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13 February 2026

17 Pages

Secretome-Wide Lysine Acetylation Profiling of Fusarium oxysporum Reveals Potential Virulence Factors in Sugarcane Pokkah Boeng Disease

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1
Guangxi Key Laboratory of Sugarcane Biology, Guangxi Sugarcane Bio-Breeding Laboratory, College of Agriculture, Guangxi University, Nanning 530005, China
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National Key Laboratory of Cotton Biobreeding and Integrated Utilization, Institute of Cotton Research, Chinese Academy of Agricultural Sciences (ICR, CAAS), Anyang 455000, China
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Hainan Seed Industry Laboratory, Sanya 572024, China
*
Authors to whom correspondence should be addressed.
Microorganisms2026, 14(2), 462;https://doi.org/10.3390/microorganisms14020462
This article belongs to the Special Issue Advances in Fungal Plant Pathogens: Diagnosis, Resistance and Control
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Abstract

Fusarium oxysporum is the causal agent of Pokkah Boeng disease (PBD) in sugarcane. Lysine acetylation (Kac) is a dynamic and reversible post-translational modification that plays a critical role in regulating diverse cellular processes. Although Kac is known to significantly influence protein function, its specific role within the F. oxysporum secretome during PBD pathogenesis remains poorly understood. In this study, we conducted a comprehensive analysis of the lysine acetylome across the F. oxysporum secretome. Utilizing highly sensitive immunoaffinity purification coupled with high-resolution liquid chromatography-tandem mass spectrometry (LC-MS/MS), we identified 291 acetylation sites within 85 potentially secreted proteins. Bioinformatics analysis revealed that these acetylated proteins are involved in a wide array of biological functions and exhibit diverse subcellular localizations. Notably, these secreted proteins represent a valuable resource for identifying novel effectors; specifically, eight upregulated genes encoding Kac proteins were identified as potential players during the initial asymptomatic stages of infection. Collectively, these findings provide a global overview of the F. oxysporum secretome acetylome and offer a foundational resource for elucidating the functional significance of lysine acetylation in sugarcane PBD pathogenesis.

