Integrated analysis of Populus deltoides PR1 genes uncovered a PdePR1 as a defense marker against foliar rust

Abstract

Pathogenesis-related protein 1 (PR1), a hallmark of plant disease resistance, plays pivotal roles in defense signaling. In this study, we identified 16 intronless PR1 genes in Populus deltoides, all classified within the CAP superfamily (cysteine-rich secretory protein, antigen 5, and pathogenesis-related 1) and characterized by conserved N-terminal signal peptides, caveolin-binding motifs, and CAP-derived peptides. Phylogenomic reconstruction of 231 PR1 homologs across 15 plant species traced their origin to Chara braunii, with lineage-specific expansions driven by gene duplication. Evolutionary analyses revealed strong purifying selection acting on ancestral PR1 paralogs to confer a selective advantage for disease resistance. Integrated transcriptomic profiling and quantitative RT-PCR analyses identified PdePR1_10 as a key marker gene for defense activation, exhibiting significant induction at two days post-inoculation in resistant poplars. Co-expression network analysis indicated that PdePR1_10 interacts with several defense-related genes, including NBS-LRR resistance genes, signaling kinases, and hormone biosynthesis enzymes. Specifically, the W-box cis-regulatory element in the PdePR1_10 promoter is hypothesized to interact with WRKY transcription factors, activating PdePR1_10 expression through a salicylic acid (SA)-dependent signaling pathway. Transgenic poplars overexpressing PdePR1_10 exhibited significantly enhanced rust resistance, confirming its critical in defense response. In summary, we thoroughly elucidated the biological functions and regulatory mechanisms of PR1 genes in rust resistance and provided a valuable transgenic poplar line for future studies.