Edited eukaryotic translation initiation factors confer resistance against maize lethal necrosis

Abstract Description:

Maize lethal necrosis (MLN), caused by maize chlorotic mottle virus (MCMV) and sugarcane mosaic virus (SCMV), poses a significant threat to the food security of smallholder farmers in Sub-Saharan Africa (SSA). Our recent discovery of a unique eukaryotic translation initiation factor 4E (eIF4E) offers a promising solution to this challenge. During viral infections, plant eIF4Es are often recruited to translate viral proteins. Virus resistances are frequently linked to loss-of-function mutations in eIF4Es. Through phylogenetic analysis, we identified two maize eIF4E genes and knocked them out individually in elite but MLN-susceptible SSA maize lines. This conferred only partial protection against MLN. Our inability to simultaneously knock out both eIF4Es indicated that at least one of these genes is essential for plant survival. Applying the same gene knockout strategy in the Fast-Flowering Mini Maize (an experimental line) yielded different results. Plants with eif4e1-KO exhibited strong resistance to MLN, while those with eif4e2-KO remained susceptible. Remarkably, neither of the causal viruses was detected in MLN-inoculated eif4e1-KO Mini Maize. Further analysis revealed that the eIF4E2 cDNA in Mini Maize lacked the entire fourth exon, resulting in a 22-amino acid in-frame deletion and a truncated protein of 198 amino acids. We introduced targeted edits (ED) in the fourth exon of eIF4E2 in the two elite, MLN-susceptible SSA lines that had been pre-edited for eif4e1-KO. These edits conferred resistance comparable to that observed in eif4e1-KO Mini Maize. Notably, the MLN-inoculated eif4e1-KO/eIF4E2-exon-4ED elite lines performed as well as uninoculated wild-type plants. Our findings demonstrate that the amino acids encoded by the fourth exon of eIF4E2 are dispensable for normal plant growth but critical for the multiplication of MLN-causing viruses. This discovery has broad implications for developing virus-resistant crop varieties across multiple plant species.

Equity, Diversity, and Inclusion: The research is conducted by researchers with different ethnic identities from research institutions located in multiple continents, including Africa, Asia and America.