Biotype composition of Hessian fly (Diptera: Cecidomyiidae) populations from the southeastern, midwestern, and northwestern United States and virulence to resistance genes in wheat

Twenty-three Hessian fly, Mayetiola destructor (Say), populations collected in the southeastern (Alabama and Mississippi), midwestern (Indiana), and northwestern (Idaho and Washington) United States from 1995 to 1999 were evaluated for biotype composition based on response to Hessian fly resistance genes H3, H5, H6, and H7H8 in wheat, Triticum aestivum L. Biotypes L and O, combined, made up at least 60% of all Alabama populations. Biotype L was predominant in the northern third of Alabama and biotype O in the southern two-thirds of the state. Based on biotype data, wheat cultivars with H7H8 resistance should be highly effective in central and southern Alabama. Fifty-four percent of the Mississippi population consisted of biotype L, and the remaining virulent biotypes (B, D, E, G, J, and O) ranged in frequency from 1 to 17%. The Mississippi population also contained 4% of the avirulent biotype GP. Only biotypes D and L were found in Indiana populations, but biotype L was predominant. Hessian fly populations from Idaho and Washington contained one or more of the virulent biotypes D-H, J, and L-O; however, only biotypes E, F, and G occurred at frequencies > 12%. The avirulent biotype GP made up 25-57% of Idaho and Washington populations, a much higher percentage than found in populations from the eastern United States. Although the highest level of virulence in Idaho and Washington populations was found to resistance genes H3 and H6, the frequency of biotype GP would indicate that the currently deployed gene H3 would provide a moderate to high level of resistance, depending on location. Nine of the populations, plus populations collected from the mid-Atlantic state area in 1989 and 1996, also were tested against the wheat cultivar 'INW9811' that carries H13 resistance to Hessian fly biotype L and two Purdue wheat lines with unidentified genes for resistance. The H13 resistance in INW9811 was highly effective against all populations tested from the eastern and northwestern U.S. wheat production areas, except Maryland and Virginia. Population studies also indicated that wheat line CI 17960-1-1-2-4-2-10 likely carries the H13 resistance gene, based on the similarity of its response and that of INW9811 to eight fly populations. Continued monitoring of biotype frequency in Hessian fly populations is required for optimal deployment and management of resistance genes in all wheat production areas.     

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.     

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

The 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.     

Characterization of Wheat Random Amplified Polymorphic DNA Markers Associated with the H11 Hessian Fly Resistance Gene

In Tunisia, the Hessian fly Mayetiola destructor Say is a major pest of durum wheat （Triticum durum Desf.） and bread wheat （T. aestivum L.）. Genetic resistance is the most efficient and economical method of control of this pest. To date, 31 resistance genes, designated H1-H31, have been identified in wheat. These genes condition resistance to the insect genes responsible for virulence. Using wheat cultivars differing for the presence of an individual Hessian fly resistance gene and random amplified polymorphic DNA （RAPD） analysis, we have identified a polymorphic 386-bp DNA marker （Xgmib1-1A.1） associated with the H11 Hessian fly resistance gene. Blast analysis showed a high identity with a short region in the wild wheat （T. monococcum） genome, adjacent to the leaf rust resistance Lr10 gene. A genetic linkage was reported between this gene （Lr10） and Hessian fly response in wheat. These data were used for screening Hessian fly resistance in Tunisian wheat germplasm. Xgmib1-1A.1-like fragments were detected in four Tunisian durum and bread wheat varieties. Using these varieties in Hessian fly breeding programs in Tunisia would be of benefit in reducing the damage caused by this fly.     

