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Title: Transcript-based Cloning of RRP46, a Regulator of rRNA Processing and R-Gene-Independent Cell Death in Barley–Powdery Mildew Interactions

Author
item XI, LIU - Iowa State University
item MOSCOU, MATTHEW - Iowa State University
item MENG, YAN - Iowa State University
item XU, WEIHUI - Iowa State University
item CALDO, RICO - Iowa State University
item SHAVER, MIRANDA - National Institutes Of Health (NIH)
item NETTLETON, DAN - Iowa State University
item Wise, Roger

Submitted to: The Plant Cell
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/2/2009
Publication Date: 10/27/2009
Citation: Xi, L., Moscou, M.J., Meng, Y., Xu, W., Caldo, R.A., Shaver, M., Nettleton, D., Wise, R.P. 2009. Transcript-based Cloning of RRP46, a Regulator of rRNA Processing and R-Gene-Independent Cell Death in Barley–Powdery Mildew Interactions. The Plant Cell. 21(10):3280-3295.

Interpretive Summary: Programmed cell death is regulated by several diverse pathways in plants. Examples include the initiation and execution of senescence during plant development, the hypersensitive response during pathogen attack, and cellular damage sustained from various abiotic stresses. Barley1 GeneChip expression profiles were used to discern the reprogramming of the transcriptome associated with the "Bgh-induced tip cell death1" mutation, bcd1, as compared to its progenitor upon challenge by the powdery mildew pathogen. Bioinformatic and functional analytic methods were used to elucidate that HvRRP46, encoding a key ribosomal RNA processing protein, regulates cell death in an R-gene-independent manner. HvRRP46 belongs to the exosome, a conserved multiexonuclease complex that mediates RNA processing and degradation, a conserved process essential for normal development in all organisms. To our knowledge, the role of the exosome during host-pathogen interactions has not previously been reported. Our results suggest a role of rRNA processing genes in mediating disease defense, implying a shared signaling pathway for exosome metabolism/processing and cell death independent of the resistance response. Plant diseases are among the greatest impediments to crop production worldwide. RRP46 appears to be a master regulator that controls the expression of every ribosomal protein gene in plants. Because of its role in cell death progression as a result of signaling during the barley-powdery mildew interaction, this finding provides new knowledge of broad significance to plant scientists, and to growers who utilize disease resistance to protect their crops.

Technical Abstract: Programmed cell death (PCD) plays a pivotal role in plant development and defense. To investigate the degree of interaction between PCD and R-gene mediated defense, we used the 22K Barley1 GeneChip to compare and contrast time-course expression profiles of Blumeria graminis f. sp. hordei (Bgh) challenged barley cultivar C.I. 16151 (harboring the Mla6 powdery mildew resistance allele) and its fast-neutron-derived Bgh-induced tip cell death1 mutant, bcd1. Mixed linear model analysis was used to identify genes associated with the cell death phenotype as opposed to R-gene mediated resistance. One-hundred fifty genes were found at the threshold p value < 0.0001 and a false discovery rate < 0.6%. Of these selected 150 genes, 124 were constitutively overexpressed in the bcd1 mutant. Gene Ontology- and rice alignment-based annotation indicates that 68 of the 124 overexpressed genes encode ribosomal proteins. A deletion harboring six genes on chromosome 5H co-segregates with bcd1-specified cell death, is associated with misprocessing of rRNAs, but segregates independent of R-gene mediated resistance. Barley stripe mosaic virus-induced gene silencing of one of the six deleted genes, HvRRP46 (Ribosomal RNA-processing protein 46), phenocopied bcd1-mediated tip cell death. These findings suggest that RRP46 mediates metabolism involved in cell death initiation as a result of attempted penetration by Bgh during the barley-powdery mildew interaction, but is independent of gene-for-gene resistance.