Genome editing for disease resistance in crops

Abstract

Plant diseases significantly reduce crop yield and quality, threatening global food security. Cultivating disease-resistant crops is essential for environmentally friendly disease control and food security. Thus, to enhance crop disease resistance, particularly broad-spectrum disease resistance (BSR), is vital for sustainable agriculture. Disease-resistance (R) genes encoded by pattern recognition receptors (PRRs) and nucleotide-binding leucine-rich repeat receptors (NLRs) confer BSR to a range of pathogens in plants. Additionally, atypical R genes, which do not encode immune receptors, often exhibit race non-specific and multipathogen resistance without yield penalty in crops. Understanding the underlying mechanisms of plant immunity, including pattern-triggered immunity (PTI), effector-triggered immunity (ETI) and atypical R gene-mediated immunity, provide new strategies for breeding disease-resistant crops. Over the past decade, genome editing has played an increasingly important role in crop breeding. Genome editing tools, such as diverse CRISPR/Cas systems, base editors, prime editors, and their derived tools, have proven highly efficient in generating single nucleotide polymorphisms (SNPs), insertions and deletions (InDels), substitutions, and large fragment deletions. These tools have significantly advanced functional genomics studies, particularly in the cloning, characterization, and engineering of BSR genes. They have also provided a wide range of strategies for enhancing disease resistance in crops. In contrast to traditional crop breeding approaches that rely on screening natural genetic variation and combining elite traits through cross-breeding, genome editing has significantly broadened the genetic diversity available for breeding disease-resistant crops and fostered innovation for disease resistance in crops. This advancement enables research on disease resistance in crops to break current barriers and progress to the next generation. In this review, we briefly introduce the principles and recent advancements of various genome editing tools. In addition, we provide examples of disease resistance achieved through CRISPR/Cas systems in multiple crops, such as rice, wheat, barley, maize, potato, tomato, soybean, pepper, cotton, and citrus. We then highlight diverse strategies employed to achieve disease resistance, for example, targeted insertion or replacement for disease resistance, saturation mutagenesis for elite R alleles, multiplexed genome editing of disease-susceptibility (S) genes for BSR, transcriptional and translational control of R and S genes for balancing between crop growth and immunity, and artificial intelligence (AI)-guided genome editing for precise editing, which accelerates the molecular breeding strategies for obtaining novel R alleles and generating disease-resistant crops. We also emphasize the potential applications of advanced genome editing tools in precisely introducing diverse R genes into crops for disease resistance in the future. Finally, we discuss the attitudes and principles of relevant domestic and foreign policies on the application of genome-edited crops. In summary, using genome editing strategies makes it possible to develop crops with durable and broad-spectrum disease resistance and promote sustainable agriculture in the future, ultimately contributing to global food security.