Biology, Ecology, and Management of the Potato Psyllid, Bactericera cockerelli (Hemiptera: Triozidae), and Zebra Chip Disease in Potato.

The potato psyllid, Bactericera cockerelli (Sulc) (Hemiptera: Triozidae), transmits the pathogen "Candidatus liberibacter solanacearum" (Lso), the putative causal agent of zebra chip disease (ZC). ZC is a disease of potato that reduces yield and quality and has disrupted integrated pest management programs in parts of the Americas and New Zealand. Advances in our understanding of the ecological factors that influence ZC epidemiology have been accelerated by the relatively recent identification of Lso and motivated by the steady increase in ZC distribution and the potential for devastating economic losses on a global scale. Management of ZC remains heavily reliant upon insecticides, which is not sustainable from the standpoint of insecticide resistance, nontarget effects on natural enemies, and regulations that may limit such tools. This review synthesizes the literature on potato psyllids and ZC, outlining recent progress, identifying knowledge gaps, and proposing avenues for further research on this important pathosystem of potatoes.

A comprehensive review of zebra chip disease in potato and its management through breeding for resistance/tolerance to 'Candidatus Liberibacter solanacearum' and its insect vector.

Zebra chip disease (ZC), associated with the plant pathogenic bacterium 'Candidatus Liberibacter solanacearum' (psyllaurous) (CLso), is a major threat to global potato production. In addition to yield loss, CLso infection causes discoloration in the tubers, rendering them unmarketable. CLso is transmitted by the potato psyllid, Bactericera cockerelli (Sulc) (Hemiptera: Triozidae). ZC is managed by prophylactic insecticide applications to control the vector, which is costly and carries environmental and human health risks. Given the expense, difficulty, and unsustainability of managing vector-borne diseases with insecticides, identifying sources of resistance to CLso and developing varieties that are resistant or tolerant to CLso and/or potato psyllids has become a major goal of breeding efforts. These efforts include field and laboratory evaluations of noncultivated germplasm and cultivars, studies of tubers in cold storage, detailed quantifications of biochemical responses to infection with CLso, possible mechanisms underlying insect resistance, and traditional examination of potato quality following infections. This review provides a brief history of ZC and potato psyllid, a summary of currently available tools to manage ZC, and a comprehensive review of breeding efforts for ZC and potato psyllid management within the greater context of Integrated Pest Management (IPM) strategies. © 2022 Society of Chemical Industry. This article has been contributed to by U.S. Government employees and their work is in the public domain in the USA.

Efficacy of Naturally Occurring and Commercial Entomopathogenic Nematodes Against Sugar Beet Wireworm (Coleoptera: Elateridae).

Wireworms are the larval stage of click beetles (Coleoptera: Elateridae), and some of their species are serious pests of many crops. In the present study, we evaluated the efficacy of naturally occurring and commercial entomopathogenic nematode species against the sugar beet wireworm, Limonius californicus (Mannerheim), in the laboratory. First, efficacies of Steinernema feltiae (Filipjev) (Rhabditida: Steinernematidae) collected from an irrigated (S. feltiae-SSK) and a dryland (S. feltiae-SSC) field and the two commercial entomopathogenic nematode species, S. carpocapsae (Weiser) (Rhabditida: Steinernematidae) and Heterorhabditis bacteriophora Poinar (Rhabditida: Heterorhabditidae), were examined. Efficacies of the two field-collected S. feltiae isolates were also compared against a commercial S. feltiae strain. In the first bioassay, S. feltiae-SSK caused 63.3% wireworm mortality, followed by 30% caused by S. carpocapsae, 23.3% by S. feltiae-SSC, and 6.7% by H.bacteriophora. In the second assay, S. feltiae-SSK killed 56.7% of the wireworms, ≈2.1- and ≈5.7-fold higher than S. feltiae-SSC and the commercial isolate, respectively.

Interspecific interactions within a vector-borne complex are influenced by a co-occurring pathosystem.

