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Expression of Hessian fly-responsive biomarker genes in Hessian fly-resistant Ae. tauschii accessions. Transcript levels of a) Hfr-1 (Hessian fly response gene 1), b) Hfr-3 (Hessian fly response gene 3), c) Cer4 (Fatty acyl CoA reductase), and d) Mds-1 (Mayetiola destructor susceptibility gene 1) quantified by qRT-PCR in infested and uninfested TA2473 (solid bar) and TA1651 (diagonal bar) lines at 1 and 3 DAH time-points. Values are plotted as the log fold-change of infested compared to uninfested control plants with standard error bars for 3 biological replicates. Statistically significant (p < 0.05) differences are indicated by '*' with linear fold-change values above each bar
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Background:
The Hessian fly (Mayetiola destructor), belonging to the gall midge family (Cecidomyiidae), is a devastating pest of wheat (Triticum aestivum) causing significant yield losses. Despite identification and characterization of numerous Hessian fly-responsive genes and associated biological pathways involved in wheat defense against this d...
Citations
... 24 Evaluation of the donor Ae. tauschii accessions, where the resistance genes were identified, found that plants used an TA1411 TA123 TA54 TA1465 TA1195 TA1464 TA1415 TA1191 TA1187 TA1390 TA1171 TA126 TA1153 TA74 TA1059 TA90 TA1108 TA1077 TA144 TA1459 TA10569 TA10629 TA10642 TA2035 TA2724 TA10574 TA10588 TA10634 TA2720 TA177 TA10916 TA2719 TA346 TA466 TA447 TA362 TA721 TA593 TA249 TA252 TA832 TA709 TA810 TA10884 TA10891 TA10889 TA1313 TA1315 TA792 TA921 TA877 TA145 TA1499 TA23 TA49 TA2892 TA48 TA6 early defense strategy consisting of the production of anti-feedant proteins (lectins), secondary metabolites (such as phenylpropanoids), and reactive oxygen species (ROS). 23 The ROS radicals may counter any larval degradation of plant cells and prevent the larva from establishing feeding sites, whereas secondary metabolites affect larval performance. The greenbug is a phloem-feeding insect pest of wheat commonly controlled with host plant resistance. ...
BACKGROUND
The wheat stem sawfly (WSS, Cephus cinctus) is a major pest of wheat (Triticum aestivum) and can cause significant yield losses. WSS damage results from stem boring and/or cutting, leading to the lodging of wheat plants. Although solid‐stem wheat genotypes can effectively reduce larval survival, they may have lower yields than hollow‐stem genotypes and show inconsistent solidness expression. Because of limited resistance sources to WSS, evaluating diverse wheat germplasm for novel resistance genes is crucial. We evaluated 91 accessions across five wild wheat species (Triticum monococcum, T. urartu, T. turgidum, T. timopheevii, and Aegilops tauschii) and common wheat cultivars (T. aestivum) for antixenosis (host selection) and antibiosis (host suitability) to WSS. Host selection was measured as the number of eggs after adult oviposition, and host suitability was determined by examining the presence or absence of larval infestation within the stem. The plants were grown in the greenhouse and brought to the field for WSS infestation. In addition, a phylogenetic analysis was performed to determine the relationship between the WSS traits and phylogenetic clustering.
RESULTS
Overall, Ae. tauschii, T. turgidum and T. urartu had lower egg counts and larval infestation than T. monococcum, and T. timopheevii. T. monococcum, T. timopheevii, T. turgidum, and T. urartu had lower larval weights compared with T. aestivum.
CONCLUSION
This study shows that wild relatives of wheat could be a valuable source of alleles for enhancing resistance to WSS and identifies specific germplasm resources that may be useful for breeding. © 2024 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.
... To overcome this barrier, we recently explored and documented the suitability of utilizing less complex genomes for undertaking functional characterization of candidate Hessian-fly-responsive genes [25][26][27]. The small grass species Brachypodium distachyon (Bd), or the purple false brome, is one such model genome with a small size (diploid, 355 Mb), short life cycle, and availability of genetic resources [28,29], besides serving as a model system for nonhost resistance for several pathogens [30] and insects [31]. ...
