Submitted to: The Plant Cell
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/26/2004
Publication Date: 8/19/2004
Citation: Caldo, R.A., Nettleton, D.A., Wise, R.P. 2004. Interaction-dependent gene expression in Mla-specified response to barley powdery mildew. The Plant Cell. 16:2514-2528.
Interpretive Summary: Plant defense to microbial attack is highly dependent upon recognition events involving associated gene products in the host and the pathogen. Both perception of general and specific pathogen-associated molecules result in signal transduction cascades ultimately leading to disease resistance. Although many studies have been conducted on plant perception of pathogen-derived molecules, the link between the recognition of general and specific elicitors in the expression of resistance and susceptibility remains poorly understood. From the analysis of 22,792 genes in parallel, this article describes, for the first time, the connection between the recognition of general elicitors and specific avirulence proteins in the expression of plant defense responses, supporting the hypothesis that host-specific resistance evolved from the recognition and prevention of the pathogen's suppression of plant basal defense. The research is of high impact because plant diseases are among the greatest impediments to crop production worldwide. Hence, major efforts have been devoted to understanding the mechanisms of genetic resistance and incorporating it into breeding programs to offset yield loss caused by pathogens. Knowledge of the basic mechanisms of disease resistance will provide breeders with better tools, resulting in less damage to crops, therefore, increasing sustainability and profitability.
Technical Abstract: Plant recognition of pathogen-derived molecules influences attack and counter-attack strategies that affect the outcome of host-microbe interactions. To ascertain the global framework of host gene expression during biotrophic pathogen invasion, we analyzed in parallel the mRNA abundance of 22,792 host genes throughout 36 (genotype x pathogen x time) interactions between barley (Hordeum vulgare) and Blumeria graminis f. sp. hordei (Bgh), the causal agent of powdery mildew disease. A split-split-plot design was used to investigate near-isogenic barley lines with introgressed Mla6, Mla13, and Mla1 CC-NBS-LRR resistance alleles challenged with Bgh isolates 5874 (AvrMla6, AvrMla1) and K1 (AvrMla13, AvrMla1). A linear mixed model analysis was employed to identify genes with significant differential expression (p-value<0.0001) in incompatible and compatible barley-Bgh interactions across six time points after pathogen challenge. Twenty-two host genes, of which five were of unknown function, exhibited highly similar patterns of up-regulation among all incompatible and compatible interactions up to 16 hours after inoculation (hai), coinciding with germination of Bgh conidiospores and formation of appressoria. In contrast, significant divergent expression was observed from 16 to 32 hai, during membrane-to-membrane contact between fungal haustoria and host epidermal cells, with notable suppression of most transcripts identified as differentially expressed in compatible interactions. These findings provide a link between the recognition of general and specific pathogen-associated molecules in gene-for-gene specified resistance and support the hypothesis that host-specific resistance evolved from the recognition and prevention of the pathogen's suppression of plant basal defense.