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Article

Whole-Genome Identification and Analysis of Carbohydrate Esterase Gene Family in Colletotrichum graminicola

by
Wenting Zhu
1,†,
Limin Wang
1,†,
Honglian Li
1,
Yan Shi
1,2,
Jiaxin Chang
1,
Senbo Wang
1,
Xu Liu
1,
Penghao Ma
1,
Jinzhang Zhao
1,
Yan Liu
1 and
Yafei Wang
1,*
1
College of Plant Protection, Henan Agricultural University, Zhengzhou 450002, China
2
State Key Laboratory of High-Efficiency Production of Wheat-Maize Double Cropping, Zhengzhou 450046, China
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Agriculture 2025, 15(7), 781; https://doi.org/10.3390/agriculture15070781
Submission received: 23 February 2025 / Revised: 25 March 2025 / Accepted: 2 April 2025 / Published: 3 April 2025
(This article belongs to the Special Issue Detection, Diagnostics and Management Control Strategies of Plant Pathogens)
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Abstract

:
Colletotrichum graminicola can cause leaf spots and stalk rot in maize. The primary function of carbohydrate esterases (CEs) is to eliminate ester modifications from monosaccharides, oligosaccharides, and polysaccharides, thereby facilitating the hydrolysis of sugars. We identified 128 CE genes through whole-genome analysis and functional annotation of C. graminicola TZ–3 here. We further analyzed the physicochemical properties, subcellular localization, conserved motifs, gene structures, promoter regulatory elements of these 128 C. graminicola CE (CgCE) genes. Our results indicated that half of the CgCE proteins were located extracellularly. The CgCE proteins demonstrated diversity in both their structures and motifs. Furthermore, the CgCE gene family contained numerous conserved domains, suggesting potential functional diversity. Regulatory elements associated with various stresses and plant hormones were identified in this study. GO enrichment and expression pattern analysis indicated that the CgCE genes were involved in metabolic processes and might contribute to the establishment of fungal infections and lesion expansion. These results enhance our understanding of the CE family genes in C. graminicola and provide a foundation for further investigations into their roles in fungal pathogenesis.

1. Introduction

Carbohydrates, often termed sugars, serve as the primary energy source essential for sustaining all biological processes [1]. Enzymes that act on carbohydrate structures form one of the most diverse groups of proteins on Earth. The carbohydrate active enzyme database classifies these enzymes into six categories based on sequence similarity, among which carbohydrate esterase (CE) is an important category [2].
CEs are enzymes that remove ester bond modifications and enhance the activity of glycoside hydrolases on complex polysaccharides [2,3]. The pectin methyl esterases, which make up the CE8 family in microorganisms, play a crucial role in the invasion of plant tissues by pathogens [4]. They can smooth the cell wall, allowing for the action of depolymerases. The structural diversity of CEs determines their substrate specificity, allowing these enzymes to act on substrates such as chitin and hemicellulose [5]. Among the most abundant polysaccharides in nature, the principal ones are those that constitute the cell walls of plants and chitin presented in fungi and arthropoda [6,7]. These polysaccharides provide structural integrity and protective functions, helping to defend against various environmental pathogens. Chitin deacetylases regulate the deacetylation of chitin, minimizing variability in this process [8,9]. Within plant cell wall polysaccharides, CEs facilitate the decomposition of these materials by removing acetyl group modifications [4]. This action assists pathogens in circumventing the multiple barriers of the plant cell wall, including the cuticle, pectin-rich cell wall, and xylan, thereby promoting the invasion of pathogens into plant cells [10,11,12,13,14,15].
Corn is a primary staple food worldwide, with its planting area and total production second only to rice and wheat [16]. Its production plays an essential role in global food security. Corn anthracnose, caused by Colletotrichum graminicola, is a severe fungal disease that can result in maize leaf blight and stalk rot [17,18,19,20,21]. This pathogen can also infect other gramineous crops, such as wheat and sorghum, leading to significant economic losses in agriculture [22,23]. Currently, the primary methods for controlling corn anthracnose rely on benzimidazole chemical agents. However, this chemical control can result in pathogen resistance, pesticide residues, and environmental pollution [24]. Biological or genetic control has the characteristics of safety and efficiency and is a rational choice for preventing the disease. Analyzing the pathogenic factors associated with C. graminicola can yield specific targets for the development of safe and effective new agents and provide a theoretical foundation for breeding disease-resistant crops.
Recent advancements in high-throughput sequencing technology and molecular biology have led researchers to focus on the genomic structure and pathogenic mechanisms of C. graminicola [25]. Researchers have identified 24 Common in Fungal Extracellular Membrane (CFEM) proteins through genomic analysis of C. graminicola and found that 10 CFEM proteins are involved in the fungal pathogenic process, playing an important role in the interaction between C. graminicola and maize hosts [25]. In this study, we identified all CE genes from the C. graminicola TZ-3 genome and analyzed their physicochemical properties. We conducted phylogenetic analysis to examine their evolutionary relationships and employed bioinformatics tools to assess their structural characteristics. Additionally, we performed gene functional enrichment and gene expression pattern analyses. These analyses have created conditions for the functional study of CEs during fungal infection.

