Skip to main content
NCBI home page
Food Science & Nutrition logoLink to Food Science & Nutrition
. 2026 Mar 10;14(3):e71622. doi: 10.1002/fsn3.71622

Genome‐Wide Identification and Expression Analysis of Pathogenesis‐Related Protein 1 in Sweet Potato and Its Two Relatives

Ziyi Wang 1, Meiyan Liu 1, Mingku Zhu 1,2, Fei Zhang 1, Yanfei Ping 1, Zongyun Li 1,✉, Xiaowan Gou 1,✉
PMCID: PMC12976141  PMID: 41822238

ABSTRACT

Pathogenesis‐related Protein 1 (PR1) is a core component of plant innate immunity and plays crucial roles in plant growth, development, and stress response, especially biological stress. However, limited information is available on the PR1 genes in sweet potato and other Ipomoea species. In this study, 33, 50, and 36 PR1 or PR1‐like genes were identified from sweet potato ( I. batatas ), I. trifida, and I. triloba , respectively. Phylogenetic analysis categorized these genes into five groups, reflecting their evolutionary divergence. Cis‐regulatory elements associated with light, hormone, and stress responses. Tissue‐specific expression profiling of I. trifida and I. triloba revealed high expression levels in the flowers and flower‐buds, indicating potential roles in reproductive developmental processes. Stress response analysis showed that most PR1 genes in sweet potato were downregulated under biotic and abiotic treatments, whereas IbPR1‐5 was consistently upregulated across all three stress conditions. Our study provides novel insights into the evolutionary dynamics of PR1 genes across the three Ipomoea genomes and contributes to the future molecular breeding of sweet potato cultivars.

Keywords: expression analysis, Ipomoea trifida , Ipomoea triloba , pathogenesis‐related protein 1, sweet potato

Pathogenesis‐related Protein 1 (PR1) is a core component of plant innate immunity. We identified 33, 50, and 36 PR1 genes in Ipomoea batatas , Ipomoea trifida , and Ipomoea triloba . Phylogenetic analysis clustered them into 5 groups. Two diploid wild species show high flower/flower‐buds expression, and most sweet potato PR1s are downregulated under stress conditions, except IbPR1‐5. These findings provide valuable insights for the molecular breeding of sweet potato.

graphic file with name FSN3-14-e71622-g003.jpg

1. Introduction

As sessile organisms, plants are inherently exposed to numerous environmental stresses throughout their life cycle, which can be broadly categorized into biotic stresses (e.g., pathogen invasion, herbivorous pest infestation, and parasitic plant attachment) and abiotic stresses (e.g., drought, soil salinity, heavy metal toxicity, and extreme temperatures). These adverse conditions disrupt cellular metabolic homeostasis, trigger oxidative stress cascades, and in severe instances, induce programmed cell death, thereby impairing plant growth, development, and even survival (Dixit et al. 2024; Saijo and Loo 2019; Suzuki et al. 2014; Tossi et al. 2022). To counteract these multifaceted challenges, plants have evolved a sophisticated innate immune system coupled with a repertoire of stress‐responsive mechanisms to bolster their adaptive capacity. A pivotal group of molecules mediating these defense and stress adaptation processes are pathogenesis‐related (PR) proteins—a class of water‐soluble proteins that are de novo synthesized or significantly upregulated in plants in response to pathogen infection as well as exposure to specific abiotic stressors (Huot et al. 2017; Joshi et al. 2021; Han and Schneiter 2024; Han et al. 2023). Since their initial identification, PR proteins have been systematically categorized into 17 distinct families based on three core criteria: enzymatic or biological activity, amino acid sequence homology, and serological cross‐reactivity (Joshi et al. 2021; Han et al. 2025; Irigoyen et al. 2020). This classification system not only encapsulates the structural and functional diversity of PR proteins but also establishes a foundational framework for elucidating their regulatory roles in plant stress resistance (Sels et al. 2008).

The first PR protein was identified in tobacco and designated PR1 (van Loon and Kammen 1970). PR1 is classified as a member of the CAP (cysteine‐rich secretory proteins, antigen 5, and pathogenesis‐related protein 1) protein superfamily (Breen et al. 2017; Lincoln et al. 2018). CAP proteins harbor four CAP motifs (CAP1–4) and six conserved cysteine residues, forming a compact α‐β‐α sandwich fold structure. The CAP domain is essential for the physiological function of PR1 proteins in countering biological and environmental stresses (Breen et al. 2017; Han et al. 2023; Schneiter and Di Pietro 2013).

PR1 proteins are widely recognized as molecular markers for systemic acquired resistance (SAR) in plants (Breen et al. 2017; Seo et al. 2008). Accumulating evidence indicates that PR1 expression is induced not only by pathogen invasion but also by abiotic stressors including salinity, cold, and drought (Akbudak et al. 2020; AlHudaib et al. 2022; Almeida‐Silva and Venancio 2022; Chu et al. 2022; Liu et al. 2023; Luo et al. 2023; Sung et al. 2021). For example, when Phytophthora infestans invade potato, secreted PR1 proteins are induced and translocated into pathogen cells, where they target the AMPK kinase complex (a Ser/Thr protein kinase), inhibit its phosphorylation activity and thereby suppress vegetative growth and pathogenicity (Luo et al. 2023). Heterologous overexpression of mango MiPR1A in Arabidopsis significantly enhances the transcription of salicylic acid (SA) pathway‐related genes in transgenic lines following inoculation with Colletotrichum gloeosporioides, consequently improving resistance to this fungal pathogen (Li et al. 2023). Overexpressing PR1 in A. thaliana also confers enhanced resistance to both salinity and water deficit stress (Kothari et al. 2016). In tomato, all SlPR1 genes are upregulated under drought stress, indicating their active involvement in drought responses (Akbudak et al. 2020). The wheat PR1 gene is induced by osmotic stress, freezing, and salinity, and its heterologous overexpression in both yeast and Arabidopsis improves tolerance to these adverse conditions (Wang et al. 2019). In oat ( Avena sativa L.), AvPR1 expression is significantly upregulated under salinity, mannitol, PEG, and heat stress, markedly elevating AvPR1 transcript levels in both roots and shoots, implying that AvPR1 is implicated in plant response to many abiotic and hormonal stresses (AlHudaib et al. 2022).

PR1 proteins are encoded by multigene families in plants, typically generating dozens of different PR1 isoforms (Han et al. 2023). In Salvia miltiorrhiza , 11 PR1 genes have been identified (Fan et al. 2025), 23 in hexaploid wheat (Lu et al. 2011) and 12 in tetraploid wheat (Zribi et al. 2023), 17 in tea (Zhang et al. 2022), 24 in soybean (Almeida‐Silva and Venancio 2022), 21 in grape (Li et al. 2011), 19 in sugarcane (Chu et al. 2022), 13 in tomato (Akbudak et al. 2020), and 10 in mango (Li et al. 2023). The number of PR1 genes varies significantly across different species.

Ipomoea is the largest genus in the Convolvulaceae family, comprising 600 to 700 species. Sweet potato ( Ipomoea batatas (L.) Lam., 2n = 6x = 90) is the only widely cultivated and consumed species globally, serving as an important food, cash, and energy crop (Hirakawa et al. 2015). I. trifida (2n = 2x = 30) and I. triloba (2n = 2x = 30) are the closest diploid wild relatives of sweet potato, characterized by their compact genomes, making them ideal model plants for studying sweet potato genome evolution (Hirakawa et al. 2015; Sun et al. 2019; Wu et al. 2018).

In recent years, the sequencing, assembly, and release of genomes from hexaploid sweet potato cultivar Taizhong 6 ( I. batatas ) and its diploid wild relatives I. trifida and I. triloba have enabled genome‐wide identification and analysis of important gene families in sweet potato (Wu et al. 2018; Yang et al. 2017). However, comparative and evolutionary analyses of PR1 genes among I. batatas , I. trifida , and I. triloba remain unclear. In this study, the PR1 gene family of sweet potato and its wild relatives was identified by bioinformatics, and their physicochemical properties, chromosome distribution, collinearity, phylogenetic relationships, and promoter cis‐regulatory elements were analyzed. Under stress treatment, the response mode of the PR1 genes to biotic and abiotic stress was studied, providing a theoretical and experimental basis for sweet potato variety improvement and molecular breeding.

