The sorghum ANTHRACNOSE RESISTANCE GENE 2 encodes a NLR protein that confers resistance to anthracnose

Authors: MEWA, DEMEKE - Purdue University; LEE, SANGHUN - Purdue University; LIAO, CHAO-JAN - Purdue University; SOUZA, AUGUSTO - Purdue University; ADEYANJU, ADEDAYO - Purdue University; Helm, Matthew; LISCH, DAMON - Purdue University; MENGISTE, TESFAYE - Purdue University

Submitted to: Plant Journal
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/22/2022
Publication Date: 11/28/2022
Citation: Mewa, D.B., Lee, S., Liao, C., Souza, A.M., Adeyanju, A., Helm, M.D., Lisch, D., Mengiste, T. 2022. ANTHRACNOSE RESISTANCE GENE 2 confers fungal resistance in sorghum. Plant Journal. 113(2):308-326. https://doi.org/10.1111/tpj.16048.
DOI: https://doi.org/10.1111/tpj.16048

Interpretive Summary: The emergence and spread of crop plant pathogens poses a significant risk to achieving global food and nutritional security sustainably. Of particular concern are those plant pathogens that can infect staple crop plants such as sorghum (Sorghum bicolor), the fifth most widely grown cereal crop globally. One such plant pathogen is Colletotrichum sublineola (C. sublineola), which causes anthracnose, the most devastating foliar disease of sorghum. Though there are anthracnose-resistant sorghum, our understanding of how sorghum confers resistance to C. sublineola is unclear. Here, we identified the underlying disease resistance protein that confers resistance to C. sublineola and named the gene ANTHRACNOSE RESISTANCE GENE 2 (ARG2). Importantly, these resistance responses to C. sublineola results in rapid activation of defense responses during the early stages of infection, thereby preventing spread of the fungal pathogen. Moreover, the resistance response to this fungal pathogen is stable at a wide range of temperatures common to most sorghum growing regions, indicating elevated temperatures do not compromise resistance. Lastly, we show the ARG2 resistance protein is localized on the plasma membrane, indicating it likely recognizes virulence proteins from the fungal pathogen. These results significantly advance our understanding of how sorghum detects fungal pathogens and opens the door for engineering new disease resistances in against plant pathogens of cereal grains.

Technical Abstract: Sorghum is an important food and feed crop globally, its production is hampered by anthracnose caused by the fungal pathogen Colletotrichum sublineola (Cs). We report isolation and characterization of ANTHRACNOSE RESISTANCE GENE2 (ARG2) encoding a nucleotide-binding leucine-rich repeat (NLR) protein that confers race-specific resistance to Cs. ARG2 is one of a cluster of several NLR genes in sorghum differential line SC328C that is resistant to some Cs strains. This cluster shows structural and copy number variations in different sorghum genotypes. Sorghum variants with independent ARG2 alleles provided the genetic validation for ARG2. ARG2 expression is induced by Cs, and chitin induced ARG2 expression in resistant but not in susceptible line. 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. ARG2 localizes to the plasma membrane after transient expression in Nicotiana benthamiana. ARG2 plants produced higher shoot dry matter than a near-isogenic line carrying the susceptible allele suggesting an absence of an ARG2 associated growth tradeoff. Further, ARG2-mediated resistance is stable at a wide range of temperatures. Our observations open avenues for resistance breeding and for dissecting mechanisms of resistance.