2. Results

2.1. Identification of CE Genes and Analysis of Their Physicochemical Properties

We identified 128 CE genes (designated as CgCE1–CgCE128) within the genome of C. graminicola TZ-3 and assessed their physicochemical properties, with detailed characteristics provided in Table 1. All CgCE proteins are divided into 12 superfamilies. Notably, 57 CgCE proteins belong to the CE10 superfamily, 20 belong to the CE1 superfamily, 16 belong to the CE4 superfamily, and 12 belong to the CE5 superfamily. The molecular weights of these CgCE proteins varied from 20.46 kDa to 288.11 kDa, with CgCE118 exhibiting the smallest theoretical molecular weight and CgCE35 the largest. Among the 128 CgCE proteins, the number of amino acids varied from 205 to 2648, with 125 proteins containing fewer than 1000 amino acids. The isoelectric points of these proteins ranged from 4.49 (CgCE40) to 9.69 (CgCE104), including 100 acidic (pI < 6.5), 20 basic (pI > 7.5), and 8 neutral proteins (6.5 < pI ≤ 7.5). The GRAVY values of these proteins ranged from −0.63 (CgCE19) to 0.858 (CgCE4), indicating that 106 CgCEs are hydrophilic (GRAVY < 0) and 22 CgCEs are hydrophobic (GRAVY > 0). Additionally, we conducted predictions for subcellular localization of CgCE proteins and found that 68 were secreted and therefore, located extracellularly, 27 in the cytosol and 18 in the mitochondria (Table 1).

2.2. Phylogenetic Analysis

Using the protein sequences of 128 CgCEs, a Neighbor-Joining (NJ) tree was constructed with MEGA7.0 to analyze relationships among CgCEs. As illustrated in Figure 1, they can be categorized into nine groups. Group V contains most members (33), followed by group VI (27). In the phylogenetic tree, group I and group II are close to each other, indicating a close evolutionary relationship. In contrast, the distance between group I and group IX is the farthest, indicating a distant evolutionary relationship between the two groups.

2.3. Structural Analysis of CgCEs

Gene structure analysis showed the differences of CgCEs’ structural characteristics, with CgCE80 containing 10 introns and 24 CgCE genes lacking introns (Figure 2A). This variability in CgCE genes suggested potential gene loss and gain events in the evolutionary trajectory of the CE gene family. They may exhibit functional differences, underscoring the importance of further functional analyses. Analysis of the protein structural domains of CgCEs revealed that 128 CgCE proteins possess a rich array of superfamily domains, with CgCE103 even containing seven superfamily domains (Figure 2B). It is worth noting that the abhydrolase superfamily domain is most abundant.
We also performed motif analysis on CgCE protein sequences and identified 10 different motifs (Figure S1, Table S1). Proteins with more identical conserved motifs have closer evolutionary relationships and may have more similar functional characteristics. CgCEs possess varying numbers and types of motifs, with Motif 2 being the most common, detected in 63 CgCE proteins, followed by Motif 3, found in 51 CE proteins. Motif 9 was only found in 6 CE proteins. Notably, 5 motifs (Motif 1, Motif 3, Motif 4, Motif 5, and Motif 6) were present in 16 CgCE proteins (CgCE1, CgCE16, CgCE18, CgCE23, CgCE25, CgCE30, CgCE33, CgCE45, CgCE46, CgCE62, CgCE64, CgCE65, CgCE75, CgCE78, CgCE115, CgCE116). Additionally, Motifs 7, 8, and 10 were concurrently present in 7 CgCE proteins (CgCE3, CgCE8, CgCE20, CgCE34, CgCE42, CgCE63, CgCE119), indicating that they may have similar biological functions (Figure 3).

