Submitted to: PLoS Genetics
Publication Type: Peer reviewed journal
Publication Acceptance Date: 6/13/2011
Publication Date: 7/28/2011
Citation: Moscou, M.J., Lauter, N.C., Steffenson, B., Wise, R.P. 2011. Quantitative and qualitative stem rust resistance factors in barley are associated with transcriptional suppression of defense regulons. PLoS Genetics. 7(7):DOI: 10.1371/journal.pgen.1002208. Interpretive Summary: Cereal crops are the nutritional foundation of humans and domesticated animals world-wide. So successfully controlling existing and emerging cereal crop diseases is vital to food security. Ug99 stem rust is a devastating fungal disease of wheat and barley. To mitigate the emerging disease threat to Ug99 stem rust, we have employed genetical genomics, in which genome-wide expression profiling is performed on entire segregating populations. Genetical genomics provides the opportunity to identify master regulators, or switches, while simultaneously identifying the downstream targets. Molecular markers for these master regulators, as well as their targets, are used by breeders to successfully combat devastating diseases. By using Barley1 GeneChips to profile expression in a population of doubled haploid lines segregating for resistance to Ug99, we identified a master switch that regulates the expression of over 500 Ug99 responsive defense genes. We further show that the master regulator coincides with an enhancer of Adult Plant Resistance to Ug99 discovered in Kenyan field trials. This is the first comprehensive study to understand genome-wide gene expression in response to Ug99 stem rust. Since Ug99 can devastate yields among nearly all wheat and barley varieties grown worldwide, characterization of the master switch, and development of allele-specific markers, will be used to accelerate the integration of adult plant resistance to Ug99, thus producing high quality barley grain with better yields, benefitting farmers and producers.
Technical Abstract: Stem rust (Puccinia graminis f. sp. tritici; Pgt) is a devastating fungal disease of wheat and barley. Pgt race TTKSK (isolate Ug99) is a serious threat to these Triticeae grain crops because resistance is rare. In barley, the complex Rpg-TTKSK locus on chromosome 5H is presently the only known source of qualitative resistance to this aggressive Pgt race. Segregation for resistance observed on seedlings of the Q21861 x SM89010 (QSM) doubled-haploid (DH) population was found to be predominantly qualitative, with little of the remaining variance explained by loci other than Rpg-TTKSK. In contrast, analysis of adult QSM DH plants infected by field inoculum of Pgt race TTKSK in Njoro, Kenya revealed several additional quantitative trait loci that contribute to resistance. To molecularly characterize these loci, Barley1 GeneChips were used to measure the expression of 22,792 genes in the QSM population after inoculation with Pgt race TTKSK and mock-inoculation. Comparison of expression Quantitative Trait Loci (eQTL) between treatments revealed an inoculation-dependent expression polymorphism implicating Actin depolymerizing factor3 (within the Rpg-TTKSK locus) as a candidate susceptibility gene. In parallel, we identified a chromosome 2H trans-eQTL hotspot that co-segregates with an enhancer of Rpg-TTKSK-mediated, adult plant resistance discovered through the Njoro field trials. Our genome-wide eQTL studies demonstrate that transcript accumulation of 25% of barley genes is altered following challenge by Pgt race TTKSK, but that few of these genes are regulated by the qualitative Rpg-TTKSK on chromosome 5H. It is instead the chromosome 2H trans-eQTL hotspot that orchestrates the largest inoculation-specific responses, where enhanced resistance is associated with transcriptional suppression of hundreds of genes scattered throughout the genome. Hence, the present study associates the early suppression of genes expressed in this host-pathogen interaction with enhancement of R-gene mediated resistance.