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Maize Response to Corn Leafhopper (Homoptera: Cicadellidae) Infestation and Achaparramiento Disease
Abstract
To determine the effect that the timing of infestation of Dalbulus maidis (DeLong &Wolcott), a vector of 3 maize pathogens, known collectively as "achaparramiento," has on stunt symptoms and maize yield, we conducted a field trial in the Sebaco Valley of Central Nicaragua. Achaparramiento has caused severe yield losses in maize throughout Central America. Six periods of D. maidis infestation were created using exclusion cages of finemesh screening. The treatments were natural infestations of D. maidis during 0-10, 10-20, 20-30, 30-40, 0-40 d after plant emergence, and no D. maidis infestation. The treatments were repeated on 3 planting dates. During the season, population densities of D. maidis varied from 4 to 8 per plant for the 1st planting date, from 1 to 3 per plant in the 2nd planting date, and from 2 to 8 per plant in the 3rd date. Planting date had a significant effect on plant height, the number of ears, and the yield per plant, but not on disease symptoms or the length of the ears. The timing and duration of D. maidis infestation affected disease symptoms, plant height, and yield: earlier periods of D. maidis infestation produced more pronounced disease symptoms, shorter plants, and lower yields than treatments with late D. maidis infestation. Plant infested 10-20 d after plant emergence had significantly lower yields than plants infested 30-40 d after plant emergence, and plants infested 30-40 d after plant emergence did not have Significantly different yields from plants that were not infested. The yield reduction was caused by smaller ears, not a reduction in the number of ears. The results demonstrate that a management program for reducing the effects of maize stunting diseases caused by the 3 pathogens should be focused on tactics that reduce D. maidis levels from seedling through midwhorl stage of maize growth.
... The reason for monitoring the vector from the first leaf to V 7-8 stages is because the early phenological stages of corn are the most susceptible to the acquisition of CSS (Hruska and Gómez Peralta 1997), and in further growth stages, the canopy is so developed that it is impossible to continue with accurate monitoring of the vector. ...
... In contrast to our results, Castro et al. (1992) while studying the influence of maize sown density on the incidence of the "corn stunting" disease, found a lower percentage of infection in plots with a higher density compared to those with a lower density, as a result of fewer vectors per plant in the former. Infected plants in the early stages show the highest levels of symptomatology (Hruska and Gómez Peralta 1997). It is noteworthy to mention that some levels of fertilization do not avoid plant infestation by the mollicutes but only limit the symptoms of the disease. ...
The corn leafhopper Dalbulus maidis is a specialist herbivore that attacks maize in the tropical and subtropical regions of the Americas. It is the vector of three relevant plant pathogens that are responsible for severe yield losses. Modern agriculture is dependent on the addition of fertilizers, especially nitrogen, which may influence the nutritional quality and/or the defense ability of the plants possibly with a subsequent increment of herbivorous insect populations. Through a field experiment, using a randomized design with four treatments with incremental levels of fertilization, we evaluated the effects of nitrogen in corn on the population level of the vector D. maidis, on the incidence of the diseases transmitted by it, and on the level of parasitism of the vectors’ eggs. The amount of nitrogen fertilizer used significantly influenced the density of the corn leafhopper and, as a consequence, the parasitism by egg parasitoids, but not the incidence of the diseases transmitted by it. Two weeks after fertilization, the vector density was significantly higher in the highly fertilized treatment. The disease incidence was not directly linked with the level of fertilization. However, the symptoms of the diseases were much less evident in plants that received higher fertilization. Levels of parasitism by egg parasitoids increased accordingly to the level of D. maidis populations. The management of nitrogen fertilization in corn crops can mitigate the negative effects of the corn stunting disease without affecting the levels of natural control performed by egg parasitoids.
... The reason for monitoring the vector from the rst leaf to V 7-8 stages is because the early phenological stages of corn are the most susceptible to the acquisition of CSS (Hruska and Gómez Peralta 1997), and in further growth stages, the canopy is so developed that it is impossible to continue with accurate monitoring of the vector. ...
... It is well known that the symptomatology caused by S. kunkelli and MBSP depends on many factors, including germplasm, climatic factors, and fundamentally the phenological stage of the corn plant at the time of infection, and perhaps also the MBSP isolate (Carpane et al. 2006;de Oliveira et al. 2018). Infected plants in the early stages show the highest levels of symptomatology (Hruska and Gómez Peralta, 1997). We assumed that infective D. maidis adults similarly colonized the plots, since the latter were randomly distributed, therefore the inoculum pressure would have been similar at the beginning of the assay in every plot. ...
