|SURANA, PRIYANKA - Iowa State University|
|XU, RUO - Iowa State University|
|CHAPMAN, ANTONY - Iowa State University|
|NETTLETON, DAN - Iowa State University|
Submitted to: Genes, Genomes, and Genomics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/4/2017
Publication Date: 8/8/2017
Citation: Surana, P., Xu, R., Fuerst, G.S., Chapman, A., Nettleton, D., Wise, R.P. 2017. Inter-chromosomal transfer of immune regulation during infection of barley with the powdery mildew pathogen. Genes, Genomes, and Genomics. https://doi.org/10.1534/g3.117.300125.
Interpretive Summary: Plant immune systems exemplify multi-tiered, signaling networks. These molecular networks can be envisioned as layers comprised of biological molecules interacting in space and time to influence each other. In the interaction between the cereal grain crop barley and the powdery mildew fungus, Blumeria graminis f. sp. hordei, successful infection results in penetration of host epidermal cells, culminating in haustorial feeding structures, which facilitate delivery of pathogen effector proteins to the host plant and also uptake of nutrients from the plant to the fungus. Host ML (mildew) immune receptors sense pathogen effectors, triggering defense networks comprising thousands of genes. We sought to understand host gene regulation in this host-pathogen interaction by utilizing expression quantitative trait locus (eQTL) analysis of a segregating barley population challenged with powdery mildew. Two major groups of defense regulators were identified on barley chromosomes 2HL and 1HS. Within these chromosomal positions reside two loci that confer immunity to powdery mildew, MlLa (conferring quantitative resistance) and Mla (conferring qualitative resistance). A major role of these immunity regulators is to control, in trans, the altered expression of 961 and 3,296 genes, respectively, corresponding to powdery mildew penetration and development of haustorial feeding structures. Intriguingly, ~30% of the genes regulated by MlLa during penetration, are repurposed by Mla during development of haustoria. Powdery mildew haustoria function in cell-cell communication between the two species, hence, host genes repurposed during this stage of development could be considered as essential for defense in the host or colonization by the pathogen. These findings imply that 1) these genes are part of an immune regulatory complex activated by disparate resistance genes, and 2) a major portion of the encoded proteins function together to achieve immunity in response to different pathogen isolates or infection stages. We postulate that a conserved core of genes can be activated by master regulators to respond to diverse pathogen attack scenarios. Knowledge from this research will impact how plant breeders select for disease resistance, one of the most important traits that affect crop yield, and thus food security.
Technical Abstract: Powdery mildews infect over 9,500 plant species, causing critical yield loss. Powdery mildew disease of barley is caused by the Ascomycete fungus, Blumeria graminis f. sp. hordei (Bgh) and has become a model for the interactions among obligate biotrophs and their cereal hosts. Successful infection results in penetration of host epidermal cells, culminating in haustorial feeding structures, which facilitate delivery of pathogen effectors to the plant and exchange of nutrients from the plant to the fungus. Genome-wide transcriptome analysis of the Bgh-infected barley Q21861 X SM89010 doubled haploid population identified significant clusters of trans eQTL (expression quantitative trait loci) near the telomeric ends of chromosomes 2HL and 1HS. Within these clusters reside the resistance (R) loci, MlLa (conferring quantitative resistance) and Mla (conferring qualitative resistance), which associate with the altered expression of 961 and 3,296 genes, respectively, corresponding to Bgh penetration and haustorial growth (q-value = 1e-3). Moreover, of the 961 genes regulated by MlLa during penetration, control of ~30% of these are repurposed by Mla during haustorial development. Time-course pattern analysis of these transcripts discerned two opposing scenarios: The first represents host genes suppressed by pathogen effectors in compatible interactions, as opposed to incompatible interactions. Protein annotations are uniquely associated with vesicle transport, secondary metabolism, and hormone signaling. In contrast, the second represents a situation where the pathogen continues to induce defense in compatible interactions, and may co-opt these host genes for its own purposes. Protein annotations encoded by these genes are enriched in chloroplasts, abiotic stress and RNA processing. We postulate that genes regulated by alternate chromosomal positions are repurposed as part of conserved immune complex to respond to different pathogen attack scenarios.