Evolution of Polygalacturonases and Polygalacturonase‐Inhibiting Proteins: A View Beyond the Classical Perspective

Abstract As the first line of defence, the plant cell wall represents a battleground for both attackers' arsenals of harmful compounds and defensive actions of plants. Plants counteract tissue maceration caused by their enemies' plant cell wall degrading enzymes. Among those, pectin‐degrading polygalacturonases (PGs) of the glycoside hydrolase family 28 (GH28) are impaired by PG‐inhibiting proteins (PGIPs), extracellular members of the leucine‐rich repeat (LRR) family. PG‐PGIP interaction is well studied in the context of microbial phytopathogens. However, hypothetically, every organism that benefits from PG activity could be affected by PGIPs. Herein, we develop this view from the plant, the insect and the evolutionary perspective: (i) Plants produce their own PGs, which are involved in different developmental processes. We revisit plant PG–PGIP interaction and discuss foundational studies in light of up‐to‐date plant PG amino acid sequence data. (ii) We summarise recent advances in the field of PGs produced by insects and insect‐associated microbial symbionts and review how PGIPs influence insect PGs. (iii) As the functions of PGIPs and closely related LRR proteins are not limited to the inhibition of PGs, we combine information on functionally characterised LRR proteins with a comprehensive phylogenetic analysis and discuss the roles of plant‐specific extracellular LRR proteins in plant resistance and beyond.