1. Introduction

Sugarcane (Saccharum spp.) is a vital economic crop cultivated extensively in tropical and subtropical regions [1]. Among the various biotic and abiotic stresses affecting sugarcane production, fungal infections are a major cause of annual yield losses. Fusarium oxysporum is a prominent soil-borne pathogen characterized by a broad host range and diverse infection strategies [2,3]. Due to its significant natural differentiation, polymorphism, and high variability, it is taxonomically classified as the F. oxysporum species complex (FOSC) [2]. This complex comprises over 150 host-specific formae speciales, each typically consisting of specific vegetative compatibility groups (VCGs) and pathogenic races [4]. The pathogen secretes numerous cell wall-degrading enzymes, including cellulases, pectinases, and glucosidases, which disrupt host cellular integrity, obstruct vascular bundles, and impair water and nutrient transport, ultimately leading to systemic wilting [5,6]. Under field conditions, F. oxysporum can enhance its virulence through adaptive evolution by interacting with the host’s genetic background. A well-documented example is the evolution of F. oxysporum f. sp. cubense, which acquired the ability to infect the previously resistant banana cultivar ‘Cavendish’ following its large-scale cultivation [7,8]. As the causal agent of sugarcane Pokkah Boeng Disease (PBD), F. oxysporum poses a severe threat to the global sugarcane industry [9,10].
Plants host a complex microbiome—a diverse community of bacteria, fungi, and viruses that reside both on and within their tissues. Among these, versatile endophytic microorganisms colonize various plant organs without causing apparent harm, forming what is known as the endophytic microbiome or endo-microbiome [11]. These endophytes play a pivotal role in fortifying plant defense systems against pathogen infection, often through direct antagonistic activities [12]. However, environmental perturbations, such as excessive nitrogen fertilization and global warming, can disrupt the homeostasis between endophytes and their host plants. Such imbalances may trigger a transition in F. oxysporum from a commensal or latent state to a pathogenic one, ultimately leading to disease outbreaks. To counter microbial invasion, plants have evolved a sophisticated two-tiered immune system. The first line of defense, PAMP-triggered immunity (PTI), relies on pattern recognition receptors (PRRs) to detect conserved pathogen-associated molecular patterns (PAMPs) [13]. When this basal defense is compromised, plants activate a second layer of immunity known as effector-triggered immunity (ETI). This process involves receptor-like cytoplasmic kinases (RLCKs) that phosphorylate downstream signaling components, triggering rapid calcium influx and reactive oxygen species (ROS) production [14]. Despite these multilayered physical and innate immune barriers [15,16], pathogens can circumvent or suppress host defenses by mutating existing effectors or secreting novel effector proteins [17,18]. These secreted proteins are critical determinants of pathogen virulence, acting to dampen plant immune signaling.
Among various post-translational modifications (PTMs), lysine acetylation (Kac) is a dynamic, reversible, and evolutionarily conserved regulatory mechanism. While its role in histones and transcriptional regulation is well-documented [19,20,21], recent advancements in high-resolution mass spectrometry and immunoaffinity purification have enabled the comprehensive mapping of the lysine acetylome across a wide range of prokaryotic [22,23] and eukaryotic organisms [24,25]. In Arabidopsis, acetylated proteins are distributed across multiple cellular compartments, regulating central metabolism and stress responses [26,27]. Global acetylome analyses further reveal that Kac preferentially targets macromolecular complexes involved in chromatin remodeling, cell cycle regulation, and nuclear transport [28]. However, the acetylome of plant pathogenic fungi, including Fusarium graminearum [29], Phytophthora sojae [30], and Magnaporthe oryzae [31,32], remains relatively understudied. Emerging evidence suggests that Kac plays a pivotal role in regulating fungal pathogenesis, offering new perspectives for disease control.
Previously, we characterized the genome and morphology of F. oxysporum strain BS2-6 and its impact on sugarcane leaf ultrastructure [33]. Nevertheless, the profile and function of lysine acetylation in the context of sugarcane PBD remain largely unexplored. In this study, we performed a secretome-wide analysis of lysine acetylation in F. oxysporum. Using LC-MS/MS, we identified 291 acetylation sites across 85 secreted proteins and characterized conserved acetylation motifs such as K*****Kac and Kac*L. The expression patterns of genes encoding these acetylated proteins were further validated via qRT-PCR. Our findings highlight several acetylated secreted proteins potentially involved in infection, underscoring the significance of Kac in fungal infection and providing novel insights into the molecular mechanisms underlying F. oxysporum infection in sugarcane.

2. Materials and Methods

2.1. Fungal Strain and Culture Conditions

The wild-type strain F. oxysporum BS2-6 was isolated by our laboratory in 2015 from Baise, Guangxi, China (E 106°62′, N 23°90′). The strain was initially cultured in potato dextrose water (PDW) medium (Hopebio, Qingdao, China) at 28 °C with shaking at 200 rpm for 3 days. Subsequently, the harvested mycelia were inoculated into Czapek medium (CM group) (1 g/L K2HPO4, 0.5 g/L MgSO4·7H2O, 0.5 g/L KCl, 0.01 g/L Fe2SO4, 30 g/L sucrose, and 3 g/L NaNO3) and sugarcane juice medium (SM group) (prepared from fresh sugarcane leaves). These cultures were incubated at 28 °C and 200 rpm for 72 h, after which the culture supernatants were collected for subsequent LC-MS/MS analysis. Additionally, agar-solidified CM and SM media were prepared, and strain BS2-6 was inoculated and cultured at 28 °C for 5 days to observe colony morphological characteristics. All treatments were performed in triplicate.