2.4. Analysis of the Promoter Regulatory Elements of CgCEs

Promoter sequences possess regulatory functions [26,27]. The analysis of promoter regulatory elements revealed a diverse array of cis-acting regulatory elements (CAREs) present in the promoter regions of the CgCE genes (Figure 4 and Table S2), which are predominantly linked to functions in development, pathogenicity, and stress responses. We concentrated on some categories of CAREs within the CgCE gene promoters. We found that many CAREs were associated with various plant hormones, such as jasmonic acid, abscisic acid, auxin, gibberellin, and salicylic acid. There were also some CAREs related to low temperature, drought, and defense. In addition, we also identified numerous light responsive elements that are associated with growth and development. Among these, MeJA response elements were the most prevalent, with 1,074 occurrences, followed by light (993 occurrences) and ABA response elements (479 occurrences) (Figure S2, Table S2). Furthermore, the CgCE gene also contains CAREs related to anaerobic induction (ARE) and callus tissue expression (CAT-box). Collectively, these CAREs underscore the potential involvement of the CgCE proteins in a variety of biological processes. Consequently, these findings offer valuable insights into the role of the CgCE gene family within the intricate regulatory networks governing developmental processes, pathogenesis, and stress responses.

2.5. Gene Ontology (GO) Enrichment Analysis of CgCEs

We conducted the GO enrichment analysis on 128 CgCE genes. These CgCE genes are predominantly enriched in carbohydrate metabolic processes (GO:0005975), polysaccharide catabolism (GO:0000272), polysaccharide metabolism (GO:0005976), and carbohydrate catabolism (GO:0016052) (Table S3). Notably, the most significant enrichment of CgCE genes was observed in metabolic processes, emphasizing their crucial role in metabolic activities, particularly in carbohydrate catabolism (Figure 5).

2.6. CgCE Gene Expression Pattern Analysis

To elucidate the infection-related CgCE gene family, transcriptomic data were analyzed and confirmed by RT-qPCR. We constructed an expression heatmap based on the Fragments Per Kilobase Million (FPKM) values of 128 CgCE genes (Figure 6). CgCE genes can be categorized into six distinct classes. Class I, IV and VI contain a total of 49 CgCEs. During the infection process, there was no significant difference in the expression changes of these genes at different time points. Class II and III contain a total of 46 CgCEs, which have high levels of expression at 24 h. Class V consists of 33 CgCEs, which have a high level of expression at 60 h. The differential expression profiles of CgCE genes at different infection time points suggest that they may have distinct functional roles. To validate the integrity of the transcriptomic data, we randomly selected eight genes and designed specific primers for RT-qPCR analysis (Table S4). UBQ gene was chosen as the reference gene and RT-qPCR values were standardized. The RT-qPCR results of eight CgCE genes largely aligned with the trends observed in the transcriptomic data, thereby confirming the reliability of these findings (Figure 7). Our analysis revealed the expression patterns of CgCE genes during pathogen infection, providing a reference for studying their roles in host–microbe interactions.

3. Discussion

CEs play a critical role in the breakdown of cellulose and hemicellulose within plant cell walls, assisting pathogens in circumventing the barriers present on the surface of plant cells. This process increases the susceptibility of plant cells to infection, thereby facilitating the infiltration of pathogens into these cells [4]. A comprehensive analysis of CgCEs can help us broaden our understanding of CEs’ roles.
A total of 128 CgCEs were identified in this study. The majority of CgCE proteins are characterized as hydrophilic and acidic. Phylogenetic analysis categorized these 128 CgCE proteins into nine distinct clades, with those sharing similar structural domains clustered together. CgCEs residing in different clades exhibit more distant evolutionary relationships, suggesting potential differences in their structure and function. These CgCE proteins are predominantly situated in the extracellular space, cytoplasmic membrane, mitochondria, cytoskeleton, and cytoplasm, implying the possibility of varied functions in these compartments. More than half of the CgCE proteins are located in the extracellular space, indicating their likely primary involvement in extracellular activities. Our results support the known function of CEs, which act on the cell wall and play a role in invading plant tissues [4].
The distribution of introns within microbial genes exhibits discrete characteristics [28]. Gene structure analysis reveals variations in intron numbers among different CgCE genes. Even genes situated on the same phylogenetic branch frequently display differences in intron count, suggesting that evolutionary events in the CgCE gene family may involve the acquisition or loss of introns. Analysis of the conserved motifs and superfamily domains of CgCE proteins indicates that proteins within the same group often share similar conserved motifs and superfamily domains. This similarity in motifs and domains implies that these proteins may possess functional similarities or correlations. It is worth noting that Motif 2 is the most identified Motif in CgCEs, and many differentially expressed CgCE genes such as CgCE48 and CgCE60 in pathogen–host interactions are only associated with Motif 2. We speculate that the conserved Motif 2 may be closely related to the pathogenesis of fungi. The presence of multiple superfamily domains may enhance the adaptability of proteins to diverse environments, thus improving the adaptability of both cells and organisms. CgCE103 and CgCE35 proteins possess a rich variety of superfamily domains, suggesting that these two proteins may serve multiple functions in cellular activities and participate in various biological processes.
The functions of genes are usually influenced by CAREs [29]. Several studies underscore the critical role of CAREs [30,31,32,33,34]. A significant number of CAREs identified in this study are related to plant hormones, and the abundant presence of MeJA and ABA response elements suggests that pathogens may impact the plant’s defense mechanisms. Some identified CAREs were also linked to drought tolerance, cold response, defense, and overall stress resilience. Furthermore, light-responsive elements encompass various CARE components. The diversity and abundance of these light-responsive elements highlight the essential role of CgCEs in light regulation. These CAREs likely contribute to growth, facilitate responses to stresses, and aid in adaptation to environmental challenges. The multitude of CAREs identified in this study suggests that pathogens may establish a complex regulatory network for gene expression, thereby enabling effective responses to intricate environments and promoting their invasion and adaptation to the host environment.
The GO enrichment analysis of the CgCE genes suggests that they primarily participate in metabolic processes, particularly in the metabolism of polysaccharides. This implies that CgCE genes may play a crucial role in the degradation of polysaccharides within plant cell walls during pathogen invasion. Additionally, gene functions are typically correlated with their expression characteristics [35,36,37]. For example, researchers have identified genes associated with sexual development and virulence by examining the infection-specific transcription patterns of the corn pathogen Cochliobolus heterotrophus [38]. In this study, many CgCE genes such as CgCE61, have high levels of expression at 24 h, indicating that they may be involved in the early stages of pathogen invasion. On the contrary, some genes such as CgCE32 have higher levels of expression at 60 h, indicating that they may play a more important role in the later stages of the infection process.
In recent years, the interaction between C. graminicola and maize crops has been a hot topic of concern for researchers, and multiple studies have provided conditions for us to understand the pathogenic mechanism of C. graminicola [17,39,40]. Our research provides comprehensive information on CgCEs, which will contribute to the ultimate unraveling of the interaction network between C. graminicola and maize crops. Through a comprehensive whole-genome analysis, we conducted a preliminary characterization of the CgCEs. However, these results are mainly based on bioinformatics analysis. Further research is essential to elucidate the roles of these genes. Especially for the genes that may be associated with pathogenicity, further functional experiments are needed for validation. Specifically, the downstream responses remain poorly understood. The identification of host genes that interact with CgCEs is also crucial.