The corn leafhopper Dalbulus maidis (Hemiptera: Cicadellidae) is a specialist herbivore that attacks maize in the tropical and subtropical regions of the Americas. It is vector of three relevant plant pathogens being responsible for severe yield losses. Modern agriculture is dependent on the addition of fertilizers, especially nitrogen, which may influence the nutritional quality of the plants possibly with a subsequent increment of herbivorous insect populations. Through a field experiment, using a randomized design with four treatments with different levels of fertilization, we evaluated the effects of nitrogen fertilization in corn on the population levels of the vector D. maidis , on the incidence of the diseases transmitted by it, and on the levels of parasitism of the vectors’ eggs. The amount of nitrogen fertilizer used significantly influenced the density of the corn leafhopper and the parasitism by egg parasitoids, but not the incidence of the diseases transmitted by it. Two weeks after fertilization, the vector density was significantly higher in the highly fertilized treatment. The disease incidence was not directly linked with the level of fertilization, however, the symptoms of the diseases were much less evident in plants that received higher fertilization. Parasitism levels by egg parasitoids increased accordingly to the level of D. maidis populations.
... Control methods, therefore, rely on attempts to either suppress or completely eradicate the insect vector, thus resulting in indirect pathogen control [27]. Indirect corn stunt disease control has been achieved through the application of insecticides, but it is debatable as to whether it produces a significant net return [30]. In addition, the application of insecticides has been recorded as having a potential negative impact on parasitoids and predators of D. maidis [30]. ...
... Indirect corn stunt disease control has been achieved through the application of insecticides, but it is debatable as to whether it produces a significant net return [30]. In addition, the application of insecticides has been recorded as having a potential negative impact on parasitoids and predators of D. maidis [30]. ...
Over 700 plant diseases identified as vector-borne negatively impact plant health and food security globally. The pest control of vector-borne diseases in agricultural settings is in urgent need of more effective tools. Ongoing research in genetics, molecular biology, physiology, and vector behavior has begun to unravel new insights into the transmission of phytopathogens by their insect vectors. However, the intricate mechanisms involved in phytopathogen transmission for certain pathosystems warrant further investigation. In this review, we propose the corn stunt pathosystem (Zea mays–Spiroplasma kunkelii–Dalbulus maidis) as an ideal model for dissecting the molecular determinants and mechanisms underpinning the persistent transmission of a mollicute by its specialist insect vector to an economically important monocotyledonous crop. Corn stunt is the most important disease of corn in the Americas and the Caribbean, where it causes the severe stunting of corn plants and can result in up to 100% yield loss. A comprehensive study of the corn stunt disease system will pave the way for the discovery of novel molecular targets for genetic pest control targeting either the insect vector or the phytopathogen.
... Due to D. maidis' efficiency as a vector of pathogens, control programs for this pest are not based upon an economic threshold (i.e., the density of a pest at which a control treatment will provide an economic return; Higley and Pedigo 1993), but rather on its mere presence in the corn field. This low tolerance may lead to excessive applications of insecticides per crop cycle, with potential negative impacts on natural enemies (Hruska et al. 1997). Several members of Mymaridae, Trichogrammatidae, and Chalcidoidea are parasitoids of D. maidis, attacking the species' eggs, nymphs and/ or adults , Querino et al. 2017). ...
Direct and indirect injury caused by Dalbulus maidis (Hemiptera: Cicadellidae) in corn is an ever-increasing concern in Brazil and other corn-producing countries of the Americas. This highly efficient vector transmits corn stunting pathogens and is of economic concern in the Neotropics, including temperate regions where epidemic outbreaks are now common. Despite the progress made so far, Brazilian corn growers continue to struggle with this pest and its associated pathosystem. In this review, we gathered relevant and updated information on the bioecology, population dynamics, and damaging potential of D. maidis. Our goal was to better understand its intimate association and complex interactions with the host crop and transmitted pathogens. Based on available scientific literature, we identified factors which explain the recent increase in D. maidis occurrence in South America, including the cultivation of corn during multiple growing seasons, overlapping of susceptible crops, and widespread use of genetically modified hybrids. The reasons for the overall inefficiency of current suppression strategies aimed at this pest are also summarized. Finally, a management program for D. maidis and corn stunt disease is proposed, combining strategies such as eradicating volunteer corn, reducing the planting period, using tolerant hybrids, and applying chemical and/or fungal insecticides. Prospects regarding the pest’s status are also outlined. Overall, the information presented here will serve as a decision-making guide within Brazilian and South American corn production systems, as well as paving the way for devising novel strategies aimed at suppressing D. maidis populations and limiting the spread of corn stunt disease.