2.2. Protein Extraction

An appropriate volume of lysis buffer (8 M urea, 1% Triton X-100, 65 mM dithiothreitol (DTT), and 0.1% protease inhibitor cocktail) was added to the collected culture supernatants. Cell lysis was enhanced by three rounds of sonication on ice, followed by incubation on ice for 30 min. The samples were then centrifuged at 20,000× g for 10 min at 4 °C, and the supernatant was recovered. Proteins were precipitated by adding 15% cold trichloroacetic acid (TCA) (Solarbio, Beijing, China) and incubated at 4 °C for 2 h. After centrifugation, the supernatant was discarded, and the protein pellet was washed three times with ice-cold 75% (v/v) ethanol (Sinopharm, Beijing, China). The final protein precipitate was re-dissolved in buffer (8 M urea, 100 mM (NH4)2CO3, pH 8.0). Protein concentration was determined using a BCA protein assay kit (Beyotime, Shanghai, China) according to the manufacturer’s instructions, and protein quality was further confirmed by SDS-PAGE and Western blotting. For SDS-PAGE, equal amounts of protein samples were mixed with 5 μL of 4× Laemmli loading buffer, and the total volume was adjusted to 20 μL with deionized water (containing 2% SDS). The mixtures were boiled at 95 °C for 5 min for denaturation. Subsequently, 1 μL of protein ladder and 20 μL of each sample were loaded onto the SDS-PAGE gels. Following electrophoresis, the gels were stained with Coomassie Brilliant Blue R-250 (Sangon Biotech, Shanghai, China) for 2 h and then immersed in a destaining solution until the protein bands became clearly distinct against a clear background. For Western blotting, the resolved proteins were transferred onto PVDF membranes. After blocking with 5% non-fat milk for 1 h at room temperature, the membranes were incubated with Anti-Acetyllysine Rabbit pAb (1:1000 dilution) overnight at 4 °C. After washing, the membranes were incubated with appropriate HRP-conjugated secondary antibodies. The protein bands were visualized using an ECL kit with a 2-s exposure, accurately reflecting the protein expression levels across different samples.

2.3. Trypsin Digestion and Affinity Enrichment of Lysine Acetylated Peptides

To provide a comprehensive qualitative profiling of the F. oxysporum secretome acetylome, protein samples collected from both CM and SM media were pooled in equal amounts to form a single combined sample for subsequent analysis. For disulfide bond reduction, protein samples were incubated with 10 mM DTT at 30 °C for 60 min, followed by alkylation with 20 mM iodoacetamide (IAM) in the dark at room temperature for 45 min. Proteins were then precipitated with cold acetone (Sinopharm, Beijing, China), washed, and resuspended in tetraethylammonium bromide (TEAB) via sonication on ice. Trypsin was then added for overnight digestion at 37 °C. The resulting peptides were desalted using a C18 solid-phase extraction (SPE) column and dried under vacuum. Dried peptides were reconstituted in NETN buffer (100 mM NaCl, 1 mM EDTA, 50 mM Tris-HCl, 0.5% NP-40, pH 8.0). Lysine-acetylated peptides were enriched using an anti-acetyl-lysine antibody-conjugated resin (Ace-K Kit, WM702, Micrometer Biotech, Hangzhou, China). Bound peptides were eluted with 0.1% trifluoroacetic acid (TFA), vacuum-dried, and further purified using C18 ZipTips prior to LC-MS/MS analysis.

2.4. LC-MS/MS Analysis and Database Searching

Peptides, spiked with iRT standard peptides for retention time normalization, were analyzed using a Vanquish Neo ultra-high-performance liquid chromatography (UHPLC) system coupled to an Orbitrap Astral high-resolution mass spectrometer (Thermo Scientific, Waltham, MA, USA). Chromatographic separation was performed at a nanoliter flow rate. Data-independent acquisition (DIA) was conducted in positive ion mode with a precursor scan range of 380–980 m/z. Full MS scans resolution was set to 240,000 at 200 m/z, with a normalized AGC target of 500% and a maximum injection time (IT) of 5 ms. For MS2, 300 DIA windows were used with a 2 m/z isolation window, 25 eV HCD collision energy, 300% AGC target, and 3 ms maximum IT. Raw data were processed using Spectronaut software v19.7. Search parameters included: trypsin digestion with up to two missed cleavages; fixed modification: Carbamidomethyl (C); and dynamic modifications: Oxidation (M), Protein N-terminal Acetylation, and Lysine Acetylation (K). A false discovery rate (FDR) threshold of <1% was applied at the protein level.

