Rapid Mobilization of Membrane Lipids in Wheat Leaf Sheaths During Incompatible Interactions with Hessian Fly

Department of Biological Science, Fayetteville State University, Fayetteville, NC 28301, USA.
Molecular Plant-Microbe Interactions (Impact Factor: 3.94). 07/2012; 25(7):920-30. DOI: 10.1094/MPMI-01-12-0022-R
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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.

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    • "44, no. 3 scale of attack by tiny mandibles, individual epidermal cells as the focus of attack, and a strategy of ETS, as well as being the target of the plant's ETI. Likewise, plant responses to Hessian fly and pathogens share features , including gene-for-gene plant resistance, subcellular features of penetration resistance (Harris et al. 2010), and the production of reactive oxygen species and materials for remodeling and strengthening the cell wall (Kosma et al. 2010, Liu et al. 2010, Williams et al. 2011, Zhu et al. 2012, Khajuria et al. 2013). However , contrary to the expectation that costs associated with defense would increase photosynthesis (Schultz et al. 2013), attack of resistant plants by avirulent pathogens has often been shown to decrease photosynthesis and this is also the case for attack by virulent pathogens (Göhre et al. 2012). "
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    ABSTRACT: Gall-inducing insects are known for altering source-sink relationships within plants. Changes in photosynthesis may contribute to this phenomenon. We investigated photosynthetic responses in wheat [Triticum aestivum L. (Poaceae: Triticeae)] seedlings attacked by the Hessian fly [Mayetiola destructor (Say) (Diptera: Cecidomyiidae], which uses a salivary effector-based strategy to induce a gall nutritive tissue in susceptible plants. Resistant plants have surveillance systems mediated by products of Resistance (R) genes. Detection of a specific salivary effector triggers downstream responses that result in a resistance that kills neonate larvae. A 2 × 2 factorial design was used to study maximum leaf photosynthetic assimilation and stomatal conductance rates. The plant treatments were-resistant or susceptible wheat lines expressing or not expressing the H13 resistance gene. The insect treatments were-no attack (control) or attack by larvae killed by H13 gene-mediated resistance. Photosynthesis was measured for the second and third leaves of the seedling, the latter being the only leaf directly attacked by larvae. We predicted effector-based attack would trigger increases in photosynthetic rates in susceptible but not resistant plants. For susceptible plants, attack was associated with increases (relative to controls) in photosynthesis for the third but not the second leaf. For resistant plants, attack was associated with increases in photosynthesis for both the second and third leaves. Mechanisms underlying the increases appeared to differ. Resistant plants exhibited responses suggesting altered source-sink relationships. Susceptible plants exhibited responses suggesting a mechanism other than altered source-sink relationships, possibly changes in water relations that contributed to increased stomatal conductance.
    Environmental Entomology 06/2015; 44(3). DOI:10.1093/ee/nvv028 · 1.30 Impact Factor
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    • "Both responses have also been observed in plants exhibiting penetration resistance to fungi (An et al., 2006; Hückelhoven, 2007). A number of biochemical changes are associated with gene-for-gene resistance to the Hessian fly, including the production of toxins (Subramanyam et al., 2006, 2008), reactive oxygen species (Liu et al., 2010), and materials for remodelling and strengthening the cell wall (Kosma et al., 2010; Williams et al., 2011; Zhu et al., 2012; Khajuria et al., 2013). "
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    ABSTRACT: In this review, we argue for a research initiative on wheat's responses to biotic stress. One goal is to begin a conversation between the disparate communities of plant pathology and entomology. Another is to understand how responses to a variety of agents of biotic stress are integrated in an important crop. We propose gene-for-gene interactions as the focus of the research initiative. On the parasite's side is an Avirulence (Avr) gene that encodes one of the many effector proteins the parasite applies to the plant to assist with colonization. On the plant's side is a Resistance (R) gene that mediates a surveillance system that detects the Avr protein directly or indirectly and triggers effector-triggered plant immunity. Even though arthropods are responsible for a significant proportion of plant biotic stress, they have not been integrated into important models of plant immunity that come from plant pathology. A roadblock has been the absence of molecular evidence for arthropod Avr effectors. Thirty years after this evidence was discovered in a plant pathogen, there is now evidence for arthropods with the cloning of the Hessian fly's vH13 Avr gene. After reviewing the two models of plant immunity, we discuss how arthropods could be incorporated. We end by showing features that make wheat an interesting system for plant immunity, including 479 resistance genes known from agriculture that target viruses, bacteria, fungi, nematodes, insects, and mites. It is not likely that humans will be subsisting on Arabidopsis in the year 2050. It is time to start understanding how agricultural plants integrate responses to biotic stress. © The Author 2014. Published by Oxford University Press on behalf of the Society for Experimental Biology. All rights reserved. For permissions, please email:
    Journal of Experimental Botany 12/2014; 66(2). DOI:10.1093/jxb/eru465 · 5.53 Impact Factor
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    • "Exogenous application of SA partially prevented the loss of the resistance in Molly plants to Hessian ßy infestation under acute, transient heat stress. As a signal molecule, SA enhances plant performance in responses to both biotic and abiotic stresses (Mandal et al. 2009, Vlot et al. 2009, Zhu et al. 2012). Exogenous application of SA led to increased transcript level of many defenserelated genes including LOX genes encoding lipoxygenase (Zhu-Salzman et al. 2004) in the jasmonic acid (JA) pathway. "
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    ABSTRACT: Resistance of plants to parasites is heavily impacted by environmental factors. In this study, we analyzed the survival and development of an avirulent Hessian fly (HF), Mayetiola destructor (Say), population ‘White eye’ on a resistant wheat cultivar ‘Molly’, and a susceptible cultivar ‘Newton’ exposed to varying periods of 40ºC heat stress. We observed that Molly began to lose resistance when subjected to 3 h heat stress, and the loss of resistance increasingly continued with 6 h of heat stress. When 2 mM salicylic solution (SA) was applied to Molly foliage before heat stress, more plants maintained their resistance than plants without SA application. Our results indicate that short periods of heat stress decreases the effectiveness of wheat resistance against Hessian fly infestation, but the application of SA significantly restores resistance in plants under heat stress.
    Entomological Society of America Annual Meeting 2013; 11/2013
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