Hessian Fly Populations Research Articles

Higher levels of virulence to multiple resistance genes were detected in Hessian fly (Mayetiola destructor) populations from Texas

AbstractHessian fly is an important pest of wheat worldwide and is of particular importance in Texas and the southeastern United States. Texas is the highest wheat‐producing state that is severely impacted by this insect. The most effective control in these areas is an integrated pest management program, including resistant varieties of wheat. Hessian fly populations are genetically diverse and can rapidly become virulent to specific resistance genes once they are widely deployed in a region. Knowing the current virulence status of regional fly populations is important for wheat breeders and producers. In this study, a virulence analysis was conducted on populations sampled in the northeastern and central Texas regions. This analysis showed that resistance genes H12, H13, H20, H22, H25, H26, H28, H29, H32, H33, H34, and Hdic are still highly effective in these regions. However, it is also evident that Texas fly populations have become more virulent to existing genes in the past 10 years, with very high levels of virulence to resistance genes H3, H5, vH6, H7/H8, H9, H10, H14, H15, H23, H24, H31, and H35/H36.

Hessian fly (Diptera: Cecidomyiidae) virulence in Louisiana: assessment of field populations from 2023 to efficacy of 27 Hessian fly resistance genes in wheat.

The Hessian fly, Mayetiola destructor (Say), is one of the most important insect pest plaguing wheat (Triticum aestivum, L) producers across the United States and around the world. Genetic resistance is the stalwart for control of Hessian fly. However, new genotypes (biotypes) arise in deployment of wheat containing resistance genes, so field populations must be evaluated periodically to provide information on the efficacy of those deployed genes. Louisiana (LA), with its diverse agricultural landscape, is not exempt from the challenges posed by this destructive pest. We previously documented the resistance response of wheat lines harboring Hessian fly resistance (H) genes against field populations collected in 2008 from across the southeastern United States, including Iberville Parish, LA. In the spring of 2023, we reevaluated the resistance response of 27 H genes from the field populations collected from Iberville Parish, LA, and compared the results with those observed in 2008. Sixteen H genes showed comparable resistance to the field populations from both years. While 3 of the H genes, H11, H23, and H24, showed a significant decrease in resistance, 2 genes, H16 and H31, had marked increase in resistance. Furthermore, 6 additional H genes were evaluated in 2023, with 4 showing >70% resistance. Our results clearly identify a total of 20 H genes that are moderate to highly effective against the 2023 Hessian fly population from Iberville Parish, LA. The resistance response documented in this study offers valuable information to wheat breeders in the region for effective management of this insect pest.

Effect of temperature on the expression of resistance to Hessian fly (Diptera: Cecidomyiidae) in durum wheat cultivars

Hessian fly, Mayetiola destructor (Say) is a destructive insect pest occurring in many wheat growing areas of the world. The most effective management option for controlling Hessian fly is the use of resistant wheat cultivars carrying specific resistance genes. However, wheat resistance genes to Hessian fly are affected by temperature. Two Moroccan cultivars ‘Chaoui’ and ‘Marouane’ and three ICARDA elites DWHF01, DWHF02 and Icamoram7 all carrying resistance to Moroccan Hessian fly populations were evaluated at three different temperatures (20, 25 and 30 °C). Results showed that the elite DWHF01 and DWHF02 resistance was less affected by higher temperatures with percentage of resistant plants remaining above 60% at 30 °C. However, ‘Marouane’, ‘Icamoram7’ and ‘Chaoui’ lost more than 50% of their resistance at 30 °C. Resistance in all these genotypes was expressed only as antibiosis with presence of dead first instars on resistant plants. The number of live larvae on susceptible plants was counted and larval density decreased with increasing temperature. Moreover, length measurements of live larvae showed significant differences across different temperatures, the size of larvae increased as temperature increased and ranged between 3.23 and 4.13 mm. In light of the warming climates and increase occurrence of days above 30 °C during the first months of the Moroccan wheat season, the data presented here are meant to help breeders recommend cultivars better adapted to the raising temperatures.