2.5. Bioinformatics Analysis

Signal peptides were predicted using SignalP v4.0 [34], and subcellular localization was determined via WoLF PSORT [35]. Motif analysis of the amino acid sequences flanking the acetylation sites (10 amino acids upstream and downstream) was performed using WebLogo [36,37]. Functional annotations were obtained by searching against COG, Swiss-Prot, TrEMBL, and Nr databases. Gene Ontology (GO) and KEGG pathway enrichment analyses were conducted using Blast2GO v5.2.5 and DAVID 6.7 [38,39,40,41,42,43]. Significance was defined as a corrected p-value < 0.05. Genomic synteny analysis between F. oxysporum BS2-6 and the reference strain 4287 was performed using BLAST v2.2.31 and the MCScanX tool in TBtools v2.09 [44,45].

2.6. qRT-PCR Analysis

Total RNA was extracted from mycelia harvested from CM and SM cultures using TRIzol reagent (Invitrogen, Carlsbad, CA, USA). Genomic DNA was removed, and cDNA was synthesized using the PrimeScript™ RT reagent Kit (Takara, Beijing, China). Quantitative PCR was performed with ChamQ Blue Universal SYBR qPCR Master Mix (Vazyme, Nanjing, China) on a LightCycler®96 system (Table S1). Relative gene expression was calculated using the 2−ΔΔCt method, with 18S rRNA as the internal control for normalization. Primer sequences are listed in Table S1. All experiments were conducted in triplicate, and the results are presented as mean ± standard deviation (SD). Statistical significance between the CM and SM groups was determined using Student’s t-test in GraphPad Prism 6.0 (GraphPad Software, San Diego, CA, USA). A p-value < 0.05 was considered statistically significant.

3. Results

3.1. Identification and Analysis of Lysine-Acetylated Proteins

Significant differences in colony morphology and pigmentation of F. oxysporum BS2-6 were observed between the two media, suggesting distinct metabolic profiles under different culture conditions. When grown on Czapek medium (CM, both solid and liquid), the mycelia were relatively sparse and exhibited a pale pinkish-purple hue. In contrast, growth on sugarcane juice medium (SM) resulted in abundant mycelial biomass with a yellowish-white appearance (Figure 1A). The quality and integrity of the BS2-6 proteome was verified by SDS-PAGE and Western blot analysis, confirming successful protein enrichment across all samples (Figure 1B). Subsequently, a combination of immunoaffinity purification and LC-MS/MS was employed to identify lysine-acetylated proteins (Figure 1C). A total of 7270 acetylated peptides corresponding to 6802 acetylation sites were identified, representing 2044 acetylated proteins (Figure 1D).
Figure 1. Identification of lysine acetylation in F. oxysporum BS2-6. (A) Phenotypic and pigmentation characteristics of F. oxysporum BS2-6 on liquid and solid CM and SM; (B) SDS-PAGE and Western blot analysis of acetylated proteins; (C) Schematic overview of the experimental workflow for identifying acetylated proteins using affinity enrichment and LC-MS/MS; (D) Summary of identified acetylated proteins based on LC-MS/MS data. Note: CM, Czapek medium; SM, sugarcane juice medium.

3.2. Identification and Subcellular Localization of Secretome-Wide Lysine Acetylation

By cross-referencing the previously determined secretome of F. oxysporum BS2-6 with the acetylated proteins identified in this study (Tables S2 and S3), we identified 85 acetylated secreted proteins containing 291 unique acetylation sites (Table 1, Figure 2A). These sites corresponded to 455 acetylated peptides with lengths ranging from 8 to 34 amino acids, which is consistent with the expected size of tryptic peptides (Figure 2B, Table S4). Analysis of the number of acetylation sites per protein revealed substantial variability, ranging from 1 to 25 sites. Specifically, the majority of the proteins (34%, 29 proteins) contained a single acetylation site, while 22% (19 proteins) had two sites, and 11% (9 proteins each) contained three or four sites (Figure 2C). To explore the functions of these lysine-acetylated proteins, their subcellular localization was annotated using WoLF PSORT. As shown in the figure, most acetylated proteins were localized in the extracellular space (21.6%), mitochondria (16.4%), and cytoplasm (15.1%). Additionally, 10.7% (41 proteins) were primarily localized in vacuoles and 8.9% (34 proteins) in the endoplasmic reticulum. These results indicate that lysine-acetylated proteins possess diverse subcellular localizations and are widely distributed within F. oxysporum cells (Figure 2D).
Table 1. Lysine-acetylated secreted proteins identified in F. oxysporum BS2-6.
Figure 2. Identification and subcellular localization of the identified acetylated proteins. (A) Venn diagram showing the overlap between acetylated proteins identified by LC-MS/MS and the secretome of F. oxysporum BS2-6; (B) Length distribution of the identified peptides; (C) Distribution of acetylated proteins based on the number of acetylation sites per protein; (D) Pie chart representing the predicted subcellular localization of the acetylated proteins.