The Hessian fly is a destructive pest of wheat. Employing additional molecular strategies can complement wheat’s native insect resistance. However, this requires functional characterization of Hessian-fly-responsive genes, which is challenging because of wheat genome complexity. The diploid Brachypodium distachyon (Bd) exhibits nonhost resistance to Hessian fly and displays phenotypic/molecular responses intermediate between resistant and susceptible host wheat, offering a surrogate genome for gene characterization. Here, we compared the transcriptomes of Biotype L larvae residing on resistant/susceptible wheat, and nonhost Bd plants. Larvae from susceptible wheat and nonhost Bd plants revealed similar molecular responses that were distinct from avirulent larval responses on resistant wheat. Secreted salivary gland proteins were strongly up-regulated in all larvae. Genes from various biological pathways and molecular processes were up-regulated in larvae from both susceptible wheat and nonhost Bd plants. However, Bd larval expression levels were intermediate between larvae from susceptible and resistant wheat. Most genes were down-regulated or unchanged in avirulent larvae, correlating with their inability to establish feeding sites and dying within 4–5 days after egg-hatch. Decreased gene expression in Bd larvae, compared to ones on susceptible wheat, potentially led to developmentally delayed 2nd-instars, followed by eventually succumbing to nonhost resistance defense mechanisms.
... However, during compatible interactions, larvae inject salivary effector proteins (Chen et al. 2006) that alter the host plant physiology and suppress plant defense responses (Baluch et al. 2012). Susceptibility in the host plant is induced as early as 1 day after egg hatch (DAH) and is characterized by: (i) increased accumulation of susceptibility-related transcripts (Puthoff et al. 2005;Liu et al. 2013;Subramanyam et al. 2015); (ii) formation of a nutritive tissue rich in amino acids, proteins and sugars (Harris et al. 2006;Saltzmann et al. 2008;Subramanyam et al. 2015Subramanyam et al. , 2018; and (iii) increased cell wall permeability that facilitates diffusion of nutrients to the feeding sites (Williams et al. 2011;Nemacheck et al. 2019). Successful establishment of virulence allows the larvae (virulent) to develop and complete their life cycle while the susceptible (lacking H gene) host wheat is stunted (Byers and Gallun 1972). ...
Insect UDP-glycosyltransferases (UGTs) play an important role in detoxification of substrates such as plant allelochemicals, and cuticle formation by the process of glucosidation. Hessian fly ( Mayetiola destructor ), belonging to the order Diptera (Family: Cecidomyiidae), is a destructive pest of host wheat causing significant economic losses. In the current study, using the assembled genome, we identified thirteen genes in M. destructor that belong to the family of UGTs ( MdesUGT ). Expression profiling revealed differential expression of MdesUGT genes in Hessian fly feeding instars. Further, we report the molecular cloning of MdesUGT1 , designated as UGT301F1, from M. destructor . Characterization of the MdesUGT1 amino acid sequence revealed a conserved signature motif and sugar donor-binding domains characteristic of UGT proteins. Further expression analysis revealed dramatic increase in transcript accumulation of MdesUGT1 in the first and second feeding instars during compatible interactions (susceptible wheat, virulent larvae) but lacked significant upregulation during incompatible wheat Hessian fly interactions. Similar increase in MdesUGT1 transcripts was also observed during interactions of Hessian fly with nonhost, Brachypodium distachyon . These findings suggest the possible early involvement of MdesUGT1 in detoxification of plant toxins, and subsequent role in cuticular formation, thus contributing to the growth and development of this dipteran insect pest. Identification and characterization of insect UGTs could provide valuable insights into the detoxification and growth inhibitory mechanisms and facilitate future plant pest management strategies.
... The production of anti-feedant proteins (lectins), secondary metabolites and ROS radicals is involved in this strategy. These successfully counter the larval extra oral salivary plant cell degrading proteases, lead to fortification of the cell wall and prevention of the Hessian fly larvae from establishing permanent feeding sites [95]. ...
Wheat (T. aestivum) is one of the key food grain crops and is a prominent source of calories and proteins globally. In addition to mushrooming population and rising abiotic stresses in this ongoing climate change era, biotic stresses pose a great threat to wheat production over the globe. Fungal diseases such as rusts, mildew, along with pests like aphid, hinder the potential yield performance of the elite wheat cultivars to a huge extent. The complex nature of plant-parasite interactions is shown to be the decisive factor for the ultimate resistance expression in wheat. However, the advancement of molecular genetics and biotechnology enabled the replacement of the tedious, time and resource consuming cytogenetic analyses of locating APR and ASR genes using molecular mapping techniques. Continuous efforts have been made to mine resistance genes from diverse genetic resources such as wild relatives for combating these diseases and pests, which are repositories of R genes. Additionally, they offer a promising source of genetic variation to be introgressed and exploited for imparting biotic stress tolerance in cultivated wheat. Though just a handful of R-genes are cloned and molecularly characterized in wheat so far, more than 350 resistance genes for various diseases have been identified and successfully introgressed into elite varieties around the globe. Modern genomics and phenomic approaches coupled with next-generation sequencing techniques have facilitated the fine-mapping as well as marker aided selection of resistance genes for biotic stress resistance wheat breeding.