Distribution,population dynamics and damage of Hessian fly,Mayetiola destructor (Diptera: Cecidomyiidae) in North Tunisia

A three years survey and monitoring studies (2013–2014–2015) were carried out through 4 regions of north Tunisia in order to follow the evolution of the distribution, the frequency of occurrence and damage caused by the Hessian fly Mayetiola destructor (Say) to bread wheat (Triticum aestivum L.) and durum wheat (Triticum durum Desf). Moreover, the effectiveness of resistance genes H3, H5, H6, H7, H8, H9, H10, H11, H12, H13, H14, H15, H22, H23, H25 and H26 to protect wheat from Hessian fly attack was assessed in natural field and under controlled laboratory conditions at INRAT-Kef Station. Results showed that Hessian fly was detected in 60.33% and 51.5% of all sampled durum and bread wheat fields, respectively. This pest was more frequent with a higher percentage of infestation in semi-arid regions. Indeed, during 2013, infestation rate attained 12.39% in Kef region against 0.9% registered in Bizerte region. In order to update information about the annual number of generations, we surveyed the population dynamic of Hessian fly in Kef region. Three generations of the fly were counted annually on wheat, with two complete and one incomplete generation. This insect affects host plant growth at different developmental stages. Plant height was the most affected parameter followed by shoot dry weight and tiller number. Field investigations on host resistance revealed that among the 16 tested resistance genes, and only three were strictly effective (H22, H25 and H26). The resistance genes H5, H9, H13 and H9H13 have also conferred high levels of protection against Hessian fly. This work indicated that H22, H25 and H26 genes could be incorporated into Tunisian wheat varieties and released to farmers to manage the threat due to Hessian fly attacks.     

Biotypes of Hessian fly (Dipt., Cecidomyiidae) in Morocco

Hessian fly, Mayetiola destructor (Say), is the most important insect pest of wheat in Morocco, where host plant resistance has been used successfully for control. Our objective was to determine the frequency of Hessian fly virulence on H5, H13 and H22 resistance genes. Five Hessian fly populations from the principal cereal‐growing regions in Morocco were studied. The variability in percentage of susceptible plants across Hessian fly populations was highly significant (P < 0.01), indicating differences in virulence frequencies. Plants with the H13 gene had the lowest percentage of susceptible plants, 1.77 and 1.51%, when infested with Hessian flies from Fes and Marchouch, respectively. A low level of virulence to H22 was detected in Fes, Abda and Marchouch populations, 1.87, 1.54 and 1.99% susceptible plants, respectively. The level of virulence to H5 was low in all the five populations. The Beni Mellal population gave the highest percentage of susceptible plants carrying H13 and H22 genes, 6.43 and 7.28%, respectively. The size of live larvae on susceptible plants of the three cultivars carrying H5, H13 and H22 was similar to that of the susceptible check, indicating that a true virulence (biotype) is developing in Hessian fly populations in Morocco. Thus, continuous monitoring of the development of Hessian fly biotypes is essential for optimal deployment of resistance genes.     

Does R gene resistance allow wheat to prevent plant growth effects associated with Hessian fly (Diptera: Cecidomyiidae) attack?

Resistance genes (R genes) are an important part of the plant's immune system. Among insects, the Hessian fly, Mayetiola destructor (Say) (Diptera: Cecidomyiidae), larva is the target of the greatest number of characterized R genes (H1-H32). The biochemical/molecular mechanism of R gene resistance to Hessian fly is not well understood. In the absence of an effective R gene, larvae caused extensive growth deficits (> 30 cm) in wheat seedlings. In the presence of one of three effective R genes, H6, H9, or H13, larvae caused small growth deficits (approximately 3-4 cm) in two leaves (third and fourth) that were actively growing during the first days of larval attack. After larvae died on R gene plants, the fifth leaf and tiller leaves exhibited small increases in growth (2-4 cm). Growth responses of susceptible and resistant plants diverged at a time when Hessian fly larvae were establishing a nutritive gall tissue at feeding sites. The results of this study support the hypothesis that R gene resistance cannot prevent initial larval attack, but, by stopping the formation of the larval gall, it prevents the most serious consequences of larval attack.     