3.3. Characterization of Lysine Acetylation Motifs in F. oxysporum

To characterize the sequence preferences around lysine acetylation sites, we analyzed the amino acid sequences from position -10 to +10 of the 291 identified sites using the WebLogo program (Table S5). Four significantly enriched motifs were identified: K*******Kac, K*****Kac, K***Kac, and Kac*L (where Kac represents the acetylated lysine and * represents any amino acid residue) (Figure 3A). Among these motifs, the Kac*L motif was the most conserved, with peptides containing this motif accounting for approximately 14% of all identified acetylated peptides. Furthermore, a heatmap of the flanking residues revealed a high frequency of Alanine (A), Glycine (G), Lysine (K), Leucine (L), Threonine (T), and Valine (V) around the acetylation sites. Conversely, Cysteine (C), Histidine (H), Isoleucine (I), Methionine (M), Glutamine (Q), Arginine (R), and Tryptophan (W) occurred at the lowest frequencies (Figure 3B,C). These findings suggest that proteins harboring these specific motifs may serve as preferred substrates for lysine acetyltransferases in F. oxysporum BS2-6.
Figure 3. Characteristics of acetylated peptides. (A) Conservation of acetylation motifs within ±10 amino acids of the acetylation sites; the size of each letter represents the frequency of that residue at a specific position. (B) Heatmap showing the amino acid composition around the modified lysine; red indicates enrichment and green indicates depletion. (C) Amino acid preferences showing high- and low-frequency residues surrounding the acetylated lysine (±10).

3.4. Functional Enrichment and Synteny Analysis

To elucidate the biological functions of the acetylated proteins, we performed Gene Ontology (GO) and KEGG pathway enrichment analyses. GO classification revealed that these proteins are primarily associated with enzymatic activity and binding functions. In the Biological Process (BP) category, acetylated proteins were predominantly involved in proteolysis, glycerol ether metabolism, and cellular redox homeostasis. In the Molecular Function (MF) category, most proteins were linked to binding and catalytic activities, while in the Cellular Component (CC) category, only three proteins were enriched in the endoplasmic reticulum (Figure 4A). KEGG analysis identified 14 secreted proteins involved in 9 pathways, and 67% of these pathways were related to metabolic processes (Figure 4B). Specifically, two proteins each were assigned to starch and sucrose metabolism, glycerophospholipid metabolism, and inositol phosphate metabolism. Notably, phospholipase C (PLC) was involved in both glycerophospholipid and inositol phosphate metabolism. Other proteins were associated with galactose, phenylalanine, and arginine/proline metabolism. Beyond metabolic pathways, individual proteins were implicated in the peroxisome and MAPK signaling pathways, while four proteins were involved in protein processing in the endoplasmic reticulum. Furthermore, we conducted a comparative genomic analysis between F. oxysporum BS2-6 and the reference strain F. oxysporum 4287, the first sequenced and characterized genome of this species. Synteny analysis revealed that all 85 identified acetylated secreted proteins in BS2-6 are located on core chromosomes rather than lineage-specific (LS) chromosomes (Figure 4C).
Figure 4. Functional enrichment and synteny analysis of 85 acetylated secreted proteins. (A) GO enrichment analysis (BP, MF, and CC); (B) KEGG pathway enrichment analysis; (C) Genomic synteny between F. oxysporum BS2-6 and F. oxysporum 4287. Gray areas indicate syntenic blocks between chromosomes, and red lines connect homologous genes.