4. Materials and Methods

4.1. Identification and Analysis of CgCE Genes

To identify the CE family genes of C. graminicola TZ-3, we retrieved genomic data from the public zenodo database (https://doi.org/10.5281/zenodo.7596976, accessed on 30 January 2025), as detailed in previous publications [41]. Excellent N50 and L50 data indicate that the genome assembly quality is good. The CAZy database employs an e-value threshold of less than 1 × 10−5 to identify CE proteins within the genome of C. graminicola. Subsequently, we predicted physicochemical properties of the CgCE proteins using the online ExPASy tool found at https://web.expasy.org/protparam/ (accessed on 30 January 2025) [42]. To ascertain the protein’s subcellular localization, we employed the PSORT tool available at the PSORT website (https://wolfpsort.hgc.jp/, accessed on 30 January 2025).

4.2. Phylogenetic Analysis

Multiple sequence alignment of CgCE protein sequences was performed using Clustal W with default parameters. A phylogenetic tree was subsequently generated via the Neighbor-Joining (NJ) method in MEGA 7.0, with a bootstrap value set at 1000. The 128 CgCE proteins were grouped based on their clustering in the phylogenetic tree. The tree was visually optimized using the Evolview website (http://evolgenius.info/evolview-v2/, accessed on 31 January 2025) [43].

4.3. Gene Structures and Protein Motifs

The gene structures of the CgCE genes were predicted utilizing the Gene Structure Display Server (GSDS) [44]. Furthermore, MEME Suite was used to identify conserved motifs in CgCE protein sequences, with a specified motif count of 10 [45].

4.4. Promoter Region Analysis and GO Analysis

PlantCARE was employed to predict the CAREs in the 2000 bp upstream region of CgCE genes [26]. Visualization was accomplished using TBtools-II v2.142 software [46]. Additionally, GO analysis was performed using the OmicShare bioinformatics platform [47]. GO terms with adjusted p-values < 0.05 were considered significantly enriched.

4.5. Analysis of CgCE Gene Expression Patterns

RNA-seq data (accession number: GSE34632) of maize infected with C. graminicola were obtained from previous studies, and then, we analyzed them to elucidate the expression changes of CE genes [19]. The three time points, respectively, represent the stage of attachment cell infection (24 h), the stage of intracellular biological nutritional hyphae (36 h), and the stage of necrotic nutritional hyphae (60 h) [19]. The R package EdgeR was employed to identify differentially expressed genes between two developmental stages. In each library, the gene read counts were normalized by the total number of mapped reads. Transcripts with significant p-values (p < 0.05) and fold changes exceeding twofold (log2) were classified as differentially expressed genes. The Benjamini--Hochberg method was utilized to adjust for the false discovery rate in multiple hypothesis testing [19]. The OmicShare bioinformatics platform was employed to generate a heatmap based on FPKM values, thereby facilitating the visualization of the CgCE genes’ expression patterns [47]. Z-score normalization was performed on the data, and a hierarchical clustering method was used to generate the heatmap.