Association of a DNA marker with Hessian fly resistance gene H9 in wheat

The Hessian fly [Mayetiola destructor (Say)] is a major pest of wheat (Triticum aestivum L.) and genetic resistance has been used effectively over the past 30 years to protect wheat against serious damage by the fly. To-date, 25 Hessian fly resistance genes, designated H1 to H25, have been identified in wheat. With near-isogenic wheat lines differing for the presence of an individual Hessian fly resistance gene, in conjunction with random amplified polymorphic DNA (RAPD) analysis and denaturing gradient-gel electrophoresis (DGGE), we have identified a DNA marker associated with the H9 resistance gene. The H9 gene confers resistance against biotype L of the Hessian fly, the most virulent biotype. The RAPD marker cosegregates with resistance in a segregating F₂ population, remains associated with H9 resistance in a number of different T. aestivum and T. durum L. genetic backgrounds, and is readily detected by either DGGE or DNA gel-blot hybridization.Purdue University, Agric. Exp. Stn. Journal paper No. 14440     

Molecular genetic mapping of three X-linked avirulence genes, vH6, vH9 and vH13, in the Hessian fly.

Three X-linked avirulence genes, vH6, vH9, and vH13 in the Hessian fly, Mayetiola destructor, confer avirulence to Hessian fly resistance genes H6, H9, and H13 in wheat. We used a combination of two- and three-point crosses to determine the order of these genes with respect to each other, the white eye mutation and three X-linked molecular markers, G15-1, 020, and 021, developed from genomic lambda clones, lambda G15-1, lambda 020, and lambda 021. The gene order was determined to be vH9-vH6-G15-1-w-vH13-020-021. In situ hybridization of lambda G15-1, lambda 020, and lambda 021, on the polytene chromosomes of the Hessian fly salivary gland established their orientation on Hessian fly chromosome X1. Based on the size of the Hessian fly genome, and the genetic distances between markers, the relationship of physical to genetic distance was estimated at no more than 300 kb/cM along Hessian fly chromosome X1, suggesting that map-based cloning of these avirulence genes will be feasible.     

Genotypic interaction between resistance genes in wheat and virulence genes in the Hessian fly Mayetiola destructor (Diptera: Cecidomyiidae)

The genotypic interaction between wheat resistance genes H3, H6, H7H8, H9 and virulence genes vH3, vH6, vH7vH8, vH9 of Hessian fly, Mayetiola destructor (Say), was studied in a growth chamber. Results showed that plants homozygous and heterozygous for the H3 gene expressed a high level of resistance against homozygous avirulent and heterozygous larvae carrying the vH3 virulence allele. The H7H8 genes were highly effective in the homozygous condition, but displayed a reduced level of resistance in the heterozygous condition. The H6 and H9 genes showed different levels of resistance against the reciprocal heterozygous larvae (vH6(a)vH6(A) versus vH6(A)vH6(a) and vH9(a)vH9(A) versus vH9(A)vH9(a)). Adults reared from vH6(a)vH6(A) and vH9(a)vH9(A) larvae were all males, consistent with the vH6 and vH9 X-linkage. Plants homozygous for H3, H6, H7H8, and H9 allowed for greater larval survival of heterozygous larvae, which suggests that avirulence to these resistance genes is incompletely dominant. Greater survival of homozygous avirulent larvae on heterozygous plants (H3h3, H6h6, H7h7H8h8, H9h9) suggests incomplete dominance of these wheat genes. Survival of heterozygous along with homozygous virulent larvae would reduce selection pressure for virulence in Hessian fly populations infesting fields of resistant wheat cultivars. This would be expected to slow the increase in frequency of virulence alleles that often results from deployment of resistant cultivars.     