Potato virus Y (PVY) and zebra chip (ZC) disease are major threats to solanaceous crop production in North America. PVY can be spread by aphid vectors and through vegetative propagation in potatoes. ZC is associated with "Candidatus Liberibacter solanacearum" (Lso), which is transmitted by the tomato/potato psyllid, Bactericera cockerelli Sulc (Hemiptera: Triozidae). As these two pathosystems may co-occur, we studied whether the presence of one virus strain, PVY°, affected the host preference, oviposition, and egg hatch rate of Lso-free or Lso-carrying psyllids in tomato plants. We also examined whether PVY infection influenced Lso transmission success by psyllids, Lso titer and plant chemistry (amino acids, sugars, and phytohormones). Lso-carrying psyllids showed a preference toward healthy hosts, whereas the Lso-free psyllids preferentially settled on the PVY-infected tomatoes. Oviposition of the Lso-carrying psyllids was lower on PVY-infected than healthy tomatoes, but Lso transmission, titer, and psyllid egg hatch were not significantly affected by PVY. The induction of salicylic acid and its related responses, and not nutritional losses, may explain the reduced attractiveness of the PVY-infected host to the Lso-carrying psyllids. Although our study demonstrated that pre-existing PVY infection can reduce oviposition by the Lso-carrying vector, the preference of the Lso-carrying psyllids to settle on healthy hosts could contribute to Lso spread to healthy plants in the presence of PVY infection in a field.

Mortality of Potato Psyllid (Hemiptera: Triozidae) on Host Clippings Inoculated With Ergot Alkaloids.

Our previous study provided correlative evidence that morning glory species harboring endophytic fungi (Periglandula) are resistant to potato psyllid [Bactericera cockerelli (Sulc)], whereas species free of fungi often allowed psyllid development. In this study, we manipulated levels of ergot alkaloids in host tissues by inoculating clippings from potato plants with extracts from morning glories that harbor Periglandula [Ipomoea leptophylla Torrey, Ipomoea imperati (Vahl) Grisebach, Ipomoea tricolor Cavanilles, Ipomoea pandurata (L.) G. F. Meyer, and Turbina corymbosa (L.)] and one species (Ipomoea alba L.) that does not harbor the endophyte. Ergot alkaloids (clavines, lysergic acid amides, and ergopeptines) were detected in potato clippings, thus confirming that leaves had taken up compounds from solutions of crude extracts. Psyllid mortality rates on inoculated clippings ranged between 53 and 93% in treatments producing biochemically detectable levels of alkaloids, when compared with 15% mortality in water controls or the alkaloid-free I. alba. We then tested synthetic analogs from each of the three alkaloid classes that had been detected in the crude extracts. Each compound was assayed by inoculating clippings of two host species (potato and tomato) at increasing concentrations (0, 1, 10, and 100 µg/ml in solution). Psyllids exhibited a large and significant increase in mortality rate beginning at the lowest two concentrations, indicating that even very small quantities of these chemicals led to mortality. Feeding by nymphs on artificial diets containing synthetic compounds resulted in 100% mortality within 48 h, irrespective of compound. Further testing of ergot alkaloids to characterize the mode of action that leads to psyllid mortality is warranted.

Potato Psyllid (Hemiptera: Triozidae) Behavior on Three Potato Genotypes With Tolerance to 'Candidatus Liberibacter solanacearum'.

The potato/tomato psyllid Bactericera cockerelli (Sulc) transmits 'Candidatus Liberibacter solanacearum' (Lso) (also known as 'Candidatus Liberibacter psyllaurous'), the bacterium associated with zebra chip disease (ZC) in potato. When disease incidence is high, ZC causes large economic losses through reductions in potato yield and tuber quality. No commercial potato variety has been found totally resistant to the pathogen. We evaluated host acceptance behaviors using no-choice assays on three breeding clones derived from Solanum chacoense Bitter with putative tolerance to Lso and/or ZC as part of an effort to determine whether the disease tolerance observed in those breeding clones was related to effects on psyllid settling behavior. We also counted the number of eggs laid and nymphs hatched on the different genotypes to observe any differences in reproduction. The potato variety 'Russet Burbank' was used as a susceptible control. Probing frequency and female walking duration were greater on Russet Burbank than the other genotypes. Oviposition did not differ among genotypes. However, female psyllids on two of the Lso-tolerant genotypes displayed reduced fertility 18-24 d after confinement with a male, relative to females on Russet Burbank. These results suggest that although the germplasms display minor abiotic activity on psyllid fertility, tolerance to Lso may be more strongly linked with plant tolerance to the pathogen rather than effects on host acceptance behaviors.

Effect of the level of "Candidatus Liberibacter solanacearum" infection on the development of zebra chip disease in different potato genotypes at harvest and post storage.

