Host-Induced gene silencing in barley powdery mildew reveals a class of ribonuclease-like effectors

Authors: PLIEGO, CLARA - Imperial College; NOWARA, DANIELA - Leibniz Institute Of Plant Genetics And Crop Plant Research; BONCIANI, GIULIA - Imperial College; GHEORGHE, DANA - Imperial College; XU, RUO - Iowa State University; SURANA, PRIYANKA - Iowa State University; WHIGHAM, EHREN - Iowa State University; NETTLETON, DAN - Iowa State University; BOGDANOVE, ADAM - Iowa State University; Wise, Roger; SCHWEIZER, PATRICK - Leibniz Institute Of Plant Genetics And Crop Plant Research; BINDSCHEDLER, LAURENCE - University Of Reading; SPANU, PIETRO - Imperial College

Submitted to: Molecular Plant-Microbe Interactions
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/20/2013
Publication Date: 6/1/2013
Citation: Pliego, C., Nowara, D., Bonciani, G., Gheorghe, D., Xu, R., Surana, P., Whigham, E., Nettleton, D., Bogdanove, A., Wise, R.P., Schweizer, P., Bindschedler, L., Spanu, P. 2013. Host-Induced gene silencing in barley powdery mildew reveals a class of ribonuclease-like effectors. Molecular Plant-Microbe Interactions. 26(6):633-642.

Interpretive Summary: ARS researchers collaborate with International team to defeat plant-pathogenic microbes. Plant diseases are among the greatest deterrents to crop production worldwide. Pathogenic microbes are able to infect plant cells by producing effector proteins that supercede the host’s immune response. The resulting selective pressures require the host to evolve mechanisms that detect these foreign proteins in order to resist infection. For example, the cereal powdery mildew pathogen penetrates living plant surface cells and develops a feeding structure inside the host to take up nutrients for colony proliferation. We leveraged the recent genome sequencing of the powdery mildew fungus (Spanu 2010, Science) to carry out a large-scale screen for effector proteins in this important cereal pathogen. Several novel pathogen proteins were discovered that manipulate the host cell to cause disease. This finding, like similar discoveries in human medicine, will be used to develop new ways to combat diseases of crop plants, most notable cereal grains, which are our most important food sources. Impact: Because common themes govern all plant-pathogen interactions, this finding provides new knowledge of broad significance to plant scientists, and to growers who utilize disease resistance to protect their crops.

Technical Abstract: Obligate biotrophic pathogens of plants require the ability to circumvent host defenses to enable colonization. To establish compatibility, pathogens secrete a variety of effectors, which regulate host immunity, and thus, facilitate the establishment of haustorial feeding structures. These structures promote nutrient exchange between host and pathogen, which manifest in disease. The barley powdery mildew fungus, Blumeria graminis f. sp. hordei, produces a vast array of effector candidate proteins that are specifically associated with infected host tissues. Fifty of these Blumeria Effector Candidates (BECs) were screened by Host Induced Gene Silencing (HIGS), identifying eight that produced a significant and reproducible decrease in pathogen development. Four of the eight effectors have similarities with ß-1,3 glucosyltransferase (1), metallo-protease (1) and microbial secreted RNAse (2); the other four are of unknown function. Transcript abundance of all eight BECs increases dramatically in the early stages of pathogenic development, consistent with their essential role in early infection and establishment of haustoria. Genes encoding BEC1011 and 1054 are paralogs in the Blumeria genome, but have undergone evolutionary sub-functionalization. Thus, these two BECs can be complemented independently, are necessary for full disease, and BEC1011 significantly interferes with pathogen-induced host cell death. BEC1011 and 1054 are part of gene super-family unique to the mildews distantly related to fungal RNAses and represent a novel class of experimentally-validated effectors.