Identification of RAPD markers for 11 Hessian fly resistance genes in wheat

 The pyramiding of genes that confer race- or biotype-specific resistance has become increasingly attractive as a breeding strategy now that DNA-based marker-assisted selection is feasible. Our objective here was to identify DNA markers closely linked to genes in wheat (Triticum aestivum L.) that condition resistance to Hessian fly [Mayetiola destructor (Say)]. We used a set of near-isogenic wheat lines, each carrying a resistance gene at 1 of 11 loci (H3, H5, H6, H9, H10, H11, H12, H13, H14, H16 or H17) and developed by backcrossing to the Hessian fly-susceptible wheat cultivar ‘Newton’. Using genomic DNA of these 11 lines and ‘Newton’, we have identified 18 randomly amplified polymorphic DNA (RAPD) markers linked to the 11 resistance genes. Seven of these markers were identified by denaturing gradient gel electrophoresis and the others by agarose gel electrophoresis. We confirmed linkage to the Hessian fly resistance loci by cosegregation analysis in F₂ populations of 50–120 plants for each different gene. Several of the DNA markers were used to determine the presence/absence of specific Hessian fly resistance genes in resistant wheat lines that have 1 or possibly multiple genes for resistance. The use of RAPD markers presents a valuable strategy for selection of single and combined Hessian fly resistance genes in wheat improvement. Received: 20 March 1996 / Accepted: 6 September 1996     

No fitness cost for wheat's H gene-mediated resistance to Hessian fly (Diptera: Cecidomyiidae)

Resistance (R) genes have a proven record for protecting plants against biotic stress. A problem is parasite adaptation via Avirulence (Avr) mutations, which allows the parasite to colonize the R gene plant. Scientists hope to make R genes more durable by stacking them in a single cultivar. However, stacking assumes that R gene-mediated resistance has no fitness cost for the plant. We tested this assumption for wheat's resistance to Hessian fly, Mayetiola destructor (Say) (Diptera: Cecidomyiidae). Our study included ten plant fitness measures and four wheat genotypes, one susceptible, and three expressing either the H6, H9, or H13 resistance gene. Because R gene-mediated resistance has two components, we measured two types of costs: the cost of the constitutively-expressed H gene, which functions in plant surveillance, and the cost of the downstream induced responses, which were triggered by Hessian fly larvae rather than a chemical elicitor. For the constitutively expressed Hgene, some measures indicated costs, but a greater number of measures indicated benefits of simply expressing the H gene. For the induced resistance, instead of costs, resistant plants showed benefits of being attacked. Resistant plants were more likely to survive attack than susceptible plants, and surviving resistant plants produced higher yield and quality. We discuss why resistance to the Hessian fly has little or no cost and propose that tolerance is important, with compensatory growth occurring after H gene-mediated resistance kills the larva. We end with a caution: Given that plants were given good growing conditions, fitness costs may be found under conditions of greater biotic or abiotic stress.     

Chromosome landing near avirulence gene vH13 in the Hessian fly.

AFLP markers in linkage disequilibrium with vH13, an avirulence gene in the Hessian fly (Mayetiola destructor) that conditions avirulence to resistance gene H13 in wheat (Triticum spp.), were discovered by bulked segregant analysis. Five AFLPs were converted into codominant site-specific markers that genetically mapped within 13 cM of this gene. Flanking markers used as probes positioned vH13 near the telomere of the short arm of Hessian fly chromosome X2. These results suggest that the X-linked avirulence genes vH6, vH9, and vH13 are present on Hessian fly chromosome X2 rather than on chromosome X1 as reported previously. Genetic complementation demonstrated that recessive alleles of vH13 were responsible for the H13-virulence observed in populations derived from four different states in the U.S.A.: Georgia, Maryland, Virginia, and Washington. Results support the hypothesis that a gene-for-gene interaction exists between wheat and Hessian fly.     