... The RNA preps were subjected to DNase-treatment using TURBO DNA-free kit (Invitrogen). cDNA for transcript quantification was generated by reverse transcription using random hexamers for Hessian fly larval samples 15 and oligo dT for plant samples 28 . Transcript profiling was undertaken using quantitative real-time reverse transcription PCR (qRT-PCR). ...
The Hessian fly is an obligate parasite of wheat causing significant economic damage, and triggers either a resistant or susceptible reaction. However, the molecular mechanisms of susceptibility leading to the establishment of the larvae are unknown. Larval survival on the plant requires the establishment of a steady source of readily available nutrition. Unlike other insect pests, the Hessian fly larvae have minute mandibles and cannot derive their nutrition by chewing tissue or sucking phloem sap. Here, we show that the virulent larvae produce the glycoside hydrolase MdesGH32 extra-orally, that localizes within the leaf tissue being fed upon. MdesGH32 has strong inulinase and invertase activity aiding in the breakdown of the plant cell wall inulin polymer into monomers and converting sucrose, the primary transport sugar in plants, to glucose and fructose, resulting in the formation of a nutrient-rich tissue. Our finding elucidates the molecular mechanism of nutrient sink formation and establishment of susceptibility.
... To determine if the epidermal cell wall integrity is disrupted by Hessian larval feeding on Kitaake seedling, the crown tissue (feeding site) was stained with neutral red (NR) as described in Nemacheck et al. (2019). Cell wall permeability was assessed in Biotype-L infested Kitaake seedlings at 1, 4, and 9 DAH time points. ...
... The susceptible plants have dark leaves and show stunted growth (Schmid et al. 2018). In contrast, although the leaves on Hessian fly-infested resistant host hexaploid and diploid wheats, and nonhost Bd, exhibit some measure of initial leaf stunting on leaves that are actively growing during larval feeding, once the larvae die, there is an accelerated growth of leaves which end up having the same leaf length as compared to the uninfested controls (Hargarten et al. 2017;Nemacheck et al. 2019). None of the four leaves in Kitaake seedlings exhibited the initial stunting observed in leaves of resistant host wheat and Bd nonhost plants, suggesting that there are no physical consequences to the Kitaake rice plants in response to attempted larval feeding. ...
... The epidermal cell wall layer is considered as the first line of plant defense against herbivory (Schönherr 1982;Javelle et al. 2011). Previous studies using neutral red, a stain that enters cuticular gaps or damaged cell walls and spreads mainly in the major vasculature (Joel and Juniper 1982), revealed a two-way exchange of molecules during host wheat-and nonhost Bd-Hessian fly interactions (Williams et al. 2011;Subramanyam et al. 2019;Nemacheck et al. 2019). The increased and sustained wall permeability in susceptible wheat has been attributed to the delivery of salivary effectors from the virulent Hessian fly larvae, altering host plant physiology and offering a nutrient-rich environment conducive to the developing larvae (Williams et al. 2011). ...
The Hessian fly causes severe economic losses in host wheat. The genome complexity of hexaploid wheat makes functional characterization of candidate defense genes extremely challenging. Kitaake rice, a model and simpler genome, exhibits responses resembling nonhost resistance to Hessian fly. Larvae feeding on Kitaake rice plants do not develop beyond first-instars similar to resistant host wheat, although, they show prolonged survival. Kitaake nonhost differs from nonhost Brachypodium, where some larvae develop into second-instars. Kitaake rice plants exhibit a molecular response similar to not only resistant but also susceptible host wheat for six Hessian fly-responsive biomarker genes assayed. Further, in Kitaake, lectins and secondary metabolites may play an important role in early defense preventing the larvae from developing. The phenotypic and molecular characterization of Kitaake rice reveals its suitability as a surrogate model genome for undertaking downstream functional genomics studies of candidate wheat genes that respond to Hessian fly larval attack.
