Transcriptomic and Targeted Metabolomic Analyses of Partially Resistant and Susceptible Pea Genotypes Reveal Differential Defense Responses During Their Interaction With Aphanomyces euteiches

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ABSTRACT Aphanomyces root rot (ARR) incidence and prevalence are increasing throughout pea‐growing regions worldwide, highlighting the need for effective management strategies to safeguard yields. Understanding pea defense against ARR is essential for developing resistant cultivars. To decipher defense mechanisms, a comprehensive transcriptional study was conducted using RNA‐seq from roots of partially resistant (PR, PI 660736, PI 660729, PI 557550 and 5001) and a susceptible (S, CDC Meadow) pea genotype at various time points (2, 6, 12, and 24 h post‐pathogen inoculation [hpi]). We found significant differences in metabolic pathway enrichment between the PR and S genotypes, with notable distinctions at 6 and 24 hpi. At 6 hpi, ethylene‐activated signaling and phosphorylation pathways were enriched across all PR genotypes, whereas response to abscisic acid and response to stress were enriched only in the S genotype. By 24 hpi, PR genotypes demonstrated upregulation of processes related to regulation of DNA‐templated transcription , and RNA biosynthetic and metabolic processes , while the processes linked to shift in photosynthesis and energy reallocation were associated with the S genotype. The PR genotypes also exhibited upregulation of critical defense signaling genes, including WRKY transcription factors, ethylene response factors, MAPKs, and JAZ proteins, which remained unchanged in the S genotype. RNA‐seq and targeted metabolomics revealed the upregulation of pisatin (a phytoalexin) biosynthesis genes and the accumulation of pisatin in the PR genotypes. Our results suggest that partial resistance is controlled by the jasmonic acid and ethylene‐related signaling pathways, reactive oxygen species, and ubiquitin‐related proteins which modulate transcription factor activity and initiate wholescale changes in transcription, leading to activated phenylpropanoid and ultimately pisatin biosynthesis. These findings provide novel insights into pea partial resistance to Aphanomyces euteiches , paving the groundwork for resistance breeding and alternative strategies to mitigate the impact of ARR.

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