2. Materials and Methods

2.1. Identification and Chromosomal Distribution of PR1 Family Members

The genome‐wide information and annotation files of I. batatas , I. trifida , and I. triloba were downloaded from the Ipomoea Genome Hub (https://ipomoea‐genome.org/) and Sweet potato Genomics Resource (http://sweetpotato.plantbiology.msu.edu/).

To accurately identify all PR1 family members, three distinct screening approaches were employed. First, we performed BLASTP searches (E‐value ≤ 1 × 10−5) against the three Ipomoea species using all known PR1 family protein sequences from A. thaliana as queries to identify the predicted PR1 proteins. Next, potential PR1 proteins were identified using HMMER 3.0 software (hmmsearch, E‐value ≤ 1 × 10−5) with hidden Markov model profiles of the CAP domain (PF00188) obtained from the Pfam database (http://pfam.xfam.org/). Finally, all predicted PR1 proteins were verified using SMART (http://smart.embl‐heidelberg.de/) and CD‐search (https://www.ncbi.nlm.nih.gov/Structure/cdd/wrpsb.cgi). The ExPASy web‐based online tool (https://web.expasy.org) was used to analyze the physicochemical properties of predicted proteins, including molecular weight, theoretical pI, instability index, aliphatic index, and GRAVY. The prediction of three‐dimensional structures of PR1s was completed by SWISS‐MODEL (https://swissmodel.expasy.org/) online tool.

Based on the chromosomal positions provided by the Ipomoea Genome Hub (https://ipomoea‐genome.org/) and Sweet potato Genomics Resource (http://sweetpotato.plantbiology.msu.edu/), the IbPR1s, ItfPR1s, and ItbPR1s were mapped onto the I. batatas , I. trifida , and I. triloba chromosomes, respectively. The visualization was created using TBtools‐II software v2.388 (South China Agricultural University, Guangzhou, China) (Chen et al. 2023).

2.2. Phylogenetic Analysis of PR1s

The 22 PR1 protein sequences encoded by A. thaliana were downloaded from the TAIR database (http://www.arabidopsis.org/). The PR1 amino acid sequences of I. batatas , I. trifida, I. triloba , and A. thaliana were aligned using ClustalW with default settings, followed by phylogenetic tree construction in MEGA 10 with the neighbor‐joining (NJ) method (1000 bootstrap replicates) (www.megasoftware.net). The phylogenetic tree was visualized using iTOL (http://itol.embl.de/).

2.3. Gene Structure and Conserved Motif Analysis of PR1s

The exon‐intron structures of PR1 genes were extracted from the GFF3 file of the I. batatas , I. trifida , and I. triloba genome. Conserved motifs in PR1 proteins were analyzed using the online MEME suite (https://memesuite.org/meme/) with a parameter setting of maximum 15 motifs to be identified. The results were visualized using TBtools‐II software v2.388 (South China Agricultural University, Guangzhou, China). Multiple sequence alignment was performed using ClustalW (https://www.genome.jp/tools‐bin/clustalw) with default settings.

2.4. Cis‐Acting Element Analysis of PR1s

Cis‐acting elements within the 2000 bp promoter regions of PR1 genes were predicted by PlantCARE database (http://bioinformatics.psb.ugent.be/webtools/plantcare/html/), with subsequent visualization performed by TBtools‐II software.

2.5. Synteny Relationship and Ka/Ks Analysis

The genome sequences of A. thaliana , S. lycopersicum , G. max (L.) Merr. were downloaded from TAIR (http://www.arabidopsis.org/), Solanaceae Genomics Network (https://solgenomics.net/), and PHYTOZOME (https://phytozome.jgi.doe.gov/), respectively. The MCScanX function of TBtools software was used to construct inter‐species and intra‐species collinearity relationships, and TBtools‐II was used to visualize the relationships. Similarly, we used TBtools‐II with default parameters to calculate the Ka/Ks ratio for estimating the rate of evolution of PR1 genes over repetition. (Ka: non‐synonymous substitution rate, Ks: synonymous substitution rate).

2.6. Transcriptome Analysis

RNA‐seq data of F. solani were downloaded from NCBI under accession number SRR19136367, SRR19136368, SRR19136369, SRR19136370, SRR19136371, and SRR19136372. The read counts were normalized to Transcripts per Millions (TPM) value for gene expression quantification. The RNA‐seq data of C. fimbriata and drought stress for I. batatas PR1 expression analysis were obtained from related research in our laboratory. C. fimbriata was used to inoculate NJ92 (resistant) and YT252 (sensitive) for 4 days and 8 days. 10% PEG6000 was used to simulate drought stress in Xu32 (sensitive) for 48 h. While the gene expression data of I. trifida and I. triloba were downloaded from the Sweet Potato Genomics Resource (http://sweetpotato.plantbiology.msu.edu/). PR1 expression levels were measured in fragments per kilo base of exon per million fragments mapped (FPKM) and visualized through heatmaps using TBtools‐II software v2.388.

2.7. RNA Isolation and Quantitative Real‐Time PCR Analysis

Total RNA was isolated using the MolPure Plant Plus RNA Kit (Yeasen Biotechnology (Shanghai) Co. Ltd., Shanghai, China; Cat. No. 19292ES). RNA quality and concentration were assessed by agarose gel electrophoresis and ND‐2000C spectrophotometry. First strand cDNA was synthesized from 600 ng total RNA using Hifair III 1st Strand cDNA Synthesis SuperMix for qPCR (gDNA digester plus) (Yeasen Biotechnology (Shanghai) Co. Ltd., Shanghai, China, code no. 11141ES). The primers used for quantitative real‐time PCR (qRT‐PCR) were designed using Primer 3 Plus (http://www.bioinformatics.nl/cgi‐bin/primer3 plus/primer3plus.cgi) and are listed in Table S5. qRT‐PCR was performed using Hieff qPCR SYBR Green Master Mix (High Rox Plus) (Yeasen Biotechnology (Shanghai) Co. Ltd., Shanghai, China; Cat. No.: 11203ES). The thermal cycling conditions were as follows: 95°C (5 min)/(95°C (10 s)/60°C (30 s)/ × 40 cycles); A melting curve analysis was conducted from 60°C to 95°C with increments of 0.3°C per step to assess reaction specificity. These reactions were put in 96‐well optical reaction plates (Beijing Labgic Technology Co. Ltd., Beijing, China, code no. PP‐96‐NS‐0100) and performed on an ABI StepOne Plus real‐time PCR system. Each reaction was run in triplicate. Glyceraldehyde‐3‐phosphate dehydrogenase (GAPDH) was used as the internal control to normalize variations in sweet potato templates. The relative mRNA levels were calculated using the 2−∆∆Ct method.

3. Results

3.1. Identification of PR1 Genes in Three Ipomoea Species

In order to comprehensively identify PR1 genes in genomes of cultivated sweet potato and its two diploid wild relatives ( I. trifida and I. triloba ), three typical strategies (i.e., blastp search, hmmer search, and the CDD‐search database) were used. A total of 119 PR1 genes were identified: 33 in I. batatas (designated IbPR1‐1 to IbPR1‐33), 50 in I. trifida (ItfPR1‐1 to ItfPR1‐50), and 36 in I. triloba (ItbPR1‐1 to ItbPR1‐36). Their basic characteristics were analyzed using the sequences from I. batatas , I. trifida, and I. triloba (Tables S1 and S2). The CDS length of 119 PR1s ranged from 324 to 5886 bp, with a molecular weight (MW) of 11.69 to 220.93 kDa and a theoretical isoelectric point (pI) of 4.62 to 9.85. Putative protein lengths varied from 107 to 1961 amino acids (aa): sweet potato had the largest average protein length (329.81 aa, ranging from 107 to 1961 aa), followed by I. triloba (259.94 aa, ranging from 149 to 1004 aa) and I. trifida (198.12 aa, ranging from 119 to 1005 aa). All PR1 proteins had an instability index greater than 40, indicating that they are unstable proteins. Additionally, most of the PR1 proteins were predicted to be hydrophilic, as evidenced by negative GRAVY (grand average of hydropathicity) values, except IbPR1‐17, IbPR1‐21, IbPR1‐25, IbPR1‐27 (Table S1). The prediction of the three‐dimensional structures showed that these proteins mainly consist of α‐helices, extended strands, and random coils (Figure S1).

