Apoplast Engineering Unveiled: Multi‐Target Strategies to Disarm Pathogens and Elevate Global Food Security

In nature, plants are associated with a variety of microbes that exert beneficial, neutral, and pathogenic effects within their hosts. Pathogenic bacteria, fungi, and oomycetes pose a significant threat to the health and productivity of plants in both natural ecosystems and agricultural environments. To regulate the outcomes of plant-microbe interactions, the apoplast is capable of detecting and responding to pathogens infections. The genetic regulation of apoplast activities remains largely opaque, and earlier DNA sequencing from apoplastic fluid samples may have underestimated the diversity of cell wall-associated proteins and the cell wall proteome. However, the direct genetic manipulation of apoplast structure and function in living plants has not yet been fully explored. Given the unique biology of the apoplast, its targeted modification offers a promising new avenue for plant biotechnology. In this review, we address the recent findings on how plant microbial pathogens utilised diverse strategies to damage plant immunity. Additionally, we explore emerging multi-target approaches for engineering the apoplast to enhance resistance against a broad range of pathogens. Most importantly, we propose a novel approach to establish a dual-layer immunity within the apoplast by stacking of pattern recognition receptors with sensor nucleotide-binding leucine-rich repeat receptors to trigger system-acquired response through advanced gene-editing tools. Apoplast engineering and non-expression system hold great promise for the development of genetically resistant upgraded crops varieties and may significantly contribute to sustainable, green and eco-friendly agriculture and global food security.