Wheat Yield in a Tolerant Winter Wheat Line Infested by Hessian Fly (<i>Mayetiola destructor</i>)

The Hessian fly, Mayetiola destructor, is a harmful pest of wheat (Triticum aestivum). Pioneer variety 25R78 is putatively tolerant, meaning that the plant can survive successful Hessian fly infestation with reduced growth effects. To understand if Hessian fly-tolerance in wheat results in reduced yield effects and to analyze the economic feasibility of tolerant wheat as a Hessian fly control method, this study focused on analyzing the effect of infestation on tolerant wheat yield. This study analyzed tolerant Pioneer variety 25R78, resistant Pioneer brand variety 25R32, and susceptible Pioneer brand variety 25R47 through harvest. Treated plants were infested using a plastic cover and allowing 1 - 2 female flies to lay eggs for two hours. We measured head, fertile head number and tiller number. Seeds were analyzed by measuring total seed number and weight, as well as average seed number and weight. Tolerant and resistant plants showed no significant effects on yield in comparison to susceptible wheat. The infested tolerant plants were comparable in yield to infested resistant plants. Therefore, we propose that tolerance incorporated into wheat varieties will lower selection pressure on Hessian fly populations and increase the durability of these wheat lines.

Detection of Wolbachia Infections in Natural and Laboratory Populations of the Moroccan Hessian Fly, Mayetiola destructor (Say).

Mayetiola destructor (Hessian fly) is a destructive pest of wheat in several parts of the world. Here, we investigated the presence of reproductive symbionts and the effect of the geographical location on the bacterial community associated to adult Hessian flies derived from four major wheat producing areas in Morocco. Using specific 16S rDNA PCR assay, Wolbachia infection was observed in 3% of the natural populations and 10% of the laboratory population. High throughput sequencing of V3-V4 region of the bacterial 16S rRNA gene revealed that the microbiota of adult Hessian flies was significantly influenced by their native regions. A total of 6 phyla, 10 classes and 79 genera were obtained from all the samples. Confirming the screening results, Wolbachia was identified as well in the natural Hessian flies. Phylogenetic analysis using the sequences obtained in this study indicated that there is one Wolbachia strain belonging to supergroup A. To our knowledge, this is the first report of Wolbachia in Hessian fly populations. The observed low abundance of Wolbachia most likely does not indicate induction of reproductive incompatibility. Yet, this infection may give a new insight into the use of Wolbachia for the fight against Hessian fly populations.

Susceptibility of North Dakota Hessian Fly (Diptera: Cecidomyiidae) to 31 H Genes Mediating Wheat Resistance.

The agricultural landscape of North Dakota is changing. Corn and soybean are now commonplace, but once were rare. Spring sown wheat Triticum aestivum L. and durum wheat Triticum turgidum spp. durum continue to be dominant, but more winter-sown wheat is expected in the future. The presence of wheat in the landscape throughout much of the year will benefit populations of the Hessian fly, Mayetiola destructor (Say), which occurs throughout the state, sometimes in large numbers. Hessian fly is unusual among crop pests for which resources for plant resistance are well developed. On wheat genotypes expressing a single effective H resistance gene, 100% of larvae die before exhibiting any growth. Over 35 H genes in the public domain are available for crossing into elite cultivars. We explored the effectiveness of 31 Hessian fly resistance genes for a North Dakota Hessian fly population. Six genes-H4, H15, H21, H23, H26, and H29-caused 100% larval mortality. Seven others caused at least 80% mortality. Experimental data were used to address three additional questions. Do adult females avoid laying eggs on plants that will kill their offspring: Are neonate larvae able to detect resistance that will end up killing them? Do all 31 genes confer equal protection against larval-induced growth deficits? North Dakota wheat breeders have the necessary tools to create highly resistant wheat cultivars. So far, H genes have been deployed singly in cultivars. Advances in plant breeding will enable gene stacking, a more durable strategy over time.

12-Oxo-Phytodienoic Acid Enhances Wheat Resistance to Hessian Fly (Diptera: Cecidomyiidae) Under Heat Stress

12-Oxo-phytodienoic acid (OPDA) plays unique roles in plant defenses against biotic and abiotic stresses. In the current study, we infested two resistant wheat (Triticum aestivum L.) cultivars, 'Molly' and 'Iris', with an avirulent Hessian fly population and determined the impact of exogenous OPDA application on wheat resistance to the insect under heat stress. We observed that Molly and Iris treated with OPDA solution prior to the heat treatment exhibited significantly enhanced insect resistance. We also measured OPDA concentrations at Hessian fly feeding sites in Molly infested with Hessian flies. We found that exogenous application of OPDA resulted in increased abundance of endogenous OPDA in Molly seedlings and that OPDA abundance in plants treated with the combination of heat and OPDA was similar to that of plants in the incompatible interaction. Our results suggest that high abundance of endogenous OPDA may be necessary for wheat under heat stress to resist to Hessian fly infestation.