Chromosomal localization analysis revealed that the PR1 genes were distributed across 10, 12, and 11 chromosomes in I. batatas , I. trifida , and I. triloba, respectively (Figure 1). The remaining PR1 genes (17 in I. trifida ) were mapped to unanchored scaffolds that had not yet been assigned to a chromosome. The distribution of PR1 genes in Ipomoea species was disproportionate across the 15 chromosomes. In sweet potato, more than two PR1 genes are distributed across six chromosomes, with up to 8 IbPR1s located on chromosome 9 (Figure 1A). Conversely, in I. trifida , only four chromosomes contain more than three ItfPR1 genes, with the highest number (8 genes) being on chromosome 1 (Figure 1B). In I. triloba , only three chromosomes possess more than three PR1 genes, and the largest number (12 genes) is on chromosome 1 (Figure 1C).

FIGURE 1.

FIGURE 1

Open in a new tab

Distribution of PR1s across the chromosomes of three Ipomoea species. (A) Sweet potato; (B) I. trifida ; (C) I. triloba . The bars represent chromosome lengths. The chromosome numbers (black color) are displayed on the left side, and the gene names (red color) are displayed on the right side.

3.2. Phylogenetic Relationship Analysis of PR1s in Sweet Potato and Its Two Diploid Wild Relatives

For exploring the phylogenetic relationships of the PR1 genes in Ipomoea species, a phylogenetic tree was constructed based on the alignment of the 119 Ipomoea PR1 protein sequences with the 22 A. thaliana PR1s as references (Figure 2). On the basis of the evolutionary distance, all the PR1s were clustered into five groups and unevenly distributed on each branch of the phylogenetic tree. Of these five groups, group 5 was the largest (65 PR1 proteins), and group 1 was the smallest (8 PR1 proteins) (Figure 2). Arabidopsis PR1 members were distributed in groups 1, 3, and 4 (Figure 2), indicating evolutionary conservation of PR1 genes in these three groups among dicotyledonous plants. In contrast, groups 2 and 5 represent Ipomoea‐specific clades, which may be associated with functional divergence of Ipomoea species during adaptation to specific habitats.

FIGURE 2.

FIGURE 2

Open in a new tab

Phylogenetic tree of the PR1s in sweet potato, I. trifida , I. triloba , and Arabidopsis. The phylogenetic tree was constructed using the Neighbor‐Joining (NJ) method in MEGA version 10, with 1000 bootstrap replicates to evaluate branch support. The 4 species gene names were labeled with different colors and shapes: I. batatas genes are purple circles, I. trifida genes are green stars, I. triloba genes are red triangles, and Arabidopsis genes are orange rectangles. Red, green, blue, yellow, and purple lines represent the phylogenetic group 1–5, respectively.

3.3. Conserved Domains and Gene Structures of the Ipomoea PR1 Genes

The conserved motifs of Ipomoea PR1 proteins were predicted using the MEME tool. A total of 15 motifs were detected (Figure 3A; Figure S2). Among these motifs, motif‐2 was present in all Ipomoea PR1 proteins (119 sites) and exhibited the highest conservation (Figure 3A; Figure S2), which contains the CBM (caveolin‐binding) domain of steroid binding. It was followed by motif‐1 (CAP1 domain, 111 out of 119 sequences), motif‐6 (CAP3 domain, 110 of 119), motif‐5 (CAP4 domain, 103 of 119), and motif‐4 (CAP2 and CAPE (CAP‐derived peptide) domain, 101 of 119) (Figure 3A; Figure S2). Furthermore, combined with the results of protein multiple sequence alignment, it was further confirmed that there are members of Ipomoea PR1s with incomplete CAP1‐4 domains (Figure S3). For instance, IbPR1‐6 retained only the CAP1/2 and CAPE domains, IbPR1‐21 retained the CAP3/4 domains, while the CAP3 domain was lost in ItfPR1‐12, ItfPR1‐17, ItfPR1‐48, and ItbPR1‐14. Therefore, these PR1 sequences may be more appropriately designated as PR1‐like proteins, which could offer valuable insights into further specific functional analyses.

FIGURE 3.

FIGURE 3

Open in a new tab

Conserved motifs and exon‐intron structure analysis of PR1s in I. batatas , I. trifida , and I. triloba . (A) The phylogenetic tree showed that PR1s were divided into five subgroups, and the fifteen conserved motifs were shown in different colors. (B) Exon‐intron structures of PR1s. The green boxes, yellow boxes, and black lines represent exons, UTRs, and introns, respectively.

Approximately 70% Ipomoea PR1 genes (93 of 119) contain only one exon and no intron (Figure 3B), the number of exons of the remaining 30% PR1 members (35 of 119) varies within the range from 2 to 8. However, IbPR1‐30 is an exception, as it has 16 exons (Figure 3B). NCBI Conserved Domain (CD)‐Search confirmed that in addition to the CAP domain, this gene also contains 7 additional domains (Table S2). These findings suggest that IbPR1‐30 may possess multiple functional properties. Collectively, these results indicate that the PR1 gene family has undergone evolutionary diversification, leading to increased structural complexity.

3.4. Syntenic Analysis of PR1 Genes in the Genomes of the Three Ipomoea Species

Collinearity analysis within species revealed the presence of 4 pairs, 0 pairs and 2 pairs of homologous genes in sweet potato (IbPR1‐3 and IbPR1‐4; IbPR1‐15 and IbPR1‐24; IbPR1‐30 and IbPR1‐31; IbPR1‐31 and IbPR1‐32), I. trifida (no homologous genes) and I. triloba (ItbPR1‐1 and ItbPR1‐29; ItbPR1‐3 and ItbPR1‐25) (Figure 4A–C).

FIGURE 4.

FIGURE 4

Open in a new tab

Collinearity and syntenic analysis of the PR1 genes in Ipomoea species. Collinearity analysis of (A) I. batatas , (B) I. trifida, and (C) I. triloba . The outer circle represents the haploid chromosomes, the middle circle, and the inner circle represent the distribution density of genes on the chromosomes. Duplicated gene pairs are linked with red lines for PR1 genes. (D) Blue curves show the syntenic relationships between I. batatas , I. trifida, and I. triloba PR1s.

Interspecies syntenic analysis showed that 119 PR1 genes were detected in three Ipomoea species, forming 44 orthologous gene pairs (Figure 4D; Table S3). I. batatas and I. trifida had the largest number of orthologous PR1 gene pairs (17 pairs), followed by I. batatas and I. triloba (14 pairs), I. trifida and I. triloba (13 pairs). There were 7 pairs of orthologous genes shared by the three Ipomoea species. These results indicate that I. trifida is more closely related to I. batatas than I. triloba . Moreover, syntenic analysis of four genomes of sweet potato ( I. batatas ), A. thaliana , soybean ( Glycine max (L.) Merr.) and tomato ( Solanum lycopersicum L.) were performed. There were 5 pairs, 8 pairs, and 4 pairs of PR1 genes between sweet potato and Arabidopsis genome (Figure S4A), soybean genome (Figure S4B), tomato genome (Figure S4C), respectively. These results indicated that the PR1s showed a certain degree of conservation across different species.

3.5. Ka/Ks Analysis of Duplicated and Syntenic Ipomoea PR1 Genes

To investigate the selective pressure on homologous gene pairs in three Ipomoea species, the Ka/Ks values of these homologous gene pairs were analyzed (Table S4). Most PR1 duplicated and syntenic gene pairs' Ka/Ks ratios were less than 1 (92.2%), indicating that these gene pairs were subject to purifying selection during evolution. Only one pair of PR1 genes possessed a higher Ka/Ks ratio, i.e., 1.12 in sweet potato (IbPR1‐3 and IbPR1‐4). There were one and two syntenic PR1 gene pairs that kept Ka/Ks ratio greater than 1 between I. batatas and I. triloba (IbPR1‐11 and ItbPR1‐29, 1.22), and I. trifida and I. triloba (ItfPR1‐5 and ItbPR1‐12, 1.05; ItfPR1‐26 and ItbPR1‐29, 1.18), respectively (Table S4). These results indicate that during the process of speciation, the majority of duplicated and syntenic PR1 genes underwent purifying selection within the duplicated genomic regions. Conversely, a smaller number of these genes experienced positive selection.