4.6. RT-qPCR

Total RNA was extracted from maize infected with C. graminicola using the Tiangen DP441 assay kit (Tiangen, Beijing, China). First-strand complementary DNA was synthesized using HiScript III First Strand cDNA Synthesis Kit (Vazyme, Nanjing, China). Primers were designed with Primer Premier 5.0, setting the PCR product size parameter to 150–250 bp. The primers were checked by BLAST version 2.2.25 and finally listed in Table S4. Quantitative PCR was performed using ChamQ SYBR Color RT-qPCR MasterMix (Vazyme, Nanjing, China). The RT-qPCR program is as follows: 95 °C, 30 s, followed by 40 cycles, each cycle consisting of reactions at 95 °C, 10 s, and 60 °C, 30 s. The UBQ gene was served as the internal reference gene. And 2−ΔΔCT was used to analyze gene expression.

4.7. Statistical Analysis

All analyzed data were initially processed in Microsoft Excel version 2010 and then analyzed using IBM SPSS Statistics version 29.0.2.0 for student t-test. The graphical representation was generated using GraphPad Prism version 9.3 and further refined in Microsoft Office PowerPoint version 2010.

5. Conclusions

This study involved a comprehensive analysis of the physicochemical properties of 128 CgCE genes. Additionally, the expression patterns of these CgCE genes were examined using transcriptomic data and RT-qPCR techniques, thereby improving our understanding of the CgCE gene family. This study has contributed to the CgCE gene resource database and laid the foundation for the functional research of the fungal CE gene family.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/agriculture15070781/s1, Figure S1: Sequence logo conserved motif of CgCE proteins; Figure S2: The numbers of predicted CAREs in the CgCE promoter regions. Table S1: CgCE genomic, CDS, protein and promoter sequences; Table S2: Cis-acting regulatory elements are present in the CgCE gene promoter regions; Table S3: Gene ontology enrichment analysis of CgCEs; Table S4: The primers used in this study.

Author Contributions

Y.W., H.L. and Y.S. designed and directed the research. W.Z., L.W., J.C., S.W., X.L., P.M., J.Z., Y.L. and Y.W. performed the experiments and wrote the original draft. Y.W., H.L., W.Z. and L.W. revised and polished the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the National Natural Science Foundation of China (No. 32102159), the National Key Research and Development Program of China (2023YFD1401502), Key Research and Development Project of Henan Province (231111111100), Henan Province Corn Industry Technology System Plant Protection Post Scientists Research Special Project (HARS-22-02-G3), and Program for Innovative Research Team (in Science and Technology) in University of Henan Province (25IRTSTHN031).

Institutional Review Board Statement

Not applicable.

Data Availability Statement

The contributions presented in the study are included in the article/Supplementary Materials, and further inquiries can be directed to the corresponding author.

Conflicts of Interest

The authors declare no conflicts of interest.