A Novel, Economical Way to Assess Virulence in Field Populations of Hessian Fly (Diptera: Cecidomyiidae) Utilizing Wheat Resistance Gene H13 as a Model.

Mayetiola destructor (Say) is a serious pest of wheat, Triticum aestivum L., in North America, North Africa, and Central Asia. Singly deployed resistance genes in wheat cultivars have provided effective management of Hessian fly populations for >50 yr. Thirty-five H genes have been documented. Defense mediated by the H gene constitutes strong selection on the Hessian fly population, killing 100% of larvae. A mutation in a matching Hessian fly avirulence gene confers virulence to the H gene, leading to survival on the resistant plant. As the frequency of virulence rises in the population, the H gene loses its effectiveness for pest management. Knowing the frequency of virulence in the population is not only important for monitoring but also for decisions about which H gene should be deployed in regional wheat breeding programs. Here, we present a novel assay for detecting virulence in the field. Hessian fly males were collected in Alabama, Georgia, North Carolina, and South Carolina using sticky traps baited with Hessian fly sex pheromone. Utilizing two PCR reactions, diagnostic molecular markers for the six alleles controlling avirulence and virulence to H13 can be scored based on band size. Throughout the southeast, all three avirulence and three virulence alleles can be identified. In South Carolina, the PCR assay was sensitive enough to detect the spread of virulence into two counties previously documented as 100% susceptible to H13. The new assay also indicates that the previous methods overestimated virulence in the field owing to scoring of the plant instead of the insect.

Targeted Discovery of Single‐Nucleotide Polymorphisms in an Unmarked Wheat Chromosomal Region Containing the Hessian Fly Resistance Gene H33

The durum wheat [Triticum turgidum L. subsp. durum (Desf.) Husn.] Hessian fly [Mayetiola destructor (Say)] resistance gene H33 was previously introgressed into common wheat (T. aestivum L.) and mapped to chromosome 3AS. However, H33 located to a region that is known to be devoid of molecular markers, with the closest flanking simple‐sequence repeat (SSR) markers 7.4 and 25.1 cM from the gene. This lack of markers flanking economically important genes is a common problem in self‐pollinating crops because of low polymorphism and, in the case of wheat, a large genome size. H33 is currently effective against all virulent Hessian fly populations tested from the southeastern United States, a region where deployed resistance genes are beginning to fail; thus, effort was needed to identify tightly linked flanking markers to use this valuable gene in marker‐assisted selection (MAS). To target the 25.1‐cM segment adjacent to H33 for marker discovery, eight resistant and four susceptible plants were selected for genotyping‐by‐sequencing (GBS). Four single‐nucleotide polymorphisms (SNPs) were identified, with the closest marker being only 6.7 cM away and converted into high‐throughput polymerase chain reaction (PCR)‐based markers for the Kompetitive Allele Specific PCR (KASP) assay. In addition, endonucleases were identified that cut at the SNPs for restriction profiling as an alternate to the KASP assay. Development of these cost‐effective markers provided both low‐ and high‐throughput alternatives for introgressing H33 into wheat cultivars while minimizing linkage drag associated with durum regions of chromosome 3AS.

Differential expression of candidate salivary effector proteins in field collections of Hessian fly, Mayetiola destructor

Evidence is emerging that some proteins secreted by gall-forming parasites of plants act as effectors responsible for systemic changes in the host plant, such as galling and nutrient tissue formation. A large number of secreted salivary gland proteins (SSGPs) that are the putative effectors responsible for the physiological changes elicited in susceptible seedling wheat by Hessian fly, Mayetiola destructor (Say), larvae have been documented. However, how the genes encoding these candidate effectors might respond under field conditions is unknown. The goal of this study was to use microarray analysis to investigate variation in SSGP transcript abundance amongst field collections from different geographical regions (southeastern USA, central USA, and the Middle East). Results revealed significant variation in SSGP transcript abundance amongst the field collections studied. The field collections separated into three distinct groups that corresponded to the wheat classes grown in the different geographical regions as well as to recently described Hessian fly populations. These data support previous reports correlating Hessian fly population structure with micropopulation differences owing to agro-ecosystem parameters such as cultivation of regionally adapted wheat varieties, deployment of resistance genes and variation in climatic conditions.