3.6. Cis‐Acting Elements Analysis in the Promoters of PR1s in Sweet Potato and Its Two Diploid Wild Relatives

Cis‐acting elements refer to transcription factor‐binding DNA sites and other functional regulatory motifs located within the same DNA molecule, which play a crucial role in regulating the initiation of gene transcription. Therefore, we extracted the 2000 bp promoter sequences upstream of the start codon of PR1 genes from three Ipomoea species. We found light‐responsive cis‐regulatory elements were the most abundant in the three Ipomoea species, accounting for 1231 (49.4%) occurrences (Figure 5; Figures S5 and S6). A variety of endogenous hormone response elements were also detected, including those responsive to methyl jasmonate (MeJA, 244 occurrences, 9.8%), abscisic acid (ABA, 172 occurrences, 6.9%), gibberellin (103 occurrences, 4.1%), auxin (59 occurrences, 2.4%), and salicylic acid (SA, 51 occurrences, 2.0%), indicating that PR1s were involved in the regulatory networks mediated by plant hormone. In addition, several abiotic stress‐responsive elements were identified, such as anaerobic induction elements (197 occurrences, 7.9%), drought‐inducibility elements (91 occurrences, 3.7%), low‐temperature responsiveness elements (34 occurrences, 1.4%), and defense and stress responsiveness elements (34 occurrences, 1.4%). We also characterized cis‐acting elements associated with growth, development, and biosynthesis regulation, including circadian control elements (52 occurrences, 2.1%), zein metabolism elements (50 occurrences, 2.0%), meristem expression elements (45 occurrences, 1.8%), seed‐specific regulation elements (41 occurrences, 1.6%), and endosperm expression elements (23 occurrences, 0.9%). Furthermore, several protein binding sites were identified, namely general protein binding sites (18 occurrences, 0.7%), MYBHv1 binding site (28 occurrences, 1.1%), AT‐rich DNA binding protein (ATBP‐1) site (18 occurrences, 0.7%) (Figure 5; Figures S5 and S6). Collectively, these results indicate that PR1 genes are closely associated with plant growth and development, as well as the response to biotic and abiotic stresses in sweet potato and its two diploid wild relatives.

FIGURE 5.

FIGURE 5

Open in a new tab

Cis‐element analysis in the promoters of PR1s from I. batatas. The cis‐elements were divided into 18 broad categories. The corresponding color blocks matched to the class of homeopathic components.

3.7. Expression Patterns of PR1 Genes in Sweet Potato and Its Two Diploid Wild Relatives

3.7.1. Expression Analysis of PR1 Genes in I. trifida and I. triloba

Tissue‐specific expression profiles of PR1 genes in the two diploid wild relatives were obtained by analyzing public RNA‐seq datasets (available from GT4SP Data Download, uga.edu). Specifically, the expression data were derived from eight tissues of I. trifida (Figure 6A) and six tissues of I. triloba (Figure 6B), respectively. Our analysis demonstrated that the expression patterns of PR1 genes in diploid Ipomoea species exhibited distinct organ‐specific characteristics, indicating potential functional divergence. 74% ItfPR1s and 61% ItbPR1s showed high expression in flowers or flower‐buds, implying their potential roles in flower development and reproductive processes. Six ItfPR1s and twelve ItbPR1s were expressed in stems or leaves, suggesting their possible involvement in the vegetative growth processes. Most PR1 genes in two diploids displayed low expression levels in roots (Figure 6A,B). Notably, in the unique callus tissue of I. trifida , the expression levels of all PR1 genes in stem and flower were similar, and no significant high expression advantage was observed in floral organs (Figure 6A).

FIGURE 6.

FIGURE 6

Open in a new tab

The different tissues expression profiles of PR1 genes in (A) I. trifida and (B) I. triloba . The log of fragments per kilobase per million (FPKM) values is shown in the color blocks.

Furthermore, RNA‐seq data of I. trifida and I. triloba were used to analyze the expression patterns of PR1s under cold, heat, drought, salt and hormone treatments (Figure 7). In all the control and abiotic stress treatment groups of I. trifida and I. triloba , there were 32 (64%) and 18 (50%) genes that were not expressed respectively. Using a fold change of 2 as the threshold for differentially expressed genes (DEGs), in cold stress, there were 5 genes (ItfPR1‐31; ItfPR1‐32; ItbPR1‐15; ItbPR1‐19; ItbPR1‐34) that showed decreased expression, only ItbPR1‐24 showed upregulated. In heat stress, 6 genes (ItfPR1‐15; ItfPR1‐25; ItbPR1‐15; ItbPR1‐16; ItbPR1‐19; ItbPR1‐28) showed downregulated, 4 genes (ItfPR1‐31; ItfPR1‐32; ItbPR1‐23; ItbPR1‐24) showed upregulated. In drought stress, 5 genes (ItfPR1‐9; ItbPR1‐15; ItbPR1‐16; ItbPR1‐27; ItbPR1‐28) showed downregulated, 4 genes (ItfPR1‐31; ItfPR1‐32; ItfPR1‐47; ItbPR1‐34) showed upregulated. In salt stress, 4 genes (ItbPR1‐15; ItbPR1‐16; ItbPR1‐27; ItbPR1‐28) showed downregulated, 7 genes (ItfPR1‐24; ItfPR1‐31; ItfPR1‐32; ItfPR1‐47; ItbPR1‐30; ItbPR1‐34; ItbPR1‐35) showed upregulated. In IAA stress, 4 genes (ItfPR1‐15; ItfPR1‐32; ItbPR1‐34; ItbPR1‐35) showed downregulated, while no genes were upregulated. In the ABA treatment, there were the most DEGs, 7 genes (ItfPR1‐32; ItbPR1‐15; ItbPR1‐16; ItbPR1‐23; ItbPR1‐24; ItbPR1‐34; ItbPR1‐35) showed downregulated, 8 genes (ItfPR1‐15; ItfPR1‐24; ItfPR1‐27; ItfPR1‐31; ItbPR1‐19; ItbPR1‐29; ItbPR1‐30; ItbPR1‐31) showed upregulated. In GA stress, 7 genes (ItfPR1‐32; ItfPR1‐47; ItbPR1‐19; ItbPR1‐23; ItbPR1‐24; ItbPR1‐27; ItbPR1‐35) showed downregulated, only 1 gene (ItfPR1‐31) showed upregulated. The above results indicated that a portion of the PR1 family members in I. trifida and I. triloba can respond to abiotic stress and hormonal stimulation.

FIGURE 7.

FIGURE 7

Open in a new tab

The different abiotic stress and hormonal stimulation expression profiles of PR1 genes in (A) I. trifida and (B) I. triloba . The log of FPKM values is shown in the color blocks.

3.7.2. Expression Analysis of PR1 Genes in Sweet Potato

To analyze the expression patterns of PR1 members in sweet potato, the transcriptome data of Fusarium solani (NCBI data), Ceratocystis fimbriata (unpublished data), and drought stress (unpublished data) were analyzed. We only focused on the genes with a fold change of more than 2; we found that compared with the control group, only IbPR1‐5, IbPR1‐23, and IbPR1‐28 were upregulated in F. solani. However, from the overall expression trend, excluding the 15 genes that showed no expression, the number of genes showing upregulation and downregulation was similar (Figure 8A).

FIGURE 8.

FIGURE 8

Open in a new tab

The (A) Fusarium solani, (B) Ceratocystis fimbriata , and (C) drought stress expression profiles of PR1 genes in sweet potato. The log of TPM and FPKM values is shown in the color blocks.

C. fimbriata was used to inoculate NJ92 (resistant) and YT252 (sensitive), with samples collected at 4 and 8 days post‐inoculation. Compared with the control group, both of the two sweet potato varieties showed a trend of more upregulated expression genes as the duration of pathogen treatment increased (Figure 8B). In NJ92, the upregulated genes were IbPR1‐1, IbPR1‐5, IbPR1‐7, IbPR1‐23, IbPR1‐28, and IbPR1‐33, while there were no genes with a downregulation greater than 2‐fold in C. fimbriata treated 4 and 8 days. Additionally, these genes exhibited the characteristic that their expression levels increased with the duration of pathogen infection. This indicates that these PR1 genes are responding to the pathogen infection and initiating a defense response. For YT252, 4d vs. CK, IbPR1‐5, IbPR1‐7, and IbPR1‐28 were upregulated; IbPR1‐1 was downregulated; 8d vs. CK, only IbPR1‐5 and IbPR1‐28 were upregulated. It is speculated that YT252 is a susceptible variety, so the response effect of PR1s is less robust than NJ92.