... 3 These pathogens, either alone or in combination, cause the diseases referred to as corn stunt. 4,5 High infestation rates, which can reach 100% in some areas, may result in yield losses of up to 90%, representing a relevant threat to agriculture. 6,7 Current control strategies against D. maidis are limited to cornresistant germplasm 8 and use of insecticides as seed treatments or foliar sprays. ...
BACKGROUND
The corn leafhopper Dalbulus maidis is the main vector of three important stunting pathogens that affect maize production. The most common control strategy against this species is the use of insecticides that provide minimal, short-term protection. In this context, genomic-based technologies such as RNA interference (RNAi) could be a suitable approach to control this pest in a highly specific manner, avoiding the adverse effects associated with insecticide misuse. Therefore, the objective of the present work was to assess the application of RNAi on D. maidis through different dsRNA delivery methods and known the function of target gene, Bicaudal C ( BicC ).
RESULTS
We have identified and characterized the core components of the RNAi machinery in silico and established two methods of exogenous double-stranded RNAs (dsRNA) delivery to D. maidis . BicC -an important regulator of insect oogenesis-dsRNA was successfully delivered via injection or ingestion to adult females, causing significant reductions in the transcript levels and ovipositions and observable phenotypes in the ovaries when compared to control females. The small doses of dsRNA BicC administered were enough to trigger a strong RNAi response, demonstrating that D. maidis is highly sensitive to RNAi.
CONCLUSION
This is, to our knowledge, the first report describing RNAi application in D. maidis , a tool that can be used to advance towards a novel, insecticide-free control strategy against this pest.
... Reduced yield resulting from Corn Stunt disease is directly related to symptom severity and the accumulation of the pathogen S. kunkelii [24], which are both highest if S. kunkelii is inoculated at early growth stages [25,26]. In this situation, reduced yield may be high, ranging from 12 to 100% [25][26][27][28]. ...
Corn Stunt is an important disease in the Americas due to it high prevalence and the yield reductions that can cause when present. However, changes in the presence of this disease across years hampers the effective identification of resistant genotypes to this disease. To avoid the limitations of phenotypic selection under natural pressure, this research aimed to devise an effective strategy to screen disease-resistant genotypes in the absence of high and constant natural pressures. To do so, we investigated the presence of antixenosis and antibiosis as components of resistance to the vector Dalbulus maidis as well as resistance to the pathogen Spiroplasma kunkelii under artificial inoculation conditions in four maize hybrids. The hybrids shown differences in their levels of resistance and target organisms, either the insect vector or the pathogen. Antixenosis and antibiosis to D. maidis were observed in DK72-10. Resistance to S. kunkelii by DK79-10 was seen as a delayed onset of symptoms, and DKB390 showed antixenosis to D. maidis and resistance to S. kunkelii. An association between symptom severity and yield reduction was found, but not between accumulation of pathogen S. kunkelii and symptom severity nor yield. In conclusion, the proposed methodology was efficacious and can aid in the screening of resistant genotypes in breeding programs to reduce the impact of Corn Stunt disease, ensuring that hybrids with good resistance level will be planted by farmers whenever disease occurs.
... Reduced yield resulting from Corn Stunt disease is directly related to symptom severity and the accumulation of the pathogen S. kunkelii [24], which are both highest if S. kunkelii is inoculated at early growth stages [25,26]. In this situation, reduced yield may be high, ranging from 12 to 100% [25][26][27][28]. ...
Considering the occasional but increasing presence of corn stunt disease in the subtropical region of Argentina, the objective of this research was to devise an effective strategy to screen disease-resistant genotypes in the absence of high and constant natural pressures. To do so, the presence of antixenosis and antibiosis as components of resistance to vector Dalbulus maidis (DeLong 1923) as well as resistance to the pathogen Spiroplasma kunkelii (Whitcomb et al. 1986) under artificial inoculation conditions were investigated in four widely-distributed maize hybrids in Argentina. The hybrids shown differences in the levels of resistance and target organisms (either the insect vector or the pathogen). Antixenosis and antibiosis to D . maidis were observed in DK72-10. Resistance of DK79-10 to S . kunkelii was evidenced by a delayed onset of symptoms, and DKB390 was antixenotic to D . maidis and highly resistant to S . kunkelii . A good association was found between symptom severity and yield, but not between symptom severity and accumulation of pathogen S . kunkelii . In conclusion, the proposed methodology was efficacious and can aid the screening of resistant genotypes in breeding programs to reduce the impact of corn stunt disease, ensuring that hybrids with good resistance level will be planted by farmers whenever disease occurs.