The evolution of Hessian fly from the Old World to the New World: Evidence from molecular markers.

Eighteen polymorphic microsatellite loci and 11 single-nucleotide polymorphisms were genotyped in 1,095 individual Hessian fly specimens representing 23 populations from North America, southern Europe, and southwest Asia. The genotypes were used to assess genetic diversity and interrelationship of Hessian fly populations. While phylogenetic analysis indicates that the American populations most similar to Eurasian populations come from the east coast of the United States, genetic distance is least between (Alabama and California) and (Kazakhstan and Spain). Allelic diversity and frequency vary across North America, but they are not correlated with distance from the historically documented point of introduction in New York City or with temperature or precipitation. Instead, the greatest allelic diversity mostly occurs in areas with Mediterranean climates. The microsatellite data indicate a general deficiency for heterozygotes in Hessian fly. The North American population structure is consistent with multiple introductions, isolation by distance, and human-abetted dispersal by bulk transport of puparia in infested straw or on harvesting equipment.

H33: A Wheat Gene Providing Hessian Fly Resistance for the Southeastern United States

ABSTRACTHessian fly populations adapt to overcome newly deployed resistance genes within a few years of release. Although more than 34 genes have been identified that confer resistance against Hessian fly [Mayetiola destructor (Say)] attack in wheat (Triticum aestivum L.), only five genes currently provide resistance against fly populations in the southeastern United States. But even these genes are not 100% effective, leaving Georgia and North and South Carolina with between one and three effective genes for cultivar development. With the goal of providing much needed resistance for this region in a wheat line suitable for use with marker‐assisted selection, we identified a durum wheat line that confers resistance to Hessian fly populations from Maryland, Delaware, North and South Carolina, and Georgia in 100% of the plants tested. Resistance from this tetraploid durum line, PI 134942, was introgressed into hexaploid common wheat to generate the line 97211. Segregating populations of F2:3 families were constructed with the durum donor and with the common wheat recipient to identify resistance genes and provide flanking markers. Although the resistance of the durum donor appeared to involve more than one gene, one partially dominant but very effective gene, H33, was successfully transferred and identified in the hexaploid recipient. This gene was mapped to the short arm of wheat chromosome 3A and is flanked by single sequence repeat markers xgwm218 and hbg284.

Virulence and Biotype Analyses of Hessian Fly (Diptera: Cecidomyiidae) Populations From Texas, Louisiana, and Oklahoma

Hessian fly, Mayetiola destructor (Say, 1817), is a major pest of wheat, and is controlled mainly through deploying fly-resistant wheat cultivars. The challenge for the plant resistance approach is that virulence of Hessian fly populations in the field is dynamic, and wheat cultivars may lose resistance within 6-8 yr. To ensure continuous success of host plant resistance, Hessian fly populations in the field need to be constantly monitored to determine which resistance genes remain effective in different geographic regions. This study investigated five Hessian fly populations collected from Texas, Louisiana, and Oklahoma, where infestation by Hessian fly has been high in recent years. Eight resistance genes, H12, H13, H17, H18, H22, H25, H26, and Hdic, were found to be highly effective against all tested Hessian fly populations in this region, conferring resistance to > or = 80% of plants containing one of these resistance genes. The frequencies ofbiotypes virulent to resistance genes H13 (biotype vH13), H18 (vH18), H21 (vH21), H25 (vH25), H26 (vH26), and Hdic (vHdic) were determined, and were found to vary from population to population, ranging from 0 to 45%. A logistic regression model was established to predict biotype frequencies based on the correlation between the percentages of susceptible plants obtained in a virulence test and the log-odds of virulent biotype frequencies determined by a traditional approach.

