Exogenous Salicylic Acid Enhances the Resistance of Wheat Seedlings to Hessian Fly (Diptera: Cecidomyiidae) Infestation Under Heat Stress.

Heat stress exerts significant impact on plant-parasite interactions. Phytohormones, such as salicylic acid (SA), play important roles in plant defense against parasite attacks. Here, we studied the impact of a combination of heat stress and exogenous SA on the resistance of wheat (Triticum aestivum L.) plants to the Hessian fly [Mayetiola destructor (Say)]. We found that the wheat cultivar 'Molly', which contains the resistance gene H13, lost resistance to Hessian fly under heat stress (40°C for 3 and 6 h), and that exogenous application of SA on Molly seedlings right before heat stress can partially prevent the loss of resistance of Molly plants under heat conditions. Our findings have significant implications for understanding the dynamics of plant-insect interactions in the context of heat stress.

Impact of Transient Heat Stress on Polar Lipid Metabolism in Seedlings of Wheat Near-Isogenic Lines Contrasting in Resistance to Hessian Fly (Cecidomyiidae) Infestation.

Transient heat stress compromises resistance of host plants to Hessian fly, Mayetiola destructor (Say), and other biotic stresses. However, the mechanism for the loss of plant resistance under heat stress remains to be determined. In this study, we determined polar lipid profiles in control and Hessian fly-infested resistant and susceptible wheat seedlings with and without heat stress using an automated electrospray ionization tandem mass spectrometry analysis. Heat stress, alone or in combination with Hessian fly infestation, caused significant reduction in the abundance of total detected polar lipids and double bond index. Changes in lipid profiles in 'Molly' were similar to those in 'Newton' under heat stress. However, changes in lipid profiles in Molly were significantly different from those in Newton following Hessian fly infestation. The combination of heat stress and Hessian fly infestation resulted in unique lipid profiles in comparison with those in plants either treated with heat stress or infested with Hessian fly alone. In addition, a greater impact on lipid metabolism was observed in heat-stressed plants infested with Hessian fly than that in plants treated with either heat stress or Hessian fly alone. Our results suggest that changes in lipid metabolism caused by heat stress may be part of the metabolic pathways through which heat stress suppresses resistance of wheat plants to Hessian fly infestation.

Transient heat stress compromises the resistance of wheat (Poales: Poaceae) seedlings to Hessian fly (Diptera: Cecidomyiidae) infestation.

Heat stress exerts a profound impact on the resistance of plants to parasites. In this research, we investigated the impact of an acute transient heat stress on the resistance of the wheat line 'Molly,' which contains the R gene H13, to an avirulent Hessian fly (Mayetiola destructor (Say)) population. We found that a significant portion of Molly seedlings stressed at 40 degrees C for 6 h during or after the initial Hessian fly larval attack became susceptible to otherwise avirulent insects, whereas unstressed control plants remained 100% resistant. Specifically, 77.8, 73.3, 83.3, and 46.7% of plants heat stressed at 0, 6,12, and 24 h, respectively, after the initial larval attack became susceptible. Biochemical analysis revealed that heat stress caused a transient decrease in 12-oxo-phytodienoic acid, but an increase in salicylic acid accumulation in Molly plants. The change in phytohormones after heat stress and Hessian fly infestation was not observed in 'Newton,' a near-isogenic but Hessian fly susceptible wheat line. Instead, heat stress caused a relatively prolonged reduction in palmitoleic acid. The role of phytohormones in heat-induced loss of wheat resistance was discussed.

Rapid mobilization of membrane lipids in wheat leaf sheaths during incompatible interactions with Hessian fly.

Hessian fly (HF) is a biotrophic insect that interacts with wheat on a gene-for-gene basis. We profiled changes in membrane lipids in two isogenic wheat lines: a susceptible line and its backcrossed offspring containing the resistance gene H13. Our results revealed a 32 to 45% reduction in total concentrations of 129 lipid species in resistant plants during incompatible interactions within 24 h after HF attack. A smaller and delayed response was observed in susceptible plants during compatible interactions. Microarray and real-time polymerase chain reaction analyses of 168 lipid-metabolism-related transcripts revealed that the abundance of many of these transcripts increased rapidly in resistant plants after HF attack but did not change in susceptible plants. In association with the rapid mobilization of membrane lipids, the concentrations of some fatty acids and 12-oxo-phytodienoic acid (OPDA) increased specifically in resistant plants. Exogenous application of OPDA increased mortality of HF larvae significantly. Collectively, our data, along with previously published results, indicate that the lipids were mobilized through lipolysis, producing free fatty acids, which were likely further converted into oxylipins and other defense molecules. Our results suggest that rapid mobilization of membrane lipids constitutes an important step for wheat to defend against HF attack.

