ANTHRACNOSE RESISTANCE GENE2 confers fungal resistance in sorghum

Abstract

Sorghum is an important food and feed crop globally; its production is hampered by anthracnose disease caused by the fungal pathogen Colletotrichum sublineola (Cs). Here, we report identification and characterization of ANTHRACNOSE RESISTANCE GENE 2 (ARG2) encoding a nucleotide-binding leucine-rich repeat (NLR) protein that confers race-specific resistance to Cs strains. ARG2 is one of a cluster of several NLR genes initially identified in the sorghum differential line SC328C that is resistant to some Cs strains. This cluster shows structural and copy number variations in different sorghum genotypes. Different sorghum lines carrying independent ARG2 alleles provided the genetic validation for the identity of the ARG2 gene. ARG2 expression is induced by Cs, and chitin induces ARG2 expression in resistant but not in susceptible lines. ARG2-mediated resistance is accompanied by higher expression of defense and secondary metabolite genes at early stages of infection, and anthocyanin and zeatin metabolisms are upregulated in resistant plants. Interestingly, ARG2 localizes to the plasma membrane when transiently expressed in Nicotiana benthamiana. Importantly, ARG2 plants produced higher shoot dry matter than near-isogenic lines carrying the susceptible allele suggesting an absence of an ARG2 associated growth trade-off. Furthermore, ARG2mediated resistance is stable at a wide range of temperatures. Our observations open avenues for resistance breeding and for dissecting mechanisms of resistance.

Haplotypes at the sorghum ARG4 and ARG5 NLR loci confer resistance to anthracnose

“…The new locus is designated ANTHRACNOSE RESISTANCE GENE 4 ( ARG4 ), following our sequential naming of three other anthracnose resistance loci ( ARG1 to ARG3 ) identified recently using different mapping populations. ARG1 and ARG2 have been published (Lee et al., 2022; Mewa et al., 2023) while ARG3 is pending publication. The segregation pattern of the SAP135 x TAM428 mapping populations varied when plants were inoculated with different strains suggesting SAP135 carries multiple independent loci conferring resistance to different strains.…”

“…ARG1 confers broad‐spectrum fungal resistance in sorghum. The second gene ANTHRACNOSE RESISTANCE GENE 2 ( ARG2 ) encoding another NLR protein that confers race‐specific resistance to C. sublineola strains was also identified and characterized in our lab (Mewa et al., 2023). These data, collectively, provided new insights into the genetic control of plant immunity in sorghum.…”

“…Fungal strains of C. sublineola were cultured on potato dextrose agar (BD Difco, Sparks, MD, USA) and conidia harvested from 15‐day‐old cultures and used for disease assays as described previously (Lee et al., 2022; Mewa et al., 2023). The fungal cultures were kept under a continuous florescence light for 2 weeks, after which spores were collected and used to inoculate 3 weeks old plants.…”

“…Moreover, application of whole genome sequences and other genomic tools may improve mapping of anthracnose resistance genes underlying the various QTLs. The recent discovery of anthracnose resistance genes by our group (Lee et al., 2022; Mewa et al., 2023) provided new insights into the complexity and regulation of anthracnose immune response genes in sorghum and revealed the roles of next‐generation genomic tools in unraveling the mechanisms of disease resistance in crop plants.…”

Exploring the genetic basis of anthracnose resistance in Ethiopian sorghum through a genome-wide association study

“…Among the testing sites, Haramaya stands out as the environment where the majority of accessions demonstrated a resistant reaction to anthracnose (Table S1 ). Recent studies isolated ANTHRACNOSE RESISTANCE GENES (ARG1, ARG2, ARG4, and ARG5) encoding nucleotide-binding leucine-rich repeats (NLR) proteins [ 20 – 22 ]. It is worth noting that the current study identified new loci containing new NLRs and RLKs but none of the ARGs genes were identified showing differences in mapping through biparental and GWAS approaches and differences in field and greenhouse-based genetic screens for disease resistance.…”