Population Structure and Spatial Influence of Agricultural Variables on Hessian Fly Populations in the Southeastern United States

Population structure dictates the evolution of each population, and thus, the species as a whole. Incorporating spatial variables with population genetic statistics allows for greater discovery beyond traditional population genetics alone and can inform management decisions. The understanding of population structure in Hessian fly, Mayetiola destructor (Say), a pest of wheat, has been limited in the past. We scored 14 microsatellite loci from 12 collections of Hessian fly in the southeastern United States. Through Bayesian clustering analysis, we found two major populations of Hessian fly covering the entire southeastern United States. We evaluated correlations between agriculturally significant spatial variables and population genetic differentiation to test if genetic structure has an ecological component in a wheat agro-ecosystem. Our results suggest the total amount of alternative host plants in the county may be driving some genetic differentiation. Although planting date may also be influential, geographic distance, mean annual temperature, and harvested wheat for grain do not seem to be contributing factors. The ecological or spatial component to population structure, however, may be minimal compared to factors such as genetic drift.

Hessian Fly, Mayetiola destructor (Say), Populations in the North of Tunisia: Virulence, Yield Loss Assessment and Phenological Data

Hessian fly, Mayetiola destructor (Say), is a destructive pest of wheat worldwide and an endemic pest in Tunisia. Two natural populations of this insect from the North of Tunisia were evaluated, in the field, for their virulence, based on response developed by bread wheat (Triticum aestivum L.) cultivars carrying H3, H5, H6, H7H8, H11, H13 and H16 resistance genes. H11, H13 and H16 showed a high effectiveness against both populations; therefore, their implication in Hessian fly breeding programs would be of interest. The level of infestation, as well as the yield loss, was assessed, based on the percentage of infested plants and variation in growth parameters due to infestation. The percentage of infested plants, over a 2-yr period in Mateur, averaged 18.82% for durum wheat (Triticum turgidum L. subsp. durum (Desf.) Husn.) and 32.50% for bread wheat. For the improved durum wheat cv. Karim used as reference, the plant height, number of internodes, number of productive tillers per plant, and 100-seed weight were negatively affected by infestation, while the number of tillers per plant was positively affected. Aiming to update information about the annual number of the fly generations occurring on wheat, we surveyed infestation in Jedeida. At least three Hessian fly generations were detected on bread wheat and durum wheat. Continued regular surveying of Hessian fly populations in terms of virulence, impact on yield and annual generations is required for optimal deployment of resistance genes and integrated management of Hessian fly across all wheat production areas.

Induced epidermal permeability modulates resistance and susceptibility of wheat seedlings to herbivory by Hessian fly larvae

Salivary secretions of neonate Hessian fly larvae initiate a two-way exchange of molecules with their wheat host. Changes in properties of the leaf surface allow larval effectors to enter the plant where they trigger plant processes leading to resistance and delivery of defence molecules, or susceptibility and delivery of nutrients. To increase understanding of the host plant's response, the timing and characteristics of the induced epidermal permeability were investigated. Resistant plant permeability was transient and limited in area, persisting just long enough to deliver defence molecules before gene expression and permeability reverted to pre-infestation levels. The abundance of transcripts for GDSL-motif lipase/hydrolase, thought to contribute to cuticle reorganization and increased permeability, followed the same temporal profile as permeability in resistant plants. In contrast, susceptible plants continued to increase in permeability over time until the entire crown of the plant became a nutrient sink. Permeability increased with higher infestation levels in susceptible but not in resistant plants. The ramifications of induced plant permeability on Hessian fly populations are discussed.

A Reproductive Fitness Cost Associated With Hessian Fly (Diptera: Cecidomyiidae) Virulence to Wheat's <I>H</I> Gene-Mediated Resistance

We studied whether adaptation of the Hessian fly, Mayetiola destructor (Say) (Diptera: Cecidomyiidae), to plant resistance incurs fitness costs. In this gene-for-gene interaction, adaptation to a single H resistance gene occurs via loss of a single effector encoded by an Avirulence gene. By losing the effector, the adapted larva now survives on the H gene plant, presumably because it evades the plant's H gene-mediated surveillance system. The problem is the Hessian fly larva needs its effectors for colonization. Thus, for adapted individuals, there may be a cost for losing the effector, with this then creating a trade-off between surviving on H-resistant plants and growing on plants that lack H genes. In two different tests, we used wheat lacking H genes to compare the survival and growth of a nonadapted strain to two H-adapted strains. The two adapted strains differed in that one had been selected for adaptation to H9, whereas the other strain had been selected for adaptation to H13. Tests showed that two H-adapted strains were similar to the nonadapted strain in egg-to-adult survival but that they differed in producing adults with smaller wings. By using known relationships between wing length and reproductive potential, we found that losses in wing length underestimate losses in reproductive potential. For example, H9- and H13-adapted females had 9 and 3% wing losses, respectively, but they were estimated to have 32 and 12% losses in egg production. Fitness costs of adaptation will be investigated further via selection experiments comparing Avirulence allele frequencies for Hessian fly populations exposed or not exposed to H genes.