Impact of Heat Stress on Expression of Wheat Genes Responsive to Hessian Fly Infestation.

Heat stress compromises wheat (Triticum aestivium) resistance to Hessian fly (HF, Mayetiola destructor (Say)). This study aimed to investigate the impact of heat stress on transcript expression of wheat genes associated with resistance to HF infestation under normal and heat-stressed conditions. To this end, 'Molly', a wheat cultivar containing the resistance gene H13, was subjected to HF infestation, heat stress, and the combination of HF infestation and heat stress. Our RNA-Seq approach identified 21 wheat genes regulated by HF infestation under normal temperatures (18 °C) and 155 genes regulated by HF infestation when plants were exposed to 35 °C for 6 h. Three differentially expressed genes (DEGs) from the RNA-Seq analysis were selected to validate the gene function of these DEGs using the RT-qPCR approach, indicating that these DEGs may differentially contribute to the expression of wheat resistance during the early stage of wheat-HF interaction under various stresses. Moreover, the jasmonate ZIM domain (JAZ) gene was also significantly upregulated under these treatments. Our results suggest that the genes in heat-stressed wheat plants are more responsive to HF infestation than those in plants growing under normal temperature conditions, and these genes in HF-infested wheat plants are more responsive to heat stress than those in plants without infestation.

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.

Electrical penetration graph analysis of the feeding behavior of soybean aphids on soybean cultivars with antibiosis.

The soybean aphid, Aphis glycine Matsumura (Hemiptera: Aphididae), is a major pest of soybean. In the current study, we used the Electrical Penetration Graph technique to study feeding behavior of soybean aphids on antibiotic-resistant soybean lines KS1621, KS1613, and KS1642, and a susceptible soybean line, KS4202. We observed that soybean aphids spent significantly shorter periods of time in the sieve element phase but slightly more times in nonprobing phases in all three resistant lines than in the susceptible control. Our study suggests that resistance factors exist in the phloem of the resistant soybean lines, and that these lines may contain antixenosis in addition to antibiosis.

Differential accumulation of phytohormones in wheat seedlings attacked by avirulent and virulent Hessian fly (Diptera: Cecidomyiidae) larvae.

We analyzed the accumulation of six phytohormones and phytohormone-related compounds in a wheat, Triticum aestivium L., genotype, 'Molly', after attacks by avirulent and virulent Hessian fly, Mayetiola destructor (Say) (Diptera: Cecidomyiidae), larvae, respectively, and we examined the expression of genes in the jasmonic acid (JA) pathway by Northern blot analysis. Compared with uninfested plants, attacks by avirulent larvae resulted in increased accumulation of salicylic acid (SA) by 11.3- and 8.2-fold, 12-oxo-phytodienoic acid (OPDA) by 36.4-and 18.7-fold, 18:3 fatty acid by 4.5- and 2.2-fold, and 18:1 fatty acid by 1.8- and 1.9-fold at 24 and 72 h post-initial attack (hpia), respectively, but an 20% decrease in JA accumulation at 24 hpia at the attack site. Attacks by the virulent larvae did not affect the accumulation of SA, OPDA, and 18:3 and 18:1 fatty acids but dramatically increased the concentration of auxin (AUX) from undetectable in uninfested plants to 381.7 ng/g fresh weight at 24 hpia and 71.0 ng/g fresh weight at 72 hpia in infested plants. Transcript levels of genes encoding lipoxygenase 2, allene oxide synthase, and Arabidopsis storage protein 2 were increased after avirulent larval attacks but decreased after virulent larval attacks. Our results suggest that OPDA and SA may act together in wheat resistance to the Hessian fly, whereas AUX may play a role in the susceptibility of wheat plants. The increased OPDA accumulation after avirulent larval attacks was at least partially regulated through gene transcription.

Analyzing Molecular Basis of Heat-Induced Loss-of-Wheat Resistance to Hessian Fly (Diptera: Cecidomyiidae) Infestation Using RNA-Sequencing.