Potato psyllid (Bactericera cockerelli Sulc)-transmitted "Candidatus Liberibacter solanacearum" (Lso) has been negatively impacting the potato industry in the United States as well as other potato-producing countries. Lso has been linked to a condition known as zebra chip (ZC) that affects yield and quality of potato tubers. Efforts to find sources of resistance to ZC have primarily focused on greenhouse evaluations based on a single inoculation time prior to harvest. Plant response to infection, however, could be influenced by the developmental stage of the host plant, and ZC may continue to develop after harvest. The objectives of this study were to quantify Lso inoculation success, Lso titer, ZC severity and Lso development during storage in eight potato genotypes. These evaluations were conducted on plants infested with Lso-positive psyllids at 77, 12, and 4 days before vine removal (DBVR). The evaluated genotypes were categorized according to their relative resistance to Lso and tolerance to ZC symptoms. Lso inoculation success in the genotype family A07781, derived from Solanum chacoense, was lower than that of the susceptible control ('Russet Burbank'). A07781-4LB and A07781-3LB genotypes were characterized relatively resistant to the pathogen and highly tolerant to ZC symptoms, while A07781-10LB was categorized as susceptible to Lso but relatively tolerant to symptom expression. In stored potatoes, increase in Lso concentrations was observed for all infestation times. However, significantly higher Lso titer was detected in tubers infested 12 DBVR and the effect was similar across genotypes. Overall, the A07781 family can be considered as a promising source of resistance or tolerance to ZC.

Survival and development of potato psyllid (Hemiptera: Triozidae) on Convolvulaceae: Effects of a plant-fungus symbiosis (Periglandula).

Plant species in the family Solanaceae are the usual hosts of potato psyllid, Bactericera cockerelli (Sulc) (Hemiptera: Psylloidea: Triozidae). However, the psyllid has also been shown to develop on some species of Convolvulaceae (bindweeds and morning glories). Developmental success on Convolvulaceae is surprising given the rarity of psyllid species worldwide associated with this plant family. We assayed 14 species of Convolvulaceae across four genera (Convolvulus, Calystegia, Ipomoea, Turbina) to identify species that allow development of potato psyllid. Two populations of psyllids were assayed (Texas, Washington). The Texas population overlaps extensively with native Convolvulaceae, whereas Washington State is noticeably lacking in Convolvulaceae. Results of assays were overlain on a phylogenetic analysis of plant species to examine whether Convolvulaceae distantly related to the typical host (potato) were less likely to allow development than species of Convolvulaceae more closely related. Survival was independent of psyllid population and location of the plant species on our phylogenetic tree. We then examined whether presence of a fungal symbiont of Convolvulaceae (Periglandula spp.) affected psyllid survival. These fungi associate with Convolvulaceae and produce a class of mycotoxins (ergot alkaloids) that may confer protection against plant-feeding arthropods. Periglandula was found in 11 of our 14 species, including in two genera (Convolvulus, Calystegia) not previously known to host the symbiont. Of these 11 species, leaf tissues from five contained large quantities of two classes of ergot alkaloids (clavines, amides of lysergic acid) when evaluated by LC-MS/MS. All five species also harbored Periglandula. No ergot alkaloids were detected in species free of the fungal symbiont. Potato psyllid rapidly died on the five species that harbored Periglandula and contained ergot alkaloids, but survived to adulthood on seven of the nine species in which ergot alkaloids were not detected. These results support the hypothesis that a plant-fungus symbiotic relationship affects the suitability of certain Convolvulaceae to potato psyllid.

Assessments of Temporal Variations in Haplotypes of 'Candidatus Liberibacter solanacearum' and Its Vector, the Potato Psyllid, in Potato Fields and Native Vegetation.

The potato psyllid, Bactericera cockerelli (Sulc) (Hemiptera: Triozidae), had been known for nearly a century to cause psyllid yellows of solanaceous crops. However, it has only been a decade since the insect was discovered to transmit the bacterium 'Candidatus Liberibacter solanacearum' (Lso), which putatively causes potato zebra chip disease. This project was initiated to quantify temporal incidences of haplotypes of the psyllid (Central, Southwestern, and Western) and Lso (A, B) in potato fields and in native vegetation. Psyllids were collected from native vegetation in Texas (2011-2014), and from potato fields in Texas and New Mexico (2014-2017). Psyllids were tested for Lso and haplotypes of both psyllid and Lso. In Texas, the Central psyllid haplotype was overwhelmingly dominant both in potato fields and in native vegetation regardless of location and time of collection. However, in New Mexico potato fields, although the Southwestern haplotype was overall dominant, the ratios of individual haplotypes varied among years and within a season. The Southwestern psyllid haplotype was greater in incidence than the Central early but declined later in the season in each of the 4 yr, while the Central haplotype was low in incidence early but increased over time. Lso was detected in all three psyllid haplotypes representing the first report in Southwestern psyllid haplotype. In Texas, Lso haplotype A was more frequently detected than B, but in New Mexico the incidence of positive psyllids was not high enough to make definitive conclusions regarding predominant Lso haplotype.

Postharvest Development of 'Candidatus Liberibacter solanacearum' in Late-Season Infected Potato Tubers under Commercial Storage Conditions.