Ultrastructural changes in the midguts of Hessian fly larvae feeding on resistant wheat

The focus of the present study was to compare ultrastructure in the midguts of larvae of the Hessian fly, Mayetiola destructor (Say), under different feeding regimens. Larvae were either fed on Hessian fly-resistant or -susceptible wheat, and each group was compared to starved larvae. Within 3 h of larval Hessian fly feeding on resistant wheat, midgut microvilli were disrupted, and after 6 h, microvilli were absent. The disruption in microvilli in larvae feeding on resistant wheat were similar to those reported for midgut microvilli of European corn borer, Ostrinia nubilasis (Hubner), larvae fed a diet containing wheat germ agglutinin. Results from the present ultrastructural study, coupled with previous studies documenting expression of genes encoding lectin and lectin-like proteins is rapidly up-regulated in resistant wheat to larval Hessian fly, are indications that the midgut is a target of plant resistance compounds. In addition, the midgut of the larval Hessian fly is apparently unique among other dipterans in that no peritrophic membrane was observed. Ultrastructural changes in the midgut are discussed from the prospective of their potential affects on the gut physiology of Hessian fly larvae and the mechanism of antibiosis in the resistance of wheat to Hessian fly attack.     

First combined resistance to Hessian fly and Sunn pest identified in synthetic hexaploid wheat

Hessian fly, Mayetiola destructor (Say), and Sunn pest, Eurygaster integriceps (Puton), are the two most damaging insect pests of wheat in North Africa, West and Central Asia. Host plant resistance is the most environmental friendly, cost-effective and practical means of controlling insect pests. Twenty synthetic hexaploid wheat lines selected as resistant to Syrian Sunn pest in 2010 were screened for resistance to Moroccan Hessian fly biotype in 2016. The Hessian fly screening was carried out in standard greenhouse flats using a randomized complete block design with three replications, with susceptible and resistant checks in every test flat. The results showed that three synthetic hexaploid wheat lines exhibited resistance to both Moroccan Hessian fly biotype and Syrian Sunn pest. This is the first record of combined resistance to these two pests in wheat. Mapping populations using these sources of resistance are being developed using double haploid techniques for subsequent genetic characterization and identification of linked molecular markers for marker assisted selection.     

Phenotypic assessment and mapped markers for<Emphasis Type="Italic"> H31,</Emphasis> a new wheat gene conferring resistance to Hessian fly (Diptera: Cecidomyiidae)

A new source of resistance to the highly virulent and widespread biotype L of the Hessian fly, Mayetiola destructor (Say), was identified in an accession of tetraploid durum wheat, Triticum turgidum Desf., and was introgressed into hexaploid common wheat, Triticum aestivum L. Genetic analysis and deletion mapping revealed that the common wheat line contained a single locus for resistance, H31, residing at the terminus of chromosome 5BS. H31 is the first Hessian fly-resistance gene to be placed on 5BS, making it unique from all previously reported sources of resistance. AFLP analysis identified two markers linked to the resistance locus. These markers were converted to highly specific sequence-tagged site markers. The markers are being applied to the development of cultivars carrying multiple genes for resistance to Hessian fly biotype L in order to test gene pyramiding as a strategy for extending the durability of deployed resistance.Communicated by J. Dvorak     

Changes in phytohormones and fatty acids in wheat and rice seedlings in response to Hessian fly (Diptera: Cecidomyiidae) infestation