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Agriculture 15 00781 g001
Figure 1. The neighbor-joining phylogenetic tree of CE proteins from Colletotrichum graminicola. Note: “Cg” represents C. graminicola. The bootstrap values below 70% have been cut off. According to the phylogenetic tree, all CgCE proteins can be divided into nine groups, labeled as group I to group IX.
Figure 1. The neighbor-joining phylogenetic tree of CE proteins from Colletotrichum graminicola. Note: “Cg” represents C. graminicola. The bootstrap values below 70% have been cut off. According to the phylogenetic tree, all CgCE proteins can be divided into nine groups, labeled as group I to group IX.
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Figure 2. Gene structure and domain analysis of CgCEs. Note: (A) Exon–intron structures of CgCEs. The blue boxes represent untranslated regions; the yellow boxes represent the exon; the black line represents the intron. (B) Domains of CgCEs. Color rectangles indicate the CgCEs’ superfamilies.
Figure 2. Gene structure and domain analysis of CgCEs. Note: (A) Exon–intron structures of CgCEs. The blue boxes represent untranslated regions; the yellow boxes represent the exon; the black line represents the intron. (B) Domains of CgCEs. Color rectangles indicate the CgCEs’ superfamilies.
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Figure 3. The motifs of CgCEs predicted by MEME. Note: distinct colored boxes denote various conserved motifs with differed sizes and sequences.
Figure 3. The motifs of CgCEs predicted by MEME. Note: distinct colored boxes denote various conserved motifs with differed sizes and sequences.
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Figure 4. Analysis of the 2000 bp promoter regulatory elements of CgCE genes. Note: colored blocks represent diverse cis-acting regulatory elements and their relative positions.
Figure 4. Analysis of the 2000 bp promoter regulatory elements of CgCE genes. Note: colored blocks represent diverse cis-acting regulatory elements and their relative positions.
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Figure 5. Gene ontology enrichment analysis of CgCE genes.
Figure 5. Gene ontology enrichment analysis of CgCE genes.
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Figure 6. The expression level of CgCEs based on RNA-seq data. Note: colors represent different FPKM values. Red and green indicate high and low expression levels of CgCEs, respectively. The genes validated by quantitative PCR are highlighted in red font.
Figure 6. The expression level of CgCEs based on RNA-seq data. Note: colors represent different FPKM values. Red and green indicate high and low expression levels of CgCEs, respectively. The genes validated by quantitative PCR are highlighted in red font.
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Figure 7. RT-qPCR verification of CgCEs. Note: Bars represent the mean values of three technical replicates ± SE, student’s t-test (n = 3, * p < 0.05, ** p < 0.01, *** p < 0.001).
Figure 7. RT-qPCR verification of CgCEs. Note: Bars represent the mean values of three technical replicates ± SE, student’s t-test (n = 3, * p < 0.05, ** p < 0.01, *** p < 0.001).
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Table 1. The characteristics and subcellular localization prediction results of the putative CgCEs in C. graminicola.
Table 1. The characteristics and subcellular localization prediction results of the putative CgCEs in C. graminicola.
Proposed
Gene Name		Gene IDSuperfamilyCDS Length (bp)Protein Length (aa)Mw (KDa)PIGRAVYPredicted Subcellular Localization
CgCE1EVM0000041CE10172857562.25.56−0.163extracellular, including cell wall
CgCE2EVM0000082CE596332033.385.06−0.266extracellular, including cell wall
CgCE3EVM0000127CE4200166671.885.350.046plasma membrane
CgCE4EVM0000327CE1088529432.76.830.858mitochondrion
CgCE5EVM0000354CE1097532435.875.22−0.419cytoskeleton
CgCE6EVM0000406CE565721822.795.670.135extracellular, including cell wall
CgCE7EVM0000448CE380426728.665.06−0.056extracellular, including cell wall
CgCE8EVM0000618CE475325027.214.93−0.274extracellular, including cell wall
CgCE9EVM0000742CE10100833537.075.48−0.187cytosol
CgCE10EVM0000896CE569323024.055.77−0.155extracellular, including cell wall
CgCE11EVM0000955CE1087028930.898.84−0.167extracellular, including cell wall
CgCE12EVM0000976CE1279226328.149.24−0.095extracellular, including cell wall