Zebra chip (ZC) disease of potato is associated with the putative pathogen 'Candidatus Liberibacter solanacearum', which is transmitted by the potato psyllid Bactericera cockerelli (Hem., Triozidae). The present study was initiated to investigate 'Ca. L. solanacearum' development during and following typical commercial storage practices. Using bacteriliferous psyllids, Russet Norkotah potato tubers were infested in field cages 14, 10, and 4 days before harvest. Changes in 'Ca. L. solanacearum' detection rate, 'Ca. L. solanacearum' titer, and concentrations of phenolic compounds were documented throughout storage. 'Ca. L. solanacearum' titer continued to increase during storage. Although significant increases in the frequency of 'Ca. L. solanacearum' detection were observed in all infestation treatments, the impact of 'Ca. L. solanacearum' infection on tuber quality remained comparatively low in plants infected 4 days before harvest, because the majority of the tubers remained asymptomatic. Minimizing storage and retail chain movement durations would help to limit 'Ca. L. solanacearum' impact on tuber quality in tubers infected 14 and 10 days before harvest. This study also demonstrated that 'Ca. L. solanacearum' can relocate from a newly infected leaf to a tuber in as little as 4 days. Psyllid management is recommended until at least 4 days before green harvest, when psyllid pressure is high in fields in which tubers are destined for commercial storage.

Characterization of host plant resistance to zebra chip disease from species-derived potato genotypes and the identification of new sources of zebra chip resistance.

'Candidatus Liberibacter solanacearum' (Lso), an uncultivable phloem-limited phytopathogenic bacteria, is known to be associated with Zebra Chip disease (ZC), which represents a major threat to potato production in the US and elsewhere. This pathogen is transmitted by the phloem-feeding potato psyllid, Bactericera cockerelli Sulc (Hem. Triozidae). Currently, there are no reports of resistance to ZC in cultivated potatoes. This greenhouse study was conducted to evaluate Lso transmission success and the susceptibility of 11 potato breeding clones, representing diverge genetic background, to ZC, in relation to a susceptible commercial cultivar, Russet Burbank. Individual plants were exposed to two Lso-positive potato psyllids for 48 hours. The percentage of successful Lso transmission varied across the evaluated genotypes ranging between 7 and 57%. Freshly-cut and fried tubers showed significant variation in ZC symptom severity among the breeding clones, with several genotypes expressing relative tolerance when compared to Russet Burbank. None of the evaluated clones showed statistically lower Lso titers than Russet Burbank with the exception of one genotype in the second year of the study. However, the presence of a non-significant relationship between average symptom severity and Lso titer indicated variations in phenotypic responses (i.e. tolerance) to Lso existed among evaluated breeding lines. Breeding clones A07781-3LB, A07781-4LB and A07781-10LB had relatively lower Lso titer (low susceptibility) and tuber symptom expression (high tolerance) among the tested genotypes. As these three clones represent full siblings, the observed effects could be indicative of the presence of a genetic basis for resistance/tolerance to ZC. Findings provide a better understanding of resistance/tolerance to ZC, and contribute to continued efforts in breeding for resistance to this disease.

Variations in Zebra Chip Disease Expression and Tuber Biochemistry in Response to Vector Density.

Zebra chip (ZC) disease, caused by 'Candidatus Liberibacter solanacearum', which is transmitted by the potato psyllid, has negatively affected potato production in the United States for over a decade. The present study was conducted to evaluate the affect of the number of bacteriliferous psyllids on 'Ca. L. solanacearum' titer, levels of amino acids, carbohydrates, phenolics, and, subsequently, symptom severity in potato tubers. 'Red La Soda' and 'Russet Norkotah' potato were planted in the field and later inoculated with 'Ca. L. solanacearum' using 5, 10, and 30 bacteriliferous potato psyllids. In both cultivars, the increase in the number of psyllids resulted in elevated 'Ca. L. solanacearum' titer and symptom severity. In the cases of amino acids and reducing sugars, responses to vector density appeared to be cultivar specific. Overall, phenolic compounds showed a consistent increase following infection, a response that, in most cases, was positively correlated with the number of infective psyllids. Results quantified the impact of the number of infective psyllids on 'Ca. L. solanacearum' titer and biochemical content of infected tubers previously shown to be correlated with the degree of symptom expression. Managing vector numbers is currently the only effective approach for minimizing losses to ZC in grower's fields. However, our findings on physiological responses to vector density suggest that, in combination with chemical control, development of more tolerant or resistant potato genotypes, with emphasis on interrupting pathways that are associated with increased phenolic activity levels, may lead to more sustainable management of ZC in the future.