Submitted to: Molecular Plant-Microbe Interactions
Publication Type: Peer reviewed journal
Publication Acceptance Date: 9/15/2007
Publication Date: 12/1/2007
Citation: Zhu, L., Liu, X., Liu, X., Jeannotte, R., Reese, J., Harris, M., Stuart, J., Chen, M. 2007. Hessian Fly (Mayetiola Destructor) Attack Causes Dramatic Shift in Carbon/Nitrogen Metabolism in Wheat. Molecular Plant-Microbe Interactions. 21:70-78. Interpretive Summary: The Hessian fly (Mayetiola destructor) is one of the most destructive insects of wheat. The insect is currently controlled almost exclusively by host plant resistance. The challenge for the host plant resistance strategy is that resistance conferred by R-genes is short lived, lasting for about 6 to 8 years. Therefore, new strategies with durability should be explored. To develop new strategies, we need to understand how the insect attacks wheat. This paper is towards understanding why some of the plants are resistant while others are susceptible to Hessian fly attack. We found that Hessian fly larvae can manipulate wheat to produce nutrition necessary for the insect growth and development in susceptible plants. Specifically, more sugars are converted into amino acids to provide a balanced nutrition for the insect. In the resistant plants, this conversion process is inhibited, resulting in larval death of the insect.
Technical Abstract: Carbon/nitrogen (C/N) metabolism and C/N allocation have an important implication in plant-insect interactions. Here we used the wheat-Hessian fly (HF) (Mayetiola destructor) system to analyze C/N metabolism in susceptible and resistant host plants. We found that the majority of genes involved in C/N metabolism were differentially regulated between susceptible and resistant plants, and that different C/N metabolites accumulated to different levels at the HF feeding site. In susceptible plants, the feeding site became a carbon-source sink and a center for conversion of carbon-containing compounds (C-compounds, consisting of carbon, hydrogen, and oxygen) into nitrogen-containing compounds (N-compounds). There was a 36% decrease in C-compounds and a 46% increase in N-compounds at the feeding site in susceptible plants. The C/N shift was achieved through coordinated regulation of genes in central metabolic pathways including glycolysis, tricarboxylic acid cycle, pentose phosphate pathway, urea cycle, and various pathways for amino acid synthesis. In resistant plants, the feeding site functioned like a nitrogen-source sink. The imported nitrogen in the form of asparagine may be converted into secondary metabolites toxic to insects and other phenylproponoids for cell wall strengthening. Our data suggest that the carbon-source sink and the conversion of C-compounds into N-compounds at the feeding site in susceptible plants may be a necessary condition for HF larvae to survive and develop, while the increase in phenylproponoids and other toxic secondary metabolites may be part of the resistance mechanism.