Background:
The corn leafhopper Dalbulus maidis is the main vector of important stunting pathogens that affect maize production. Currently, there are no effective methods available to manage this pest without adverse impact on the environment. In this context, genomic-based technologies such as RNA interference (RNAi) provide a more environmentally friendly pest control strategy. Therefore, we aimed to assess the application of RNAi in D. maidis and determine the function of a candidate gene related to insect reproduction and propagation.
Results:
We have characterized the core RNAi genes and evaluated the functionality of the RNAi machinery. We assessed the potential of RNAi technology in D. maidis via injection or ingestion of double-stranded RNA (dsRNA) to adult females. We chose Bicaudal C (BicC) as a target gene due to its important role during insect oogenesis. Administration of dsRNABicC caused significant reductions in the transcript levels (fold changes up to 170 times) and ovipositions. Phenotypic analysis of the ovaries revealed alterations in oocyte development, providing additional confirmation on our results and supporting the idea that Dmai-BicC is a key player of D. maidis oogenesis.
Conclusion:
This is, to our knowledge, the first report of efficient RNAi in D. maidis. We believe our findings provide a starting point for future control strategies against one of the most important maize pests in the Americas. This article is protected by copyright. All rights reserved.
BACKGROUND
The corn leafhopper, Dalbulus maidis (Hemiptera: Cicadellidae), spreads maize stunt pathogens and requires timely and effective crop protection. We determined the interaction between maize phenology and the vector feeding/infection period by stunt pathogens with the residual efficacy of neonicotinoid insecticidal seed treatments. Greenhouse- and field-grown maize plants, seed-treated with clothianidin or imidacloprid insecticides, were infested during seven growth stages with corn leafhoppers reared under controlled conditions on maize plants displaying infection symptoms by both spiroplasma (corn stunt spiroplasma – Spiroplasma kunkelii – CSS) and phytoplasma (maize bushy phytoplasma – MBSP) pathogens.
RESULTS
In the greenhouse and field settings, seed treatment reduced the stunt disease symptoms and corn yield loss during the VE–V4 maize growth stages and caused no phytotoxicity. The neonicotinoid-seed treatment reduced 20–60% of the yield losses from the corn stunt disease until the V4 growth stage. Infestation by infective corn leafhoppers in the V12 maize growth stage caused a 25–30% yield loss irrespective of seed treatment, yet no stunt disease symptom was evident. Nonetheless, corn yield losses and visual stunt symptoms as rated by a 9-category-ordinal scale were strongly correlated (r = 0.79, P < 0.01).
CONCLUSION
These results reinforce that maize plants are more susceptible to leafhopper stunt disease during the VE–V4 growth stages (emergence to the fourth-leaf stage). Seed treatment helps reduce the damage in the early growth stages (VE–V2), although supplemental control measures depending on leafhopper population density may be needed from VE–V12 to protect yield losses from the maize stunt condition.
The maize leafhopper Dalbulus maidis (DeLong) (Hemiptera: Cicadellidae) is a specialist herbivore that develops on maize plants (Zea mays L., Poaceae). Every year, it is responsible for considerable reductions in yields of the maize fields of the Americas, because alongside its direct damages it is also a vector of three relevant plant pathogens. The transmitted diseases come to have a high incidence, resulting in significant yield losses, thereby forcing farmers and technicians to attempt a tight control of the fields mostly using non‐specific insecticides. Decision support systems based on mathematical models may be valuable in helping to reduce the use of agrochemicals in this regard, as they can provide a projection of the future situation based on past and present data. With this precondition, this work aims to apply and validate a physiologically based model to describe populations of D. maidis developing in two experimental fields located in Argentina, which are characterised by different climatic conditions. Experimentation in the two fields involved a 3‐year survey during the growing seasons 2009, 2010, and 2011, where the adult populations of maize leafhoppers were monitored from the sowing of maize plants to the end of the phenological stage at which they are most susceptible to D. maidis activity. Results showed a good response of the model in describing maize leafhopper populations, also allowing the possibility of setting a threshold for intervention and a projection of the situation if any control action is applied.
