcher et al. 1998). Ultimately, AYp infects the accessory sali- Materials and Methods vary glands where it replicates, moves into the salivary ducts and is introduced into plant hosts with insect Aster Leafhopper Colony. An aster leafhopper col- ony was established from adult aster leafhopper pop- saliva during the egestion phase of feeding (Fletcher ulations collected in wheat (Triticum spp.) Þelds in et al. 1998, Kwon et al. 1999). These events occur central Missouri (April 2009) and southern Wisconsin during a two to three week latency period or the (MayÐJune 2009). Adult leafhoppers were initially period after acquisition during which the insect can- maintained on oat (Avena sativa L.) seedlings in a not transmit the pathogen. Once infectious, the leaf- controlled environment with a 16:8 (L:D) photope- hopper may transmit AYp to healthy plants during riod (24ЊC light; 19ЊC dark). To ensure a phytoplasma- relatively short inoculation feeding periods and re- free colony of leafhoppers, the Þeld caught adult fe- mains infectious for the remainder of its adult life male leafhoppers were initially placed on oat seedlings (Maramorosch 1953b). Although transovarial trans- and allowed a 36 h oviposition period after which time mission of AYp is not thought to occur, there is mount- all adult leafhoppers were removed. First instar ing evidence that transovarial transmission of phyto- nymphs resulting from those eggs were subsequently plasmas does occur for some insect-pathogen moved onto new oat seedlings not previously visited combinations (Alma et al. 1997, Kawakita et al. 2000). by aster leafhoppers. Additionally, leafhoppers were Because AYp organisms have an obligatory associ- periodically checked for phytoplasma or AYp infec- ation with their plant and insect hosts and have not tion by PCR, using primers P1 and 16sSr (Lee et al. been successfully cultured in the laboratory, much of 2006) or F4 and R1 (Davis and Lee, 1993; reaction what is known about phytoplasma replication in the conditions described below). All oat plants were insect has been derived using indirect methods of grown in a glasshouse and plants were established by measurement. For example, replication of AYp organ- sowing oat seed into 10 cm square pots containing isms
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