Journal
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
Volume 113, Issue 42, Pages E6486-E6495Publisher
NATL ACAD SCIENCES
DOI: 10.1073/pnas.1612947113
Keywords
avirulence effectors; association analysis; R genes; plant-microbe interactions; powdery mildew
Categories
Funding
- Max-Planck Society
- German Research Foundation in the Collaborative Research Centre [SFB670]
- Grains Research AMP
- Development Corporation [CUR00017, CUR00023 P8]
- JSPS KAKENHI Grant Inamori Foundation [JP16K07618]
- Grants-in-Aid for Scientific Research [16K07618] Funding Source: KAKEN
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Disease-resistance genes encoding intracellular nucleotide-binding domain and leucine-rich repeat proteins (NLRs) are key components of the plant innate immune system and typically detect the presence of isolate-specific avirulence (AVR) effectors from pathogens. NLR genes define the fastest-evolving gene family of flowering plants and are often arranged in gene clusters containing multiple paralogs, contributing to copy number and allele-specific NLR variation within a host species. Barley mildew resistance locus a (Mla) has been subject to extensive functional diversification, resulting in allelic resistance specificities each recognizing a cognate, but largely unidentified, AVR(a) gene of the powdery mildew fungus, Blumeria graminis f. sp. hordei (Bgh). We applied a transcriptome-wide association study among 17 Bgh isolates containing different AVR(a) genes and identified AVR(a1) and AVR(a13), encoding candidate-secreted effectors recognized by Mla1 and Mla13 alleles, respectively. Transient expression of the effector genes in barley leaves or protoplasts was sufficient to trigger Mla1 or Mla13 allele-specific cell death, a hallmark of NLR receptor-mediated immunity. AVR(a1) and AVR(a13) are phylogenetically unrelated, demonstrating that certain allelic MLA receptors evolved to recognize sequence-unrelated effectors. They are ancient effectors because corresponding loci are present in wheat powdery mildew. AVRA1 recognition by barley MLA1 is retained in transgenic Arabidopsis, indicating that AVR(A1) directly binds MLA1 or that its recognition involves an evolutionarily conserved host target of AVR(A1). Furthermore, analysis of transcriptome-wide sequence variation among the Bgh isolates provides evidence for Bgh population structure that is partially linked to geographic isolation.
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