Using 10% PEG6000 to simulate drought stress in Xu32 (sensitive), transcriptome sequencing was conducted on two tissues, leaves and roots (Figure 8C). The results showed that in the leaves, IbPR1‐1 and IbPR1‐5 were upregulated, while IbPR1‐8 and IbPR1‐9 were downregulated. In the roots, only IbPR1‐15 was upregulated; the downregulated genes were IbPR1‐1, IbPR1‐5, IbPR1‐8, IbPR1‐9, IbPR1‐14, IbPR1‐23, and IbPR1‐32. The qRT‐PCR results of these genes were consistent with the expression level of drought transcriptome (Figure 9). It indicated that the response of IbPR1s to drought stress may be exhibited tissue‐specific differences.

FIGURE 9.

FIGURE 9

Open in a new tab

Relative expression levels of 7 IbPR1s in sweet potato (A) leaves and (B) roots under drought stress. The x‐axes represent control (0 h) and drought treatment time (48 h); the y‐axes indicate the relative expression of IbPR1s; the significance of expression levels compared with control were denoted as *< 0.05, **< 0.01, ***< 0.001, ****< 0.0001.

Integrating the aforementioned transcriptome profiling results, we found that IbPR1‐5 exhibited an upregulated expression pattern under all three tested stress treatments. Furthermore, IbPR1‐5 clustered within the same phylogenetic clade (group 4) as the functionally characterized PR1 homolog (AT2G14610) from Arabidopsis (Figure 2) (van Loon et al. 2006), suggesting that IbPR1‐5 has the potential to serve as a promising candidate gene for stress resistance in sweet potato ( I. batatas ).

4. Discussion

PR1 proteins play a significant role in plant immunity (Huot et al. 2017). Currently, the identification and functional analysis of the PR1 protein family have been completed in multiple species (Han et al. 2023), such as Arabidopsis (van Loon et al. 2006), tomato (Akbudak et al. 2020), soybean (Almeida‐Silva and Venancio 2022), poplar (Wang et al. 2023), and S. miltiorrhiza (Fan et al. 2025). Despite its importance, comprehensive and systematic studies on PR1 genes in sweet potato and its wild relatives remain unexplored. This study represents the first comprehensive genomic analysis of PR1 genes in Ipomoea species with the aim of elucidating their roles in evolution and plant resistance breeding.

In this study, 33, 50 and 36 PR1 genes were identified from I. batatas , I. trifida and I. triloba , a relatively high number compared to that in other dicotyledonous and monocotyledonous plants (Akbudak et al. 2020; Chu et al. 2022; Zhang et al. 2022). Notably, the diploid I. trifida has more PR1 genes than the hexaploid sweet potato, which is distinct from the general trend of gene family expansion with polyploidization (e.g., wheat PR1 genes expanding with ploidy: 12 PR1s in tetraploid wheat; Zribi et al. 2023); 23 PR1s in hexaploid wheat (Lu et al. 2011). This suggests that I. trifida may have experienced a species‐specific PR1 gene expansion event, possibly driven by tandem duplication or transposon insertion, which warrants further investigation. Another possible speculation is that polyploidization was accompanied by PR1 genes loss or pseudogenization (Tossi et al. 2022). Most Ipomoea PR1 protein sequences were around 200 amino acids, whereas 12 (10%) PR1s exceed 500 amino acids (Table S1). This phenomenon is not unique to Ipomoea, as homologous PR1 members with sequences longer than 500 amino acids have also been identified in Hordeum vulgare (Yin et al. 2023) and Brassica juncea (Ali et al. 2025). Such sequence length variation may be attributed to factors including reference genome mis‐splicing, sequence duplication, and transposon insertion. For PR1 proteins structure, 70% Ipomoea PR1 genes contain only one exon and no intron (Figure 3B), this result was consistent with that of species such as tea (15 out of 17 CsPR1) (Zhang et al. 2022), banana (10 out of 11 MaPR1) (Anuradha et al. 2022), and Saccharum spontaneum (13 out of 19 ScPR1) (Chu et al. 2022), which indicated that the PR1 genes could be activated rapidly to respond to stresses,  likely due to a decrease in their intron density (Chen et al. 2018).

Phylogenetic analysis of the 141 PR1 genes across three Ipomoea Species and Arabidopsis was classified into five clades, as observed for banana (Anuradha et al. 2022), mango (Li et al. 2023), S. miltiorrhiza (Fan et al. 2025) and B. juncea (Ali et al. 2025), but not for soybean (Almeida‐Silva and Venancio 2022), durum wheat (Zribi et al. 2023) and rice (Liu and Xue, 2006), which were divided into three groups. Group 5 is the largest clade (containing 65 proteins), and I. trifida PR1 members accounting for the highest proportion within this clade. This finding aligns with the conclusion that “gene duplication is the core mechanism driving PR1 family expansion” in tea plants (Zhang et al. 2022). Considering the natural habitat of I. trifida , it can be speculated that the expansion of PR1 proteins in this group represents an evolutionary adaptation strategy of I. trifida to cope with complex environmental stressors.

The syntenic analysis of sweet potato, Arabidopsis, soybean and tomato showed a certain degree of conservation (Figure S4), especially IbPR1‐8 had conserved homologous pairs in all four species. To better characterize the evolutionary patterns of duplicated and syntenic PR1 gene pairs in the three Ipomoea species, Ka/Ks ratio analysis was conducted for these gene pairs. Our analysis revealed that most PR1 gene pairs displayed a Ka/Ks ratio below 1, whereas only a few possessed a Ka/Ks ratio above 1 (Table S4). Collectively, these results imply that purifying (negative) selection acts as the dominant evolutionary force on duplicated and syntenic PR1 genes during genome duplication and speciation events, while positive selection is restricted to a small portion of these genes (Hao et al. 2024; Hoffmann and Palmgren 2016; Shi et al. 2020; Wei et al. 2025). However, positive selection accelerates gene sequence divergence and functional specialization, thereby disrupting the integrity of syntenic blocks (Bowers et al. 2003).

The cis‐elements were identified in 119 Ipomoea PR1 genes (Figure 5; Figures S5 and S6) involved in light, hormone, stress and development response. ABA, SA and MeJA‐related cis‐elements were strongly linked to defense mechanisms. Additionally, stress‐responsive elements, such as drought and low‐temperature, indicated the potential involvement of PR1 genes in both biotic and abiotic stress responses.

The expression analysis of different tissues showed that most PR1 members in I. trifida and I. triloba were significantly highly expressed in flower tissues, which was consistent with S. miltiorrhiza (Fan et al. 2025). This result suggests that PR1 genes are not restricted to stress responses but may also be involved in the reproductive development process. Under abiotic stress and hormone treatments, more genes were downregulated in I. trifida and I. triloba , suggesting that PR1 might be negatively regulated in response to stress. Among them, ItbPR1‐15 was downregulated under all four stress conditions, while ItbPR1‐16 and ItbPR1‐28 were downregulated under heat, drought and salt treatments; ItfPR1‐32 and ItbPR1‐35 were downregulated under IAA, ABA and GA hormone conditions; meanwhile, ItfPR1‐32 and ItbPR1‐35 were orthologous genes, which might be the reason for their consistent expression results.

To investigate the expression patterns of PR1 members in sweet potato, we analyzed transcriptome datasets derived from three distinct stress conditions: infection by F. solani, infection by C. fimbriata , and exposure to drought stress. Under the three treatment conditions, the number of IbPR1 genes exhibiting a ≥ 2‐fold differential expression relative to the control group was relatively limited. Notably, IbPR1‐5 displayed significant upregulation across both biotic stress (i.e., F. solani and C. fimbriata infection) and abiotic stress (leaf under drought treatment) conditions. This cross‐stress responsive pattern not only highlights IbPR1‐5 as a priority target for subsequent functional characterization but also provides a valuable candidate gene for the genetic improvement of sweet potato—specifically for the development of germplasm with enhanced disease resistance and drought tolerance.