3.5. qRT-PCR Analysis of Expression of the Lysine Acetylation Proteins

Quantitative expression analysis revealed that 60 out of the 85 proteins exhibited statistically significant differential expression. To further verify whether these proteins are induced during growth in sugarcane leaf-derived SM, the expression patterns of these 60 genes were investigated in F. oxysporum BS2-6. Compared to CM, 8 genes were significantly up-regulated in SM, while 52 were down-regulated (Figure 5A,B). The up-regulated subset included FOXY_01438 (SCD), FOXY_01742 (signal transduction gene), FOXY_02794 (GST), FOXY_06926 (EEP family), FOXY_07862 (FAS1 domain-containing protein), FOXY_08524 (AP), FOXY_09884 (SAP), and FOXY_14387 (TRX1). Consistent with the transcriptome data, qRT-PCR validation confirmed that the expression levels of FOXY_01742, FOXY_07862, FOXY_14387, and FOXY_09884 increased by more than five-fold in SM. Statistical analysis indicated that the expression of all tested genes was significantly higher in SM than in CM (p < 0.01, Student’s t-test; Figure 5C).
Figure 5. Transcriptional expression of acetylated proteins. (A) Hierarchical clustering of transcript abundance in CM and SM; (B) Volcano plot showing differentially expressed genes; (C) qRT-PCR validation of 8 up-regulated genes. 18S rRNA was used as the internal control. Data are presented as mean ± SD (n = 3). Asterisks indicate significant differences between CM and SM groups. ** indicates p < 0.01, and *** indicates p < 0.001.