The corn leafhopper, Dalbulus maidis (Delong & Wolcott) and the “Mexican corn leafhopper, D. elimatus (Ball) were collected from the perennials Zea diploperennis Iltis, Doebley & Guzmán, Z. perennis (Hitchc.) and Tripsacum lanceolatum Rupr. ex Fourn. in Jalisco, Mexico. These maize relatives represent new host records for these leafhoppers as well as potential overwintering sites. A new species, Dalbulus tripsacoides DeLong and Nault n. sp., was collected from Tripsacum dactyloides (L.) L. on the southwestern side of the Sierra de Autlán. Dalbulus tripsacoides is morphologically the most primitive member of the genus, supporting our hypothesis that leafhoppers of the genus Dalbulus coevolved with maize from its Tripsacum ancestors. We also speculate that the Dalbulus species and the corn stunt spiroplasma, maize bushy stunt mycoplasma and maize rayado fino virus, pathogens vectored by these leafhoppers, have influenced the speciation and distribution of maize and its predecessors.
Despite the economic importance of the corn leafhopper, Dalbulus maidis (DeLong & Wolcott), little is known about how this maize pest and its congeners survive the dry winter in Mexico. In the field, Dalbulus populations were monitored weekly with yellow sticky card traps for 18 mo at three sites in Jalisco, Mexico. The sites included a maize field, Zea maysL.; a natural stand of a perennial teosinte, Zea diploperennis Iltis, Doebley & Guzman; and a natural population of gamagrasses, Tripsacum spp., which are maize relatives. At all sites, highest catches of Dalbulus adults occurred during the dry season between October and March. In a laboratory study to test the survival of adult Dalbulus leafhoppers without their host plants, significant differences were detected among leafhopper species. When denied all food and water (absolute drought), Dalbulus species that specialize on maize were more tolerant than those that specialize on gamagrass. Adults reared under environmental conditions that simulate the beginning of the wet season (June-reared) were less tolerant of absolute drought than adults reared under early dry-season conditions (October-reared). When provided water but no food, October-reared D. maidis lived significantly longer than June-reared D. maidis. Survival of females under water-only conditions was significantly longer than that of males. Field observations revealed that gamagrassspecializing D. gelbus DeLong and D. quinquenotatus DeLong & Nault overwinter as continuously developing populations on their hosts. In contrast, our data indicate that D. maidis overwinter as active adults that can subsist, at least in part, on free water in the absence of host plants until the summer rainy season begins. Surviving adults then migrate locally to newly planted maize fields.
The incidence of maize stunt diseases, or achaparramiento, rose in Nicaragua from an insignificant level to national crisis proportions, then declined to insignificant levels again, all in the space of 10 yr. The 3 pathogens that cause achaparramiento, corn stunt spiroplasma, maize bushy stunt phytoplasma, and maize ray ado fino virus are transmitted by the corn leafhopper, Dalbulus maidis (De- Long & Wolcott). Vector populations did not change sufficiently over time to explain the epidemic pattern. Nor did changes in the varieties of maize that farmers used cause the differential expression of disease symptoms during this period. The most likely explanation of the epidemic pattern is an abrupt 3- to 4-yr increase in irrigated maize production during the dry season, when maize was not grown traditionally. Irrigated maize provided a temporal bridge for the pathogens, which then were transmitted to rainy season plantings and caused epidemic disease incidence throughout the country. This explanation demonstrates the powerful impact that governmental agricultural policies, in this case to strongly promote dry-season maize production, can have on crop pest and pathogen problems.
In 1978, 182 maize farmers, stratified in six farm size classes in four production regions, the Pacific North and Central and the Interior Central and South, which cover most of Nicaragua, were interviewed. Farm characteristics, physical inputs, credit, technical assistance, risk perception, pest recognition, cultural practices and chemical control have been analysed for differences between production regions and for trends according to farm size. Farmers consider drought and insect pests the main factors limiting maize production. About 80% of all applications are directed against the whorl-feeding larvae of Spodoptera frugiperda, which farmers correctly consider the main pest in maize. Most of these applications seem unnecessary. The expected effects of cultural practices, rainfall and lunar cycle on pest incidence have been analysed. Most of the traditional pest control methods used in Nicaragua proved to be very appropriate, indicating that such inventarizations and evaluations can be of great value.-from Authors
The effect of the natural ant community as a possible source of biological control for the fall armyworm, Spodoptera frug/perda (]. E. Smith), and the corn leafhopper, Valbtllus rna/dis (De Long & Wolcott), was examined in irrigated maize, Zea mays L., in the Pacific plains of Nicaragua. By means of poison baits, ant-foraging activity was reduced in plots planted with maize and compared with control plots. Ants were found to significantly reduce fall armyworm and corn leafhopper abundance as well as damage by the fall armyworm to maize plants. The results are discussed in relation to establishing economic injury levels for the fall armyworm in irrigated maize and the possibility of incorporating ants as a component of an integrated pest management program on maize in Nicaragua.