Exploring common bean's defense arsenal: Genome-wide characterization of PR-1 gene family and its transcriptional response to Colletotrichum lindemuthianum inoculation

Abstract

Pathogenesis-related Protein 1 (PR-1) plays a crucial role in plant defense responses, particularly against fungal pathogens. Despite its significance, comprehensive studies characterizing this gene family in the common bean (Phaseolus vulgaris) are currently lacking. Therefore, the objective of this study was to conduct genomic mining and characterization of the PR-1 in common bean (PvPR-1) genome. Additionally, we assessed the transcriptional expression of all its isoforms in response to inoculation with the fungus Colletotrichum lindemuthianum. This evaluation was performed on leaf tissue samples obtained from both sensitive (Rosinha) and resistant (Africano 4) common bean varieties at 24-, 48-, and 96-hours post inoculation. Thirteen PvPR-1 genes were consistently identified, forming two major clusters across the clustering analyses. Physicochemical characterization indicated that the PvPR-1 proteins are predominantly basic, hydrophilic, and extracellularly localized. Moreover, their promoter regions contain putative cis-regulatory elements that respond to a broad spectrum of plant hormones, including jasmonic acid, gibberellin, and ethylene, which are key regulators of both biotic and abiotic stress responses. This discovery implies a multifaceted role for the studied proteins in common bean physiology. KEGG pathway analysis implicated PvPR-1 proteins in hormonal signaling (corroborating the anchored cis-regulatory elements) and plant-pathogen interaction networks. Secondary structure evaluation revealed the predominance of α-helices and coiled structures within these proteins. Subsequent 3D modeling demonstrated a conserved ‘α-β-α’ sandwich architecture characterized by a central cavity. This structural motif suggests potential functional versatility, particularly in pathogen recognition and responses. Additionally, the study provided insight into the potential interactions of PvPR-1 with Chitinase II (PR-3) and Rab-18, as suggested by the STRING platform. Temporal differences in PvPR-1 gene expression were observed between the common bean contrasting varieties following C. lindemuthianum inoculation. Africano-4, the resistant one, showed a higher abundance of up-regulated and constitutively expressed PvPR-1 transcripts compared to its sensitive counterpart (Rosinha), indicating a more effective role of this gene family against the pathogen. Furthermore, based on PCA analyses and interaction networks of differentially expressed genes, three key targets within the PvPR-1 family (PvPR-1-4, PvPR-1-5, and PvPR-1-10) emerged as promising candidates for future functional characterization. These molecular actors displayed differential transcriptional patterns between the studied varieties without compromising the transcript abundance of PvPR-1 protein synthesis in the resistant one. Consequently, they may represent key components of resistance mechanisms that contribute to the differentiation between the two organisms. These findings deepen our understanding of PvPR-1 genes and their roles in common bean defense responses. They also emphasized the potential of PvPR-1 genes as candidates for breeding stress-resistant common bean varieties, which are crucial for bolstering crop resilience to environmental adversities.