4. Discussion

Sugarcane Pokkah Boeng Disease (PBD) is a devastating foliar disease caused by a complex of Fusarium species. In recent years, its incidence has intensified significantly in China, a trend largely attributed to excessive nitrogen fertilization and global warming [46]. These environmental perturbations can induce physiological distress within the host, thereby disrupting the delicate homeostasis between endophytic microorganisms and the sugarcane plant. The equilibrium within this endo-microbiome is a critical determinant of sugarcane’s physiological state and its defense response to F. oxysporum, a primary pathogen of PBD that severely undermines sugarcane yield. Under stable conditions, beneficial endophytes bolster host fitness by modulating hormonal signaling and secondary metabolism, maintaining the plant in a state of “eustress” or heightened readiness. However, microbial dysbiosis can impair the host’s systemic acquired resistance (SAR) and facilitate the transition of F. oxysporum from a latent or commensal state to a highly aggressive pathogenic state. Deciphering the molecular mechanisms governing this pathogenic transition and host–pathogen interactions is essential for disease management. Lysine acetylation (Kac) has emerged as a key dynamic post-translational modification (PTM) that regulates protein structural integrity and diverse biological functions in both prokaryotes and eukaryotes [47,48]. While extensive research has characterized the acetylome in various organelles and its role in metabolic diseases [49,50], the functional significance of Kac in modulating the virulence and metabolic adaptation of plant pathogenic fungi like F. oxysporum remains largely unexplored. Understanding these regulatory PTMs may provide critical insights into how environmental cues are translated into pathogenic signals during PBD outbreaks.
In this study, using affinity enrichment coupled with LC-MS/MS, we characterized the secretome acetylome of F. oxysporum BS2-6 induced by sugarcane leaves. We identified 291 lysine acetylation sites across 85 proteins, significantly expanding the known acetylated protein catalog for filamentous fungi. Most of these proteins (34%) harbor a single acetylation site, a distribution pattern consistent with reports in Fusarium graminearum (70.1%) [29], Phytophthora sojae (60%) [30], Magnaporthe oryzae (53.4%) [32], and Botrytis cinerea (63.5%) [51]. Furthermore, we identified four highly conserved Kac motifs in the secretome. The preference for specific amino acids flanking the acetylation sites suggests a distinct substrate specificity for lysine acetyltransferases in F. oxysporum BS2-6. Notably, the Kac*L motif is also conserved in P. sojae [30], while the K***Kac motif is shared with F. graminearum [29] and B. cinerea [51], underscoring the evolutionary conservation of Kac across fungal species.
Fungal pathogens are among the most destructive threats to food crops, utilizing secreted effector proteins to manipulate host cellular processes and facilitate colonization [52]. Many of these effectors are low-molecular-weight proteins encoded by avirulence (Avr) genes that suppress plant innate immunity [17,53]. The 85 acetylated secreted proteins identified here exhibit high synteny and sequence homology with F. oxysporum 4287, suggesting conserved functional roles across lineages. Notably, the observation that these genes are predominantly located on the “core” chromosomes, rather than on pathogenicity-specific ones, provides a profound insight into their evolutionary and functional significance. This genomic localization, coupled with the universal nature of acetylation as a regulatory mechanism, underscores that these proteins likely govern fundamental biological processes. Such proteins may contribute to both basic fitness and virulence, reflecting a dual role in maintaining cellular homeostasis and facilitating host infection. Most of these proteins contain signal peptides and are predicted to function as proteases or hydrolases, localizing to various cellular compartments and participating in diverse biological processes. However, 19 proteins remain annotated as “hypothetical” or “function unknown.” Functional characterization of these candidates, particularly through site-directed mutagenesis and in planta assays, will further enrich our understanding of how the F. oxysporum acetylome coordinates basic survival with pathogenic success.
To verify the induction of these proteins by host-derived signals, qRT-PCR analysis was performed, confirming that eight acetylated proteins were significantly upregulated in sugarcane juice medium (SM). Notably, three of these proteins possess highly conserved homologs in other Fusarium species with established roles in stress adaptation or virulence. For instance, FOXG_08382 (a homolog of the glutathione S-transferase FOXY_02794) is known to be upregulated during biotic stress, likely reflecting the fungal defense response [54,55,56]. FOXG_07382 (homologous to the acid phosphatase FOXY_08524) has been identified as a target of the antifungal lipopeptide iturin A, which suppresses fungal growth and mycotoxin synthesis [57]. Furthermore, FOXG_01527 (homologous to the soluble alkaline phosphatase FOXY_09884) is strongly induced during host–root interactions, suggesting a potential role in early-stage infection [58]. Collectively, these comparative genomic insights, combined with our expression data, suggest that these eight upregulated acetylated proteins may play pivotal roles in the pathogenesis of F. oxysporum BS2-6.
Based on the functional characterization of these eight key genes, we propose a comprehensive pathogenic model for F. oxysporum BS2-6 (Figure 6), consisting of four interconnected stages. (a) Breakthrough Stage: The fungus initially perceives environmental cues (temperature, light, moisture, and host exudates), which activate signal transduction pathways (STG) that coordinate the expression of infection-related genes. During this stage, short-chain dehydrogenase SCD facilitates energy metabolism by providing the ATP and reducing power necessary for fungal growth and invasion. (b) Defense Stage: The fungus secretes enzymes such as EEP to degrade cell wall components (cellulose and pectin), breaching physical barriers. Simultaneously, GST and TRX1 act synergistically to neutralize host-derived reactive oxygen species (ROS), stabilizing the fungal membrane against the plant immune system. This mechanism parallels the role of the FRP1 gene in F. oxysporum f. sp. lycopersici, where its loss leads to reduced expression of cell wall-degrading enzyme and loss of infectivity [59,60]. (c) Colonization Stage: Expression of FAS1P contributes to the maintenance of fungal cell wall integrity during tissue colonization. At the same time, SAP and AP modulate host phosphate metabolism to suppress PTI and ETI. (d) Adaptation Stage: Throughout infection, STG-mediated signaling continuously adjusts the expression of these genes, allowing the fungus to adapt to the fluctuating internal environment of the host. This dynamic regulation is reminiscent of the fmk1 MAPK gene in F. oxysporum f. sp. lycopersici, which is essential for pathogenicity but dispensable for vegetative growth [61]. Overall, this ‘Breakthrough–Defense–Colonization’ model represents a sophisticated evolutionary strategy employed by F. oxysporum BS2-6 to ensure successful infection.
Figure 6. Schematic model of the pathogenic mechanism of F. oxysporum BS2-6 infecting sugarcane leaves. The diagram illustrates the infection cycle through four integrated stages: Breakthrough, Defense, Colonization, and Adaptation.
Despite providing the first comprehensive map of the F. oxysporum secretome acetylome, we acknowledge that this study is based on a qualitative analysis of pooled samples from different cultivation conditions. This approach allowed for a broad identification of acetylated proteins but did not permit a direct comparison of acetylation dynamics between synthetic and inductive environments. Given that the acetylation of secreted proteins is a critical regulatory process in fungal pathogenesis, future research should employ comparative quantitative proteomic strategies, such as Tandem Mass Tag (TMT) labeling or Data-Independent Acquisition (DIA) with biological replicates. Such studies will be essential to precisely quantify changes in acetylation levels at individual sites under different conditions, thereby fully elucidating the regulatory mechanisms by which lysine acetylation modulates fungal virulence during infection development.

