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Title:   Author  item
                                            Halterman, Dennisitem
                                            WEI, FUSHENG - IOWA STATE UNIVERSITYitem
                                            Wise, Roger
  Submitted to: Plant Physiology
                                    Publication Type: Peer Reviewed Journal
                                    Publication Acceptance Date: 11/21/2002
                                    Publication  Date: 2/2/2003
                                    Citation: Halterman, D.A., Wei, F., Wise, R.P. 2003. Powdery mildew induced Mla mRNAs are alternatively spliced and contain upstream open reading frames. Plant Physiology. 131(2):558-567.Interpretive Summary: Powdery mildew of barley is an ideal system for investigating fungal diseases in cereal crops.  At least 30 resistance variants have been identified at a major resistance determinant to this disease, designated Mla.  However, the mechanisms of regulation of plant disease resistance genes and resistance gene products are largely unknown.  We cloned the Mla13 variant by a map-based approach, and have used it as a model for the regulation of host resistance to obligate biotrophic fungi.  We demonstrated for the first time that expression of Mla13, as well as two additional genes required for Mla resistance, Rar1 and Sgt1, are coordinately induced during the same time frame that powdery mildew feeding structures make contact with the host cell plasma membrane.  Three small genes upstream of Mla13 control the regulation of downstream protein synthesis and appear to be required for proper activity of the resistance gene.  Our results indicate that regulation of Mla transcription is not constitutive and that induction is coordinately controlled by recognition-specific plant factors.  The sudden increase in transcription could account for the rapid defense response phenotype conferred by Mla13, while simultaneous control of the amount of protein synthesis would prevent uncontrolled cell death.  This is the first description of specific induction of resistance gene expression in grain crops.  The results described in this manuscript will impact scientists who are working to understand the intricacies of disease defense responses in plants.
                                Technical Abstract: In barley, the Mla13 powdery mildew resistance gene confers Rar1-dependent, AvrMla13-specific resistance to Blumeria graminis f. sp. hordei (Bgh).  We have identified cDNA and genomic copies of Mla13, and used these as a model for the regulation of host resistance to obligate biotrophic fungi.  We demonstrated quantitatively that transcription of Mla6 and Mla13, as well as the Mla-signaling pathway components, Rar1 and Sgt1, are induced at 16 hours post inoculation, the same time frame that haustoria of avirulent Bgh make contact with the host cell plasma membrane.  Three upstream open reading frames (uORFs) within the transcript leader regions (TLRs) of Mla6 and Mla13 mRNAs control synergistically the down-regulation of reporter protein synthesis by up to 13-fold.  Alternative splicing of two introns within this TLR of Mla13 can lead to a different number of these uORFs and variability in the size of uORF2.  The presence of the Mla TLR, which regulates levels of translated reporter protein, appears to be required for proper activity in vivo since Mla6 with a deleted TLR, under the control of a strong promoter, leads to a loss of resistance specificity.  Our results indicate that regulation of Mla transcription is not constitutive and that induction is coordinately controlled by recognition-specific plant factors.  The sudden increase in transcription could account for the rapid defense response phenotype conferred by Mla6 and Mla13, while simultaneous control of the amount of protein synthesis would prevent uncontrolled cell death.


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