Deploying resistant wheat cultivars is the most economical and environment‐friendly strategy to manage the devastating effects of the dipteran pest, Hessian fly (Hf; Mayetiola destructor ). Currently, 37 Hf resistance genes have been identified to combat the 18 Hf genotypes documented so far. However, the Hf populations adapt rapidly to overcome the newly deployed resistance genes within a few years of release resulting in development of virulent Hf biotypes and breakdown of plant resistance. Identification of new and novel sources of resistance offers breeders additional resources that can be included in the breeding programmes to develop elite Hf‐resistant cultivars. In the current study, we screened 374 wheat (tetraploid and hexaploid) accessions originating from different regions of the United States and identified three tetraploid ( Triticum turgidum ) pasta wheat lines, one originating from North Dakota (PI 639869) and two from Minnesota (PI 352398 and CItr 15710) exhibiting ≥95% resistance to Hf biotype L at 20°C. Further, the wheat cultivar PI 352398 showed 100% resistance to six additional Hf genotypes including biotypes B, C, D, O, GP and vH13 . The lines PI 639869 and CItr 15710 also showed >70% resistance with most biotypes, except against biotype GP with the former and biotype B with the latter. Interestingly, a few plants from these two cultivars exhibited putative tolerance to these biotypes where the plants showed normal growth but harboured white, live larvae and showed cell permeability that was intermediate in levels between Hf‐infested resistant and susceptible wheat. Additionally, since the increase in environmental temperatures to 25–30°C also negatively impacts Hf resistance, the three T. turgidum (PI 639869, PI 352398 and CItr 15710) cultivars were evaluated for Hf resistance at 30°C. None of the wheat cultivars were resistant to Hf biotype L at 30°C indicating a temperature‐dependent breakdown of resistance and are therefore not suitable for geographical regions with higher environmental temperatures. Taken together, these three wheat lines represent additional sources of Hf resistance that can be leveraged by breeders for developing durable elite lines.
Hessian fly (HF) (Mayetiola destructor Say) is an obligate destructive pest of wheat (Triticum aestivum L.) causing severe economic losses worldwide. Deployment of resistant wheat cultivars harboring HF resistance (H) genes is still the most effective and economical method to manage this insect pest. However, extensive use of H genes can impose selection pressure on HF populations, leading to the development of virulent biotypes that can breakdown plant resistance. Further, increase in environmental temperatures to 25–30°C during the wheat‐growing season can also negatively impact HF resistance, thereby necessitating the identification of new and novel sources of HF resistance and evaluate them for temperature sensitivity. In the current study, we evaluated the phenotypic response of 254 Triticum turgidum (L.) wheat accessions of African origin to Biotype L HF infestation. Of these, 10 accessions exhibited >70% resistance to Biotype L HF infestation. These 10 resistant accessions also showed >70% resistance when screened with vH13 HF biotype. Additionally, these HF resistant lines were evaluated for expression of resistance at a higher temperature of 30°C, and three tetraploid wheat accessions that maintained 100% resistance to Biotype L HF at the increased temperature were identified. These newly identified HF resistant lines offer valuable tools to breeders and farmers that can be used in breeding programs to develop cultivars for durable resistance to HF and efficient crop management.
Wild crop relatives are a very important genetic resource for introducing new diversity in the modern-day crop plants. Generation of synthetic hexaploid wheat (SHW) is one of the most successful strategy to use diversity of progenitor species of wheat. Ever since the independent introduction by Kihara (1944) and McFadden and Sears (1944), SHWs have proven to be one of the most valuable sources for the wheat improvement. Earlier studies focused on the extensive use of Ae. tauschii, the D genome donor of wheat, for SHW generation. But use of other progenitor and non-progenitor species for synthetic wheat generation is now well documented in the literature. Although SHWs have been developed in different institutions, CIMMYT is actively involved in the development and distribution of SHWs and synthetic-derived lines (SDLs) all over the world. The novel allelic variants from SHWs and SDLs have imparted resistance to various biotic and abiotic stresses along with improvement of different quality traits. Due to the immense potential, 86 SHWs and SDLs derived varieties have been released in 20 countries with maximum adoption rate in southwest China and India. Due to the higher yield potential of these varieties along with resistance to pests and pathogens and their good quality attributes, the contribution of SHW and SDLs is expected to increase further in the wheat cropping systems worldwide.KeywordsWheat progenitorsSynthetic wheat
Aegilops tauschii
Biotic stress toleranceAbiotic stress tolerance