5. Conclusions

In this study, we characterized the secretome acetylome of F. oxysporum BS2-6, a primary pathogen responsible for sugarcane PBD. Through a combination of affinity enrichment with high-resolution mass spectrometry-based proteomics, we successfully identified a diverse array of novel secreted proteins undergoing lysine acetylation. Our findings demonstrate that these acetylated proteins are involved in a wide range of biological functions and are distributed across various cellular compartments. Notably, we identified eight candidate effector proteins that are significantly induced by host signals. Based on these data, we proposed a comprehensive pathogenic model illustrating the infection strategy of F. oxysporum BS2-6 on sugarcane leaves through four integrated stages: breakthrough, defense, colonization, and adaptation. In this study, the 8 identified proteins are proposed as potential virulence factors, supported by their inducible expression in response to host signals and their homology to established pathogenicity-related proteins. We acknowledge that their precise biological roles require further confirmation through rigorous functional validation. Consequently, our future research will involve the construction of site-specific mutants to elucidate the regulatory impact of acetylation on these proteins. Furthermore, in planta assays on sugarcane will be conducted to validate these findings in a biological context, thereby addressing the limitations of the current in vitro approach that relies on culture media to simulate the host environment. This study provides the first extensive dataset of the lysine acetylome in the sugarcane PBD pathogen, offering valuable insights into the regulatory mechanisms of fungal pathogenesis and providing potential molecular targets for the development of disease-resistant sugarcane varieties.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/microorganisms14020462/s1, Table S1: The primer pairs used for qRT-PCR; Table S2: The identified 2044 acetylated proteins by LC-MS/MS; Table S3: The 1243 secreted proteins in F. oxysporum BS2-6; Table S4: 455 acetylated peptides in 85 secreted acetylated proteins in F. oxysporum BS2-6; Table S5: 291 acetylated sites in 85 secreted acetylated proteins in F. oxysporum BS2-6.

Author Contributions

Conceptualization, Y.B. and M.Z.; methodology, G.W. and C.Z.; software, J.Z., Y.W. and Y.B.; validation, G.W. and J.Z.; investigation, C.Z. and Y.Z.; writing—original draft preparation, G.W.; writing—review and editing, S.A., J.Z., Y.B. and M.Z.; funding acquisition, Y.B. All authors have read and agreed to the published version of the manuscript.

Funding

This research was financially supported by the Guangxi Natural Science Foundation (2024GXNSFAA010441), the Guangxi Science and Technology Base and Talent Special Project (Guike AD25069107), the Innovational Fund for Scientific and Technological Personnel of Hainan Province (KJRC2023D06), the Guangxi Young Elite Scientist Sponsorship Program (GXYESS2025050), the China Agricultural Research System (CARS-17) and 2026 Sugarcane Industry Technology Pioneer Team (Guike Alliance 202603-2).

Institutional Review Board Statement

Not applicable.

Data Availability Statement

All data generated or analyzed during this study were included in this published article and its Supplementary Information files. Further inquiries can be directed to the corresponding authors.

Acknowledgments

The authors thank all members of the team for their valuable discussion.

Conflicts of Interest

The authors declare no conflicts of interest.

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