Heat stress compromises wheat resistance to Hessian fly (HF, Mayetiola destructor (Say)) (Diptera: Cecidomyiidae) infestation. The objective of this research is to analyze the molecular basis of heat-induced loss of wheat resistance to HF infestation using RNA Sequencing (RNA-seq). To this end, two resistant wheat cultivars 'Molly' and 'Caldwell' containing the resistance genes H13 and H6, respectively, were infested with an avirulent HF biotype GP and treated with different temperatures to examine the impact of heat stress on their resistance phenotypes. Tissue samples collected from HF feeding sites in Molly plants were subjected to RNA-seq analysis to determine the effect of heat stress on transcript expression of genes in wheat plants. Our results indicate that resistance to HF infestation in Caldwell is more sensitive to heat stress than that in Molly, and that heat stress down-regulates most genes involved in primary metabolism and biosynthesis of lignin and cuticular wax, but up-regulate most or all genes involved in auxin and 12-oxo-phytodienoic acid (OPDA) signaling pathways. Our results and previous reports suggest that heat stress may impair the processes in wheat plants that produce and mobilize chemical resources needed for synthesizing defensive compounds, weaken cell wall and cuticle defense, decrease OPDA signaling, but increase auxin signaling, leading to the suppressed resistance and activation of susceptibility.

Hessian fly (Mayetiola destructor) attack causes a dramatic shift in carbon and nitrogen metabolism in wheat.

Carbon and nitrogen (C/N) metabolism and allocation within the plant have important implications for plant-parasite interactions. Many plant parasites manipulate the host by inducing C/N changes that benefit their own survival and growth. Plant resistance can prevent this parasite manipulation. We used the wheat-Hessian fly (Mayetiola destructor) system to analyze C/N changes in plants during compatible and incompatible interactions. The Hessian fly is an insect but shares many features with plant pathogens, being sessile during feeding stages and having avirulence (Avr) genes that match plant resistance genes in gene-for-gene relationships. Many wheat genes involved in C/N metabolism were differentially regulated in plants during compatible and incompatible interactions. In plants during compatible interactions, the content of free carbon-containing compounds decreased 36%, whereas the content of free nitrogen-containing compounds increased 46%. This C/N shift was likely achieved through a coordinated regulation of genes in a number of central metabolic pathways, including glycolysis, the tricarboxylic acid cycle, and amino-acid synthesis. Our data on plants during compatible interactions support recent findings that Hessian fly larvae create nutritive cells at feeding (attack) sites and manipulate host plants to enhance their own survival and growth. In plants during incompatible interactions, most of the metabolic genes examined were not affected or down-regulated.

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.

Categories and inheritance of resistance to Russian wheat aphid (Homoptera: Aphididae) biotype 2 in a selection from wheat cereal introduction 2401.

The Russian wheat aphid, Diuraphis noxia (Kurdjumov) (Homoptera: Aphididae), is one of the most devastating insect pests of wheat (Triticum spp.) and barley (Hordeum spp.) in the world. Yield losses and control costs are valued at several hundred million dollars each year. The use of D. noxia-resistant cultivars is an ecologically, economically, and biologically sound method of managing this pest. Several D. noxia resistance (Dn) genes from wheat have been used to develop cultivars resistant to D. noxia. However, a new U.S. D. noxia biotype (biotype 2) in Colorado is virulent to all known Dn genes except the Dn7 gene from rye (Secale spp.). Hence, there is an immediate need to identify and characterize unique sources of D. noxia resistance to biotypes. In this article, we report resistance to D. noxia biotype 2, identified in a selection from wheat cereal introduction (CItr) 2401, that is controlled by two dominant genes. CItr2401 has a strong antibiosis effect that is exhibited as a reduced intrinsic rate of increase of D. noxia biotype 2. CItr2401 plants also exhibit tolerance to leaf rolling and chlorosis. No antixenosis was detected in CItr2401.

Gene expression of different wheat genotypes during attack by virulent and avirulent Hessian fly (Mayetiola destructor) larvae.

Wheat and its relatives possess a number of resistance (R) genes specific for the Hessian fly (HF) [Mayetiola destructor (Say)]. HF populations overcome R gene resistance by evolving virulence. Virulent HF larvae manipulate the plant to produce a nutritionally enhanced feeding tissue and, probably, also suppress plant defense responses. Using two wheat R genes, H9 and H13, and three HF strains (biotypes) differing in virulence for H9 and H13, we conducted a genome-wide transcriptional analysis of gene expression during compatible interactions with virulent larvae and incompatible interactions with avirulent larvae. During both types of interactions, a large number of genes (>1,000) showed alterations in gene expression. Analysis of genes with known functions revealed that major targets for differential regulation were genes that encoded defense proteins or enzymes involved in the phenylpropanoid, cell wall, and lipid metabolism pathways. A combination of the enhancement of antibiosis defense, the evasion of nutrient metabolism induction, and the fortification and expansion of the cell wall are likely the collective mechanism for host-plant resistance observed during incompatible interactions. To overcome this resistance, virulent larvae appeared to suppress antibiosis defense while inducing nutrient metabolism, weakening cell wall, and inhibiting plant growth.