Many putative PR1 genes of Ipomoea in the transcriptome show negligible expression and are unresponsive to stress. This result is not unexpected, as low‐expression members are often found in many studies of the PR1 family (e.g., tomato (Akbudak et al. 2020); mango (Li et al. 2023)). Furthermore, we only evaluated 4 abiotic stresses (cold, heat, salt, drought), 3 hormones (IAA, ABA, GA), and 2 pathogens (F. solani, C. fimbriata ). PR1 genes often exhibit stress‐specific induction. For instance, wheat TaPR1 responds to freezing and stripe rust but not drought (Liu et al. 2023), while oat AvPR1 is induced by heat but not salt (AlHudaib et al. 2022). The low‐expression PR1s here may respond to untested stresses (e.g., heavy metals, UV radiation, or other pathogens) or combinatorial stresses (Suzuki et al. 2014). In addition, PR1 proteins are often regulated at the translation or secretion level. Published studies show that PR1 mRNA may be low, but proteins accumulate rapidly in apoplasts or pathogen‐infected sites (Breen et al. 2017; Luo et al. 2023). For example, tomato SlPR1 proteins are detected in leaves under drought stress even when transcript levels are not significantly upregulated (Akbudak et al. 2020). Thus, negligible transcript levels do not equate to non‐functional proteins.

5. Conclusions

This study characterized the PR1 gene family in I. batatas (sweet potato) and its wild relatives I. trifida and I. triloba . Using bioinformatic analyses, 119 PR1 genes were identified (33 in I. batatas , 50 in I. trifida , 36 in I. triloba ). Chromosomal localization showed disproportionate distribution, with the highest density on I. batatas chromosome 9 (8 genes), I. trifida chromosome 1 (8 genes) and I. triloba chromosome 1 (12 genes). Phylogenetic analysis of Ipomoea and A. thaliana PR1s clustered the 141 PR1s into five groups, indicating evolutionary conservation and potential functional specialization. Conserved domain analysis revealed that the majority of PR1 family members harbor intact CAP1‐4 motifs. In contrast, members with incomplete CAP motifs were designated as PR1‐like proteins. 70% of PR1 genes had one exon, while IbPR1‐30 (16 exons) suggested complexity. Syntenic analysis revealed 4, 0, 2 intra‐species homologous pairs (in I. batatas , I. trifida , I. triloba , respectively) and 44 inter‐species orthologous pairs, with cross‐species conservation. Ka/Ks analysis showed 92.2% of pairs underwent purifying selection (Ka/Ks < 1), with a few under positive selection. Cis‐element analysis found light‐responsive elements most abundant (49.4%), followed by hormone and abiotic stress‐responsive elements. Expression profiling showed two wild relatives PR1s highly expressed in flowers/flower buds and responsive to stresses/hormones (e.g., 15 ABA‐induced DEGs). In sweet potato, IbPR1‐5 was consistently upregulated under F. solani, C. fimbriata and drought; while drought responses were tissue‐specific (e.g., IbPR1‐1 up in leaves, down in roots), with qRT‐PCR validation. These results clarify Ipomoea PR1 characteristics, highlighting IbPR1‐5 as a candidate for sweet potato stress resistance improvement.

Author Contributions

Zongyun Li: investigation, conceptualization. Xiaowan Gou: writing – original draft, conceptualization. Ziyi Wang: formal analysis, project administration. Meiyan Liu: data curation. Mingku Zhu: methodology, conceptualization. Fei Zhang: data curation. Yanfei Ping: data curation.

Funding

This work was supported by the earmarked fund for CARS‐10‐Sweetpotato and Basic Research Program of Jiangsu (BK20231174).

Ethics Statement

The authors have nothing to report.

Conflicts of Interest

The authors declare no conflicts of interest.

Supporting information

Figure S1: Predicted 3D structure of the 119 PR1 proteins. (A) I. batatas , (B) I. trifida, and (C) I. triloba .

FSN3-14-e71622-s001.jpg (7.5MB, jpg)

Figure S2: Conserved motifs of the Ipomoea PR1 proteins. Each motif is marked with a specific color and a unique number (1–15).

FSN3-14-e71622-s010.jpg (1.5MB, jpg)

Figure S3: Multiple sequence alignment of Ipomoea PR1 proteins. (A) I. batatas , (B) I. trifida, and (C) I. triloba . The blue lines represent CAP1‐4 motifs and CAPE (CAP‐derived peptide). The green rectangle represented the caveolin‐binding motif (CBM). The blue asterisk represents six cysteine motifs.

FSN3-14-e71622-s008.jpg (9.6MB, jpg)

Figure S4: Syntenic analysis of the PR1 genes between I. batatas , A. thaliana , soybean ( Glycine max (L.) Merr.), and tomato ( Solanum lycopersicum L.).

FSN3-14-e71622-s007.tif (5.3MB, tif)

Figure S5: Cis‐element analysis in the promoters of PR1s from I. trifida. The cis‐elements were divided into 17 broad categories. The corresponding color blocks matched to the class of homeopathic components.

FSN3-14-e71622-s003.jpg (3.4MB, jpg)

Figure S6: Cis‐element analysis in the promoters of PR1s from I. triloba. The cis‐elements were divided into 18 broad categories. The corresponding color blocks matched to the class of homeopathic components.

FSN3-14-e71622-s011.jpg (3.6MB, jpg)

Table S1: Molecular information of the 119 PR1s identified in the three Ipomoea species.

FSN3-14-e71622-s002.xlsx (19.6KB, xlsx)

Table S2: Positions of the CAP domain in 119 Ipomoea PR1 sequences detected by NCBI CD‐search.

FSN3-14-e71622-s006.xlsx (19.1KB, xlsx)

Table S3: Orthologous PR1 gene pairs in the three Ipomoea species.

FSN3-14-e71622-s004.xlsx (11.3KB, xlsx)

Table S4: Ka and Ks of duplicated PR1 genes within or between sweet potato, I. trifida , and I. triloba .

FSN3-14-e71622-s009.xlsx (13.8KB, xlsx)

Table S5: qRT‐PCR primer sequences.

FSN3-14-e71622-s005.xlsx (10.4KB, xlsx)

Acknowledgments

The authors have nothing to report.

Contributor Information

Zongyun Li, Email: zongyunli@jsnu.edu.cn.

Xiaowan Gou, Email: gouxw@jsnu.edu.cn.

Data Availability Statement

Data sharing not applicable to this article as no datasets were generated or analyzed during the current study.