CgCE13EVM0001025CE1278326027.414.85−0.135extracellular, including cell wall
CgCE14EVM0001088CE10263187695.616.23−0.476mitochondrion
CgCE15EVM0001101CE10202567474.044.79−0.253extracellular, including cell wall
CgCE16EVM0001121CE10195665168.664.81−0.286extracellular, including cell wall
CgCE17EVM0001137CE476525427.157.68−0.113extracellular, including cell wall
CgCE18EVM0001148CE10167155662.035.81−0.329extracellular, including cell wall
CgCE19EVM0001168CE499032937.855.58−0.63cytosol
CgCE20EVM0001222CE4120940242.985.01−0.319extracellular, including cell wall
CgCE21EVM0001274CE584928230.128.550.03extracellular, including cell wall
CgCE22EVM0001394CE10172857561.325.9−0.16mitochondrion
CgCE23EVM0001905CE10165655160.555.31−0.279cytosol
CgCE24EVM0001952CE1125141646.396.28−0.338cytosol
CgCE25EVM0002004CE10154251356.274.72−0.142extracellular, including cell wall
CgCE26EVM0002064CE187028930.957.65−0.209extracellular, including cell wall
CgCE27EVM0002115CE10161753857.254.59−0.087extracellular, including cell wall
CgCE28EVM0002178CE2153651155.65.35−0.122extracellular, including cell wall
CgCE29EVM0002192CE14104734838.27.73−0.307cytosol_mitochondrion
CgCE30EVM0002202CE10187862567.126.46−0.101cytosol
CgCE31EVM0002514CE1108636140.35.86−0.314cytosol
CgCE32EVM0002515CE4228676181.846.17−0.105extracellular, including cell wall
CgCE33EVM0002914CE10156652155.045.150.012extracellular, including cell wall
CgCE34EVM0002966CE4192063966.126.45−0.29extracellular, including cell wall
CgCE35EVM0003070CE1079472648288.116.2−0.122extracellular, including cell wall
CgCE36EVM0003146CE191530432.386.050.03extracellular, including cell wall
CgCE37EVM0003231CE10115838542.248.31−0.286mitochondrion
CgCE38EVM0003289CE1259286394.048.950.098plasma membrane
CgCE39EVM0003589CE4117639141.894.85−0.243extracellular, including cell wall
CgCE40EVM0003593CE1692730833.324.490.044extracellular, including cell wall
CgCE41EVM0003606CE381627129.866.07−0.295cytoskeleton
CgCE42EVM0003618CE4120039943.086.81−0.179extracellular, including cell wall
CgCE43EVM0003652CE4192964270.285.74−0.266mitochondrion
CgCE44EVM0003752CE10104134637.285.480.003cytosol
CgCE45EVM0003815CE10160553459.946.4−0.399peroxisome
CgCE46EVM0003847CE10183361066.425.6−0.188extracellular, including cell wall
CgCE47EVM0004162CE10162354056.787.50.078extracellular, including cell wall
CgCE48EVM0004283CE10233477787.034.9−0.327extracellular, including cell wall
CgCE49EVM0004290CE565421721.986.020.109extracellular, including cell wall
CgCE50EVM0004486CE190630133.858.38−0.337mitochondrion
CgCE51EVM0004596CE10118539444.619.65−0.279mitochondrion
CgCE52EVM0004622CE186728830.58.18−0.103extracellular, including cell wall
CgCE53EVM0004635CE389129631.914.710.001extracellular, including cell wall
CgCE54EVM0004691CE10147649154.826.88−0.24mitochondrion
CgCE55EVM0004748CE1275024926.465.75−0.127extracellular, including cell wall
CgCE56EVM0004803CE3110736840.885.18−0.419cytoskeleton
CgCE57EVM0004811CE575024926.085.33−0.071extracellular, including cell wall
CgCE58EVM0005092CE15822273308.94−0.237extracellular, including cell wall
CgCE59EVM0005152CE493331035.545.44−0.54cytoskeleton
CgCE60EVM0005295CE1102334037.675.23−0.136extracellular, including cell wall
CgCE61EVM0005306CE372624124.954.830.119extracellular, including cell wall
CgCE62EVM0005332CE10171957261.54.580.03extracellular, including cell wall
CgCE63EVM0005686CE4176458759.165.02−0.152extracellular, including cell wall
CgCE64EVM0005870CE10150049955.785.61−0.31nucleus
CgCE65EVM0005918CE10166555460.995.50 −0.264extracellular, including cell wall
CgCE66EVM0006071CE10109236341.096.01−0.493mitochondrion
CgCE67EVM0006162CE592430731.915.80 0.087extracellular, including cell wall
CgCE68EVM0006271CE188229330.835.910.072mitochondrion
CgCE69EVM0006315CE4247882589.216.12−0.262extracellular, including cell wall
CgCE70EVM0006622CE1092130633.255.09−0.202cytosol
CgCE71EVM0006844CE10135345050.815.48−0.159cytosol
CgCE72EVM0007096CE575024925.734.860.184extracellular, including cell wall
CgCE73EVM0007201CE1086728832.145.09−0.281cytosol
CgCE74EVM0007448CE10 189963268.155.05−0.166plasma membrane
CgCE75EVM0007455CE10180360065.594.94−0.156extracellular, including cell wall
CgCE76EVM0007471CE1080126628.304.920.013extracellular, including cell wall
CgCE77EVM0007645CE5102334034.365.16−0.001extracellular, including cell wall
CgCE78EVM0007714CE10159353057.785.93−0.186extracellular, including cell wall
CgCE79EVM0007728CE1171657162.836.11−0.223mitochondrion
CgCE80EVM0007815CE1031471048114.635.70 −0.143cytosol
