A Genome-Wide Analysis of Pathogenesis-Related Protein-1 (PR-1) Genes from Piper nigrum Reveals Its Critical Role during Phytophthora capsici Infection

Abstract

Black pepper (Piper nigrum L.) is a prominent spice that is an indispensable ingredient in cuisine and traditional medicine. Phytophthora capsici, the causative agent of footrot disease, causes a drastic constraint in P. nigrum cultivation and productivity. To counterattack various biotic and abiotic stresses, plants employ a broad array of mechanisms that includes the accumulation of pathogenesis-related (PR) proteins. Through a genome-wide survey, eleven PR-1 genes that belong to a CAP superfamily protein with a caveolin-binding motif (CBM) and a CAP-derived peptide (CAPE) were identified from P. nigrum. Despite the critical functional domains, PnPR-1 homologs differ in their signal peptide motifs and core amino acid composition in the functional protein domains. The conserved motifs of PnPR-1 proteins were identified using MEME. Most of the PnPR-1 proteins were basic in nature. Secondary and 3D structure analyses of the PnPR-1 proteins were also predicted, which may be linked to a functional role in P. nigrum. The GO and KEGG functional annotations predicted their function in the defense responses of plant-pathogen interactions. Furthermore, a transcriptome-assisted FPKM analysis revealed PnPR-1 genes mapped to the P. nigrum-P. capsici interaction pathway. An altered expression pattern was detected for PnPR-1 transcripts among which a significant upregulation was noted for basic PnPR-1 genes such as CL10113.C1 and Unigene17664. The drastic variation in the transcript levels of CL10113.C1 was further validated through qRT-PCR and it showed a significant upregulation in infected leaf samples compared with the control. A subsequent analysis revealed the structural details, phylogenetic relationships, conserved sequence motifs and critical cis-regulatory elements of PnPR-1 genes. This is the first genome-wide study that identified the role of PR-1 genes during P. nigrum-P. capsici interactions. The detailed in silico experimental analysis revealed the vital role of PnPR-1 genes in regulating the first layer of defense towards a P. capsici infection in Panniyur-1 plants.

Genome-Wide Characterization and Expression Analysis of Pathogenesis-Related 1 (PR-1) Gene Family in Tea Plant (Camellia sinensis (L.) O. Kuntze) in Response to Blister-Blight Disease Stress

“…Previous studies on Triticum aestivum and Vitis showed that all PR-1 proteins contain an SP at the N terminal, which could secrete PR-1 proteins into the extracellular environment [14,24]. Two PnPR-1 proteins without SPs were also found in Piper nigrum, which is consistent with the present results [13]. Most CsPR-1 proteins containing an SP at the N terminal might be guided into special subcellular organelles for their biological functions.…”

“…PR-1 proteins occur in multigene families within plant genomes and can be further classified as acidic or basic, depending on their theoretical isoelectric point (pI) [12]. Numerous studies have demonstrated that PR-1 proteins abundantly accumulate during plant-defense responses and are ubiquitous across plant species [8,13]. In grapevine ('BN5-4'), the basic-type VvPR1b1 gene confers high resistance against Pseudomonas syringae [14].…”

“…Recently, with the development of gene-sequencing technology and the improvement of bioinformatics prediction systems, a growing number of gene families has been identified [17][18][19][20][21][22]. At present, the PR-1 gene family has been identified, as well expression profiles in response to biotic and abiotic stresses in many species-for instance, 11 genes in Piper nigrum [13], 13 in Solanum lycopersicum [23], 21 in Vitis vinifera [14], 22 in Arabidopsis [8], 23 in Triticum aestivum [24], 24 in Glycine max [25], and 32 in Oryza sativa [8]. Clarifying the classification and composition of gene-family members in the genome is the first step to explore species-related characteristics and biological problems and can lay a solid foundation for subsequent gene-function characterization and genetic manipulation.…”

The Wheat Pathogenesis Related Protein (TdPR1.2) Ensures Contrasting Behaviors to <i>E. coli</i> Transformant Cells under Stress Conditions

“…The first member of PR-1 family, PR1-a was identified in Nicotiana tabacum plants infected with Tobacco Mosaic Virus (TMV) [4]. Subsequently, several other PR-1 proteins have been identified and characterized in monocot and dicot plant species, such as tomato (Solanum lycopersicum) [5], Triticum aestivum [6], Piper nigrum [7], Grapevine [8], Arabidopsis thaliana, Oryza sativa [9] and cassava (Manihot esculenta) [10]. Their important roles were reported in response to stress conditions [5]- [10].…”

Non-Targeted Metabolite Profiling Reveals Host Metabolomic Reprogramming during the Interaction of Black Pepper with Phytophthora capsici

“…We have examined miRNA-mediated gene regulation in P. nigrum [ 35 ], tRNA-derived sRNAs effects on the transcriptome of pathogen-infected plants [ 36 ] and the role of microRNA mediated post-transcriptional regulation during P. capsici infections. Moreover, our studies in black pepper during P. capsici infection demonstrated the differential regulation and the presence of phytohormone-responsive transcription activators in the promoter regions of PR-1 genes, which are crucial for SAR induction during pathogen attack [ 37 ]. In our current study, we employ flow-infusion electrospray-high-resolution mass spectrometry (FIE-HRMS) to provide a comprehensive description of the metabolome during quick wilt disease development, both at the site of infection and systemically.…”