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SUMMARY Sorghum anthracnose caused by the fungusColletotrichum sublineola(Cs) is a damaging disease of the crop. Here, we describe the identification ofANTHRACNOSE RESISTANCE GENES(ARG4andARG5) encoding canonical nucleotide‐binding leucine‐rich repeat (NLR) receptors.ARG4andARG5are dominant resistance genes identified in the sorghum lines SAP135 and P9830, respectively, that show broad‐spectrum resistance toCs. Independent genetic studies using populations generated by crossing SAP135 and P9830 with TAM428, fine mapping using molecular markers, comparative genomics and gene expression studies determined thatARG4andARG5are resistance genes againstCsstrains. Interestingly,ARG4andARG5are both located within clusters of duplicate NLR genes at linked loci separated by ~1 Mb genomic region. SAP135 and P9830 each carry only one of theARGgenes while having the recessive allele at the second locus. Only two copies of theARG5candidate genes were present in the resistant P9830 line while five non‐functional copies were identified in the susceptible line. The resistant parents and their recombinant inbred lines carrying eitherARG4orARG5are resistant to strains Csgl1 and Csgrg suggesting that these genes have overlapping specificities. The role ofARG4andARG5in resistance was validated through sorghum lines carrying independent recessive alleles that show increased susceptibility.ARG4andARG5are located within complex loci displaying interesting haplotype structures and copy number variation that may have resulted from duplication. Overall, the identification of anthracnose resistance genes with unique haplotype stucture provides a foundation for genetic studies and resistance breeding. 

Abstract Sorghum (Sorghum bicolor), the fifth most widely grown cereal crop globally, provides food security for millions of people. Anthracnose caused by the fungus Colletotrichum sublineola is a major disease of sorghum worldwide. We discovered a major fungal resistance locus in sorghum composed of the nucleotide-binding leucine-rich repeat receptor gene ANTHRACNOSE RESISTANCE GENE1 (ARG1) that is completely nested in an intron of a cis-natural antisense transcript (NAT) gene designated CARRIER OF ARG1 (CARG). Susceptible genotypes express CARG and two alternatively spliced ARG1 transcripts encoding truncated proteins lacking the leucine-rich repeat domains. In resistant genotypes, elevated expression of an intact allele of ARG1, attributed to the loss of CARG transcription and the presence of miniature inverted-repeat transposable element sequences, resulted in broad-spectrum resistance to fungal pathogens with distinct virulence strategies. Increased ARG1 expression in resistant genotypes is also associated with higher histone H3K4 and H3K36 methylation. In susceptible genotypes, lower ARG1 expression is associated with reduced H3K4 and H3K36 methylation and increased expression of NATs of CARG. The repressive chromatin state associated with H3K9me2 is low in CARG-expressing genotypes within the CARG exon and higher in genotypes with low CARG expression. Thus, ARG1 is regulated by multiple mechanisms and confers broad-spectrum, strong resistance to fungal pathogens.