References

  1. Akbudak, M. A. , Yildiz S., and Filiz E.. 2020. “Pathogenesis Related Protein‐1 (PR‐1) Genes in Tomato ( Solanum lycopersicum L.): Bioinformatics Analyses and Expression Profiles in Response to Drought Stress.” Genomics 112, no. 6: 4089–4099. 10.1016/j.ygeno.2020.07.004. [DOI] [PubMed] [Google Scholar]
  2. AlHudaib, K. A. , Alanazi N. A., Ghorbel M., El‐Ganainy S. M., and Brini F.. 2022. “Isolation and Characterization of a Novel Pathogenesis‐Related Protein‐1 Gene (AvPR‐1) With Induced Expression in Oat (Avena sativa L.) During Abiotic and Hormonal Stresses.” Plants 11, no. 17: 2284. 10.3390/plants11172284. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Ali, S. , Mishra A. K., Singh M., et al. 2025. “Genome‐Wide Identification and Characterization of Pathogenesis Related Protein 1 Gene Family in Brassica juncea .” International Journal of Biological Macromolecules 312: 144066. 10.1016/j.ijbiomac.2025.144066. [DOI] [PubMed] [Google Scholar]
  4. Almeida‐Silva, F. , and Venancio T. M.. 2022. “Pathogenesis‐Related Protein 1 (PR‐1) Genes in Soybean: Genome‐Wide Identification, Structural Analysis and Expression Profiling Under Multiple Biotic and Abiotic Stresses.” Gene 809: 146013. 10.1016/j.gene.2021.146013. [DOI] [PubMed] [Google Scholar]
  5. Anuradha, C. , Chandrasekar A., Backiyarani S., Thangavelu R., Giribabu P., and Uma S.. 2022. “Genome‐Wide Analysis of Pathogenesis‐Related Protein 1 (PR‐1) Gene Family From Musa spp. and Its Role in Defense Response During Stresses.” Gene 821: 146334. 10.1016/j.gene.2022.146334. [DOI] [PubMed] [Google Scholar]
  6. Bowers, J. E. , Chapman B. A., Rong J., and Paterson P. A.. 2003. “Unravelling Angiosperm Genome Evolution by Phylogenetic Analysis of Chromosomal Duplication Events.” Nature 422: 433–438. 10.1038/nature01521. [DOI] [PubMed] [Google Scholar]
  7. Breen, S. , Williams S. J., Outram M., Kobe B., and Solomon P. S.. 2017. “Emerging Insights Into the Functions of Pathogenesis‐Related Protein 1.” Trends in Plant Science 22, no. 10: 871–879. 10.1016/j.tplants.2017.06.013. [DOI] [PubMed] [Google Scholar]
  8. Chen, C. , Wu Y., Li J., et al. 2023. “TBtools‐II: A “One for All, All for One” Bioinformatics Platform for Biological Big‐Data Mining.” Molecular Plant 16, no. 11: 1733–1742. 10.1016/j.molp.2023.09.010. [DOI] [PubMed] [Google Scholar]
  9. Chen, J. , Gao T., Wan S., et al. 2018. “Genome‐Wide Identification, Classification and Expression Analysis of the HSP Gene Superfamily in Tea Plant (Camellia sinensis).” International Journal of Molecular Sciences 19, no. 9: 2633. 10.3390/ijms19092633. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Chu, N. , Zhou J., Rott P., et al. 2022. “ScPR1 Plays a Positive Role in the Regulation of Resistance to Diverse Stresses in Sugarcane (Saccharum spp.) and Arabidopsis thaliana .” Industrial Crops and Products 180: 114736. 10.1016/j.indcrop.2022.114736. [DOI] [Google Scholar]
  11. Dixit, S. , Sivalingam P. N., Baskaran R. K. M., Senthil‐Kumar M., and Ghosh P. K.. 2024. “Plant Responses to Concurrent Abiotic and Biotic Stress: Unravelling Physiological and Morphological Mechanisms.” Plant Physiology Reports 29, no. 1: 6–17. 10.1007/s40502-023-00766-0. [DOI] [Google Scholar]
  12. Fan, H. , Zhou J., Wang Q., et al. 2025. “Comprehensive Genome‐Wide Analysis and Expression Profiling of Pathogenesis‐Related Protein 1 (PR‐1) Genes in Salvia miltiorrhiza .” Food Science & Nutrition 13: e70117. 10.1002/fsn3.70117. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Han, C. , Wang Q., Su Z., et al. 2025. “PATHOGENESIS‐RELATED PROTEINS: Identification, Evolution and Functional Analysis in Pear (Pyrus bretschneideri).” Horticulture Advances 3, no. 1: 10. 10.1007/s44281-025-00064-9. [DOI] [Google Scholar]
  14. Han, Z. , and Schneiter R.. 2024. “Dual Functionality of Pathogenesis‐Related Proteins: Defensive Role in Plants Versus Immunosuppressive Role in Pathogens.” Frontiers in Plant Science 15: 1368467. 10.3389/fpls.2024.1368467. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Han, Z. , Xiong D., Schneiter R., and Tian C.. 2023. “The Function of Plant PR1 and Other Members of the CAP Protein Superfamily in Plant–Pathogen Interactions.” Molecular Plant Pathology 24, no. 6: 651–668. 10.1111/mpp.13320. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hao, X. , Liu F., Liu L., et al. 2024. “Zucchini Yellow Mosaic Virus‐Induced Hypersensitive Response Is Associated With Pathogenesis‐Related 1 Protein Expression and Confers Resistance in Watermelon.” Plant Cell Reports 43, no. 12: 277. 10.1007/s00299-024-03364-y. [DOI] [PubMed] [Google Scholar]
  17. Hirakawa, H. , Okada Y., Tabuchi H., et al. 2015. “Survey of Genome Sequences in a Wild Sweet Potato, Ipomoea trifida (H. B. K.) G. Don.” DNA Research 22, no. 2: 171–179. 10.1093/dnares/dsv002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hoffmann, R. D. , and Palmgren M.. 2016. “Purifying Selection Acts on Coding and Non‐Coding Sequences of Paralogous Genes in Arabidopsis thaliana .” BMC Genomics 17: 456. 10.1186/s12864-016-2803-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Huot, B. , Castroverde C. D. M., Velásquez A. C., et al. 2017. “Dual Impact of Elevated Temperature on Plant Defence and Bacterial Virulence in Arabidopsis .” Nature Communications 8, no. 1: 1808. 10.1038/s41467-017-01674-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Irigoyen, M. L. , Garceau D. C., Bohorquez‐Chaux A., et al. 2020. “Genome‐Wide Analyses of Cassava Pathogenesis‐Related (PR) Gene Families Reveal Core Transcriptome Responses to Whitefly Infestation, Salicylic Acid and Jasmonic Acid.” BMC Genomics 21, no. 1: 93. 10.1186/s12864-019-6443-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Joshi, V. , Joshi N., Vyas A., and Jadhav S. K.. 2021. “Pathogenesis‐Related Proteins: Role in Plant Defense.” In Biocontrol Agents and Secondary Metabolites, 573–590. Woodhead Publishing. 10.1016/b978-0-12-822919-4.00025-9. [DOI] [Google Scholar]
  22. Kothari, K. S. , Dansana P. K., Giri J., and Tyagi A. K.. 2016. “Rice Stress Associated Protein 1 (OsSAP1) Interacts With Aminotransferase (OsAMTR1) and Pathogenesis‐Related 1a Protein (OsSCP) and Regulates Abiotic Stress Responses.” Frontiers in Plant Science 7: 1057. 10.3389/fpls.2016.01057. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Li, J. , Luo C., Yang X., et al. 2023. “Genome‐Wide Identification of the Mango Pathogenesis‐Related 1 (PR1) Gene Family and Functional Analysis of MiPR1A Genes in Transgenic Arabidopsis .” Scientia Horticulturae 321: 112254. 10.1016/j.scienta.2023.112254. [DOI] [Google Scholar]
  24. Li, Z. , Dhekney S. A., and Gray D. J.. 2011. “PR‐1 Gene Family of Grapevine: A Uniquely Duplicated PR‐1 Gene From a Vitis Interspecific Hybrid Confers High Level Resistance to Bacterial Disease in Transgenic Tobacco.” Plant Cell Reports 30, no. 1: 1–11. 10.1007/s00299-010-0934-5. [DOI] [PubMed] [Google Scholar]
  25. Lincoln, J. E. , Sanchez J. P., Zumstein K., and Gilchrist D. G.. 2018. “Plant and Animal PR1 Family Members Inhibit Programmed Cell Death and Suppress Bacterial Pathogens in Plant Tissues.” Molecular Plant Pathology 19, no. 9: 2111–2123. 10.1111/mpp.12685. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Liu, R. , Lu J., Xing J., Xue L., Wu Y., and Zhang L.. 2023. “Characterization and Functional Analyses of Wheat TaPR1 Genes in Response to Stripe Rust Fungal Infection.” Scientific Reports 13, no. 1: 3362. 10.1038/s41598-023-30456-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Liu, Q., and Q. Xue. 2006. Computational Identification of Novel PR‐1‐Type Genes in Oryza Sativa. J Genet 85, no. 3: 193–198. 10.1007/bf02935330. [DOI] [PubMed] [Google Scholar]
  28. Lu, S. , Friesen T. L., and Faris J. D.. 2011. “Molecular Characterization and Genomic Mapping of the Pathogenesis‐Related Protein 1 (PR‐1) Gene Family in Hexaploid Wheat ( Triticum aestivum L.).” Molecular Genetics and Genomics 285, no. 6: 485–503. 10.1007/s00438-011-0618-z. [DOI] [PubMed] [Google Scholar]
  29. Luo, X. , Tian T., Feng L., et al. 2023. “Pathogenesis‐Related Protein 1 Suppresses Oomycete Pathogen by Targeting Against AMPK Kinase Complex.” Journal of Advanced Research 43: 13–26. 10.1016/j.jare.2022.02.002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Saijo, Y. , and Loo E. P.. 2019. “Plant Immunity in Signal Integration Between Biotic and Abiotic Stress Responses.” New Phytologist 225, no. 1: 87–104. 10.1111/nph.15989. [DOI] [PubMed] [Google Scholar]
  31. Schneiter, R. , and Di Pietro A.. 2013. “The CAP Protein Superfamily: Function in Sterol Export and Fungal Virulence.” Biomolecular Concepts 4, no. 5: 519–525. 10.1515/bmc-2013-0021. [DOI] [PubMed] [Google Scholar]
  32. Sels, J. , Mathys J., De Coninck B. M. A., Cammue B. P. A., and De Bolle M. F. C.. 2008. “Plant Pathogenesis‐Related (PR) Proteins: A Focus on PR Peptides.” Plant Physiology and Biochemistry 46, no. 11: 941–950. 10.1016/j.plaphy.2008.06.011. [DOI] [PubMed] [Google Scholar]
  33. Seo, P. J. , Lee A. K., Xiang F., and Park C. M.. 2008. “Molecular and Functional Profiling of Arabidopsis Pathogenesis‐Related Genes: Insights Into Their Roles in Salt Response of Seed Germination.” Plant and Cell Physiology 49, no. 3: 334–344. 10.1093/pcp/pcn011. [DOI] [PubMed] [Google Scholar]
  34. Shi, T. , Rahmani R. S., Gugger P. F., et al. 2020. “Distinct Expression and Methylation Patterns for Genes With Different Fates Following a Single Whole‐Genome Duplication in Flowering Plants.” Molecular Biology and Evolution 37, no. 8: 2394–2413. 10.1093/molbev/msaa105. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Sun, J. , Yu L., Cai Z., et al. 2019. “Comparative Karyotype Analysis Among Six Species of Ipomoea Based on Two Newly Identified Repetitive Sequences.” Genome 62, no. 4: 243–252. 10.1139/gen-2018-0169. [DOI] [PubMed] [Google Scholar]
  36. Sung, Y. C. , Outram M. A., Breen S., et al. 2021. “PR1‐Mediated Defence via C‐Terminal Peptide Release Is Targeted by a Fungal Pathogen Effector.” New Phytologist 229, no. 6: 3467–3480. 10.1111/nph.17128. [DOI] [PubMed] [Google Scholar]
  37. Suzuki, N. , Rivero R. M., Shulaev V., Blumwald E., and Mittler R.. 2014. “Abiotic and Biotic Stress Combinations.” New Phytologist 203, no. 1: 32–43. 10.1111/nph.12797. [DOI] [PubMed] [Google Scholar]
  38. Tossi, V. E. , Martínez Tosar L. J., Laino L. E., et al. 2022. “Impact of Polyploidy on Plant Tolerance to Abiotic and Biotic Stresses.” Frontiers in Plant Science 13: 869423. 10.3389/fpls.2022.869423. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. van Loon, L. C. , and Kammen A.. 1970. “Polyacrylamide Disc Electrophoresis of the Soluble Leaf Proteins From Nicotiana tabacum Var. “Samsun” and “Samsun NN”. II. Changes in Protein Constitution After Infection With Tobacco Mosaic Virus.” Virology 40, no. 2: 190–211. 10.1016/0042-6822(70)90395-8. [DOI] [PubMed] [Google Scholar]
  40. van Loon, L. C. , Rep M., and Pieterse C. M. J.. 2006. “Significance of Inducible Defense‐Related Proteins in Infected Plants.” Annual Review of Phytopathology 44, no. 1: 135–162. 10.1146/annurev.phyto.44.070505.143425. [DOI] [PubMed] [Google Scholar]
  41. Wang, J. , Mao X., Wang R., et al. 2019. “Identification of Wheat Stress‐Responding Genes and TaPR‐1‐1 Function by Screening a cDNA Yeast Library Prepared Following Abiotic Stress.” Scientific Reports 9, no. 1: 141. 10.1038/s41598-018-37859-y. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Wang, P. , Zhou J., Sun W., Li H., Li D., and Zhuge Q.. 2023. “Characteristics and Function of the Pathogenesis‐Related Protein 1 Gene Family in Poplar.” Plant Science 336: 111857. 10.1016/j.plantsci.2023.111857. [DOI] [PubMed] [Google Scholar]
  43. Wei, S. , Zheng B., Wang S., Yang X., Chen Y., and Yin T.. 2025. “Integrated Analysis of Populus deltoides PR1 Genes Uncovered a PdePR1 as a Defense Marker Against Foliar Rust.” Plant Physiology and Biochemistry 222: 109769. 10.1016/j.plaphy.2025.109769. [DOI] [PubMed] [Google Scholar]
  44. Wu, S. , Lau K. H., Cao Q., et al. 2018. “Genome Sequences of Two Diploid Wild Relatives of Cultivated Sweetpotato Reveal Targets for Genetic Improvement.” Nature Communications 9, no. 1: 4580. 10.1038/s41467-018-06983-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Yang, J. , Moeinzadeh M. H., Kuhl H., et al. 2017. “Haplotype‐Resolved Sweet Potato Genome Traces Back Its Hexaploidization History.” Nature Plants 3, no. 9: 696–703. 10.1038/s41477-017-0002-z. [DOI] [PubMed] [Google Scholar]
  46. Yin, W., Y. Bai, S. Wang, et al. 2023. Genome‐Wide Analysis of Pathogenesis‐Related Protein‐1 (PR‐1) Genes From Qingke (Hordeum vulgare L. var. nudum) Reveals Their Roles in Stress Responses. Heliyon 9 no. 4: e14899. 10.1016/j.heliyon.2023.e14899. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Zhang, Q. , Guo N., Zhang Y., Yu Y., and Liu S.. 2022. “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.” International Journal of Molecular Sciences 23, no. 3: 1292. 10.3390/ijms23031292. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Zribi, I. , Ghorbel M., Haddaji N., Besbes M., and Brini F.. 2023. “Genome‐Wide Identification and Expression Profiling of Pathogenesis‐Related Protein 1 (PR‐1) Genes in Durum Wheat (Triticum durum Desf.).” Plants 12, no. 10: 1998. 10.3390/plants12101998. [DOI] [PMC free article] [PubMed] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Figure S1: Predicted 3D structure of the 119 PR1 proteins. (A) I. batatas , (B) I. trifida, and (C) I. triloba .

