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Title: Lr34-mediated leaf rust resistance in wheat: transcript profiling reveals a high energetic demand supported by transient recruitment of multiple metabolic pathways

item Bolton, Melvin
item Kolmer, James - Jim
item Garvin, David

Submitted to: Molecular Plant-Microbe Interactions
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/18/2008
Publication Date: 11/1/2008
Citation: Bolton, M.D., Kolmer, J.A., Xu, W., Garvin, D.F. 2008. Lr34-Mediated Leaf Rust Resistance in Wheat: Transcript Profiling Reveals a High Energetic Demand Supported by Transient Recruitment of Multiple Metabolic Pathways. Molecular Plant-Microbe Interactions. 21(12):1515-1527.

Interpretive Summary: Leaf rust is a disease that reduces wheat yield and quality in nearly all places that this crop is grown, including the U.S. Many naturally occurring leaf rust resistance genes are available for wheat breeders to use for developing new varieties that resist this disease. Unfortunately, most of these genes rarely are able to provide resistance to leaf rust for more than a few years because new forms of the fungus causing leaf rust quickly appear and overcome them. A leaf rust resistance gene called Lr34 is unusual because in contrast to most other leaf rust resistance genes, it does provide long-lasting leaf rust resistance to wheat grown both in the U.S. and around the world. For this reason, the biological mechanisms that underpin the durability of Lr34 are of great interest because they may provide opportunities to greatly reduce damage from leaf rust and other diseases on wheat. In this study, wheat either with no leaf rust resistance gene, with Lr34, or with the more prototypical leaf rust gene Lr1 was exposed to leaf rust. Differences between the sets of genes that were turned on or off in each wheat were identified, providing an opportunity to examine how a wheat plant with Lr34 responds differently to leaf rust compared to wheat with Lr1. We were able to determine that a group of genes that support the production of energy needed by cells are turned on in wheat with Lr34 but not in wheat with Lr1. This indicates that the leaf rust resistance of Lr34 requires a large amount of cellular energy, and this feature distinguishes it from wheat with Lr1. Over time, the ability of plants with Lr34 to enhance energy production to support leaf rust resistance dissipates. This explains why wheat with Lr34 ultimately does show delayed leaf rust symptoms. Modification of wheat with genes that play a role in the action of Lr34 could translate into millions of dollars of additional profits for wheat growers due to reduced losses from leaf rust, as well as provide additional protection to the U.S. food supply.

Technical Abstract: The wheat gene Lr34 confers partial resistance to all races of Puccinia triticina, the causal agent of wheat leaf rust. However, the biological basis for the exceptional durability of Lr34 is unclear. We used the Affymetrix GeneChip Wheat Genome Array to compare transcriptional changes of wheat in a compatible interaction, an incompatible interaction conferred by the R-gene Lr1, and the race non-specific response conditioned by Lr34 3 and 7 days post inoculation (dpi) with P. triticina. Surprisingly, no differentially expressed genes were detected in Lr1 plants at either timepoint, while in the compatible interaction differentially expressed genes were detected only at 7 dpi. In contrast, differentially expressed genes were identified at both timepoints in Lr34 plants. At 3 dpi, up-regulated genes associated with Lr34-mediated resistance encode defense and stress-related proteins, secondary metabolism enzymes, and transcriptional regulation and cellular signaling proteins. Interestingly, coordinated up-regulation of genes in several metabolic pathways generally associated with anaerobic metabolism and oxygen deficiency stress response was detected. This indicates that the Lr34 resistance response imposes an extremely high energetic cost, leading to the induction of multiple metabolic responses to maintain cellular energy production. This response was not sustained at 7 dpi, suggesting that the high energy demand associated with Lr34 cannot be maintained over a prolonged period of time and may explain why Lr34 ultimately fails to inhibit the pathogen fully. Thus, at the molecular level, the modes of action of Lr34 and Lr1 are distinctly different, as predicted by their divergent resistance phenotypes.