Phytohormones and fatty acids (FAs) play important roles in plant resistance to insects and pathogens. In this study, we investigated the similarities and differences in the accumulations of phytohormones and FAs in the resistant wheat (Triticum aestivum L.) 'Molly' and the nonhost rice (Oryza sativa L.) 'Niponbare' in responses to Hessian fly, Mayetiola destructor (Say) (Diptera: Cecidomyiidae), larval attacks. Using chemical ionization-gas-chromatography/mass spectrometry, we analyzed the concentrations of 13 phytohomones and FAs at the attack site of wheat and rice plants at 1, 6, 24, or 48 h after the initial attack. Hessian fly attack resulted in increases of salicylic acid (SA), 12-oxo-phytodienoic acid (OPDA), palmitic acid (FA16:0), but a decrease of abscisic acid in both wheat and rice plants. In addition, the accumulation of jasmonic acid (JA) increased, whereas the accumulation of cinnamic acid (CA) decreased in wheat plants, but no changes were observed in the accumulation of JA, and the accumulation of CA increased in rice plants after Hessian fly attack. However, the accumulations of benzoic acid, strearic acid (FA18:0), and oleic acid (FA18:1) increased in rice plants, but no changes were observed in wheat plants after Hessian fly attack. Hessian fly-induced changes were more rapid in wheat plants in comparison with those in rice plants. Our study suggests that SA and OPDA may be involved in resistance of wheat and rice plants to Hessian fly and that the R gene-mediated resistance responses are more rapid than nonhost resistance responses.     

A new Hessian fly resistance gene (<Emphasis Type="Italic">H</Emphasis>30) transferred from the wild grass <Emphasis Type="Italic">Aegilops triuncialis</Emphasis> to hexaploid wheat

A new Hessian fly (Mayetiola destructor Say) resistance gene from Aegilops triuncialis and its transfer to hexaploid wheat via interspecific hybridisation is described. The transfer line TR-3531 (42 chromosomes), derived from the cross [(Triticum turgidum x Ae. triuncialis) x Triticum aestivum] and carrying the Heterodera avenae resistance gene Cre7, showed a high level of resistance to the M. destructor biotype prevailing in the SW of Spain. A single dominant gene (H30) seems to determine the Hessian fly resistance in this introgression line, and its linkage with an isozyme marker (Acph-U1) has also been studied. It has been demonstrated that the resistance gene H30 in the TR-3531 line is non-allelic with respect to the genes H3, H6, H9, H11, H12, H13, H18 and H21, present in wheat cultivars from the Uniform Hessian Fly Nursery (UHFN), as well as to H27, carried by the introgression line H-93-33. Advanced lines with the H30 gene were obtained by backcrossing the transfer line and different commercial wheats as recurrent parents. Several of them showed a high yield in tests carried out in the infested field. Electronic Supplementary Material is available if you access this article at http://dx.doi.org/10.1007/s00122-002-1182-z. On that page (frame on the left side), a link takes you directly to the supplementary material.     

Saturation and comparative mapping of the genomic region harboring Hessian fly resistance gene H26 in wheat

Resistance gene H26, derived from Aegilops tauschii Coss., is one of the most effective R genes against the Hessian fly [Mayetiola destructor (Say)], an important pest of wheat (Triticum aestivum L.). Using a limited number of PCR-based molecular markers a previous study mapped H26 to the wheat chromosomal deletion bin 3DL3-0.81-1.00. The objectives of this study were to saturate the chromosomal region harboring H26 with newly developed PCR-based markers and to investigate the collinearity of this wheat chromosomal region with rice (Oryza sativa L.) and Brachypodium distachyon genome. A population of 96 F₂ individuals segregating at the H26 gene locus was used for saturation mapping. All wheat ESTs assigned to the deletion bin 3DL3-0.81-1.00 were used to design STS (sequence tagged site) primers. The wheat ESTs mapped near H26 were further used to BLAST rice and B. distachyon genomic sequences for comparative mapping. To date, 26 newly developed STS markers have been mapped to the chromosomal region spanning the H26 locus. Two of them were mapped 1.0 cM away from the H26 locus. Comparative analysis identified genomic regions on rice chromosome 1 and Brachypodium Super contig 13 which are collinear with the genomic region spanning the H26 locus within the distal region of 3DL. The newly developed STS markers closely linked to H26 will be useful for mapped-based cloning of H26 and marker-assisted selection of this gene in wheat breeding. The results will also enhance understanding of this chromosomal region which contains several other Hessian fly resistance genes. Mention of trade names or commercial products in this article is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the U.S. Department of Agriculture.