Development and Validation of Molecular Markers Closely Linked to H32 for Resistance to Hessian Fly in Wheat

Hessian fly [Mayetiola destructor (Say)] is an important insect pest of wheat (Triticum aestivum L.). Host resistance conferred by H genes has been the most effective means to manage Hessian fly populations. More than 32 H genes have been identified in wheat and its relatives. In a previous study, Hessian fly‐resistance gene H32 was assigned to the chromosomal bin 3DL3–0.81–1.00, which also harbors H26 The objectives of this study were to develop and validate sequence‐tagged site (STS) markers closely linked to H32 and to determine the genetic relationship between H26 and H32 In this study, 11 wheat EST‐derived STS markers linked to H26 and three new STS markers were added to the linkage map of H32 using the International Triticeae Mapping Initiative (ITMI) population. Two of the STS markers, Xrwgs10 and Xrwgs12, were found to flank H32 with a genetic distance of 0.5 cM. Another STS marker Xrwgs11, co‐segregated with H32 Molecular markers tightly linked to H32 were validated in 12 bread wheat cultivars and an elite breeding line, demonstrating the efficacy of these markers for marker‐assisted selection. Comparative mapping analysis indicated that H26 and H32 are either different alleles at the same gene locus or two different, but tightly linked H genes. Ongoing efforts to perform fine mapping and positional cloning of H26 will resolve the relationship between H26 and H32

Virulence of Hessian fly (Diptera: Cecidomyiidae) in the Fertile Crescent

AbstractThe Hessian fly, Mayetiola destructor (Say), is an important insect pest of wheat (Triticum spp.) in North Africa, North America, southern Europe and northern Kazakhstan. Both wheat and this pest are believed to have originated from West Asia in the Fertile Crescent. The virulence of a Hessian fly population from Syria against a set of cultivars carrying different resistance genes, in addition to other effective sources with unknown genes, was determined in the field and laboratory at the International Center for Agricultural Research in the Dry Areas (ICARDA) during the 2005/2006 cropping season. Only two resistance genes (H25 and H26) were effective against the Syrian Hessian fly population, making it the most virulent worldwide. This high virulence supports the hypothesis that Hessian fly coevolved with wheat in the Fertile Crescent of West Asia. The ICARDA screening programme is using this Hessian fly population to identify new resistance genes to this pest.

Virulence Analysis of Hessian Fly Populations From Texas, Oklahoma, and Kansas

In recent years, the number of wheat, Triticum aestivum L., fields heavily infested by Hessian fly, Mayetiola destructor (Say), has increased in the Great Plains of the United States. Historically, resistance genes in wheat have been the most efficient means of controlling this insect pest. To determine which resistance genes are still effective in this area, virulence of six Hessian fly populations from Texas, Oklahoma, and Kansas was determined, using the resistance genes H3, H4, H5, H6, H7H8, H9, H10, H11, H12, H13, H16, H17, H18, H21, H22, H23, H24, H25, H26, H31, and Hdic. Five of the tested genes, H13, H21, H25, H26, and Hdic, conferred high levels of resistance (> 80% of plants scored resistant) to all tested populations. Resistance levels for other genes varied depending on which Hessian fly population they were tested against. Biotype composition analysis of insects collected directly from wheat fields in Grayson County, TX, revealed that the proportion of individuals within this population virulent to the major resistance genes was highly variable (89% for H6, 58% for H9, 28% for H5, 22% for H26, 15% for H3, 9% for H18, 4% for H21, and 0% for H13). Results also revealed that the percentages of biotypes virulent to specific resistance genes in a given population are highly correlated (r2 = 0.97) with the percentages of susceptible plants in a virulence test. This suggests that virulence assays, which require less time and effort, can be used to approximate biotype composition.