FSN3-14-e71622-s001.jpg (7.5MB, jpg)

Figure S2: Conserved motifs of the Ipomoea PR1 proteins. Each motif is marked with a specific color and a unique number (1–15).

FSN3-14-e71622-s010.jpg (1.5MB, jpg)

Figure S3: Multiple sequence alignment of Ipomoea PR1 proteins. (A) I. batatas , (B) I. trifida, and (C) I. triloba . The blue lines represent CAP1‐4 motifs and CAPE (CAP‐derived peptide). The green rectangle represented the caveolin‐binding motif (CBM). The blue asterisk represents six cysteine motifs.

FSN3-14-e71622-s008.jpg (9.6MB, jpg)

Figure S4: Syntenic analysis of the PR1 genes between I. batatas , A. thaliana , soybean ( Glycine max (L.) Merr.), and tomato ( Solanum lycopersicum L.).

FSN3-14-e71622-s007.tif (5.3MB, tif)

Figure S5: Cis‐element analysis in the promoters of PR1s from I. trifida. The cis‐elements were divided into 17 broad categories. The corresponding color blocks matched to the class of homeopathic components.

FSN3-14-e71622-s003.jpg (3.4MB, jpg)

Figure S6: Cis‐element analysis in the promoters of PR1s from I. triloba. The cis‐elements were divided into 18 broad categories. The corresponding color blocks matched to the class of homeopathic components.

FSN3-14-e71622-s011.jpg (3.6MB, jpg)

Table S1: Molecular information of the 119 PR1s identified in the three Ipomoea species.

FSN3-14-e71622-s002.xlsx (19.6KB, xlsx)

Table S2: Positions of the CAP domain in 119 Ipomoea PR1 sequences detected by NCBI CD‐search.

FSN3-14-e71622-s006.xlsx (19.1KB, xlsx)

Table S3: Orthologous PR1 gene pairs in the three Ipomoea species.

FSN3-14-e71622-s004.xlsx (11.3KB, xlsx)

Table S4: Ka and Ks of duplicated PR1 genes within or between sweet potato, I. trifida , and I. triloba .

FSN3-14-e71622-s009.xlsx (13.8KB, xlsx)

Table S5: qRT‐PCR primer sequences.

FSN3-14-e71622-s005.xlsx (10.4KB, xlsx)

Data Availability Statement

Data sharing not applicable to this article as no datasets were generated or analyzed during the current study.

Articles from Food Science & Nutrition are provided here courtesy of Wiley

RESOURCES