CgCE81EVM0007953CE1276525427.615.97−0.15cytosol
CgCE82EVM0007971CE10250883595.926.72−0.423cytosol
CgCE83EVM0008001CE16114338040.044.64−0.003extracellular, including cell wall
CgCE84EVM0008060CE10116138643.298.09−0.096mitochondrion
CgCE85EVM0008211CE10101133636.255.66−0.029cytosol
CgCE86EVM0008226CE10113437741.845.83−0.236cytosol
CgCE87EVM0008257CE9132043946.915.59−0.070 mitochondrion
CgCE88EVM0008267CE16103534437.595.32−0.124extracellular, including cell wall
CgCE89EVM0008341CE598732833.595.32−0.185extracellular, including cell wall
CgCE90EVM0008636CE10218472781.429.43−0.411mitochondrion
CgCE91EVM0008653CE1103234338.575.41−0.443cytosol
CgCE92EVM0008781CE1090029932.515.91−0.129extracellular, including cell wall
CgCE93EVM0008811CE495431736.685.33−0.606cytosol
CgCE94EVM0009004CE899333034.928.62−0.149extracellular, including cell wall
CgCE95EVM0009041CE1106535439.136.74−0.225cytosol
CgCE96EVM0009064CE8123641144.485.02−0.151extracellular, including cell wall
CgCE97EVM0009089CE197832533.488.27−0.091extracellular, including cell wall
CgCE98EVM0009119CE10116438742.675.94−0.192cytosol
CgCE99EVM0009168CE1287629130.887.03−0.208extracellular, including cell wall
CgCE100EVM0009371CE1084328031.576.09−0.32cytoskeleton
CgCE101EVM0009479CE102859952104.335.34−0.376mitochondrion
CgCE102EVM0009532CE187929230.8 8.18−0.088extracellular, including cell wall
CgCE103EVM0009598CE1076892562281.55.97−0.149plasma membrane
CgCE104EVM0009626CE479226330.619.69−0.254mitochondrion
CgCE105EVM0009763CE10179759865.314.7−0.159extracellular, including cell wall
CgCE106EVM0009964CE8103534437.629.19−0.177extracellular, including cell wall
CgCE107EVM0010126CE1112837539.816.29−0.048extracellular, including cell wall
CgCE108EVM0010143CE1120340042.955.74−0.233cytosol
CgCE109EVM0010192CE1127842547.635.38−0.173cytoskeleton
CgCE110EVM0010694CE10108936238.465.02−0.076cytosol
CgCE111EVM0010772CE1688529431.775.3−0.018extracellular, including cell wall
CgCE112EVM0010805CE1106535439.675.6−0.309cytosol
CgCE113EVM0010845CE10104734837.635.82−0.051cytosol
CgCE114EVM0010929CE1105935238.234.850.006cytosol
CgCE115EVM0011053CE10168055960.214.76−0.205extracellular, including cell wall
CgCE116EVM0011097CE10170756862.495.16−0.21extracellular, including cell wall
CgCE117EVM0011119CE10210069977.725.75−0.166mitochondrion
CgCE118EVM0011152CE561820520.466.70.272extracellular, including cell wall
CgCE119EVM0011272CE4160553456.85.86−0.364extracellular, including cell wall
CgCE120EVM0011291CE583427728.635.420.034extracellular, including cell wall
CgCE121EVM0011300CE102766921103.285.26−0.486plasma membrane
CgCE122EVM0011392CE1191763871.296.4−0.52cytosol
CgCE123EVM0011443CE389129631.914.710.001extracellular, including cell wall
CgCE124EVM0011496CE1093331033.555.21−0.011cytosol
CgCE125EVM0011686CE101101366405.27−0.242cytosol
CgCE126EVM0011848CE10105635139.137.86−0.179mitochondrion
CgCE127EVM0011904CE10212170675.465.33−0.139extracellular, including cell wall
CgCE128EVM0011910CE374124627.855.54−0.552cytosol_nucleus
ID: identity; bp: base pair; aa: amino acids; PI: isoelectric point; Mw: molecular weight; GRAVY: grand average of hydropathicity; KDa: kilo dalton.
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Zhu, W.; Wang, L.; Li, H.; Shi, Y.; Chang, J.; Wang, S.; Liu, X.; Ma, P.; Zhao, J.; Liu, Y.; et al. Whole-Genome Identification and Analysis of Carbohydrate Esterase Gene Family in Colletotrichum graminicola. Agriculture 2025, 15, 781. https://doi.org/10.3390/agriculture15070781

AMA Style

Zhu W, Wang L, Li H, Shi Y, Chang J, Wang S, Liu X, Ma P, Zhao J, Liu Y, et al. Whole-Genome Identification and Analysis of Carbohydrate Esterase Gene Family in Colletotrichum graminicola. Agriculture. 2025; 15(7):781. https://doi.org/10.3390/agriculture15070781

Chicago/Turabian Style

Zhu, Wenting, Limin Wang, Honglian Li, Yan Shi, Jiaxin Chang, Senbo Wang, Xu Liu, Penghao Ma, Jinzhang Zhao, Yan Liu, and et al. 2025. "Whole-Genome Identification and Analysis of Carbohydrate Esterase Gene Family in Colletotrichum graminicola" Agriculture 15, no. 7: 781. https://doi.org/10.3390/agriculture15070781

APA Style

Zhu, W., Wang, L., Li, H., Shi, Y., Chang, J., Wang, S., Liu, X., Ma, P., Zhao, J., Liu, Y., & Wang, Y. (2025). Whole-Genome Identification and Analysis of Carbohydrate Esterase Gene Family in Colletotrichum graminicola. Agriculture, 15(7), 781. https://doi.org/10.3390/agriculture15070781

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