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Article

Transcriptome Analysis Elucidates the Mechanism of an Endophytic Fungus Cladosporium sp. ‘BF-F’ in Enhancing the Growth of Sesuvium portulacastrum

by
Dan Wang
,
Wenbin Zhang
,
Dinging Cao
and
Xiangying Wei
*
Fuzhou Institute of Oceanography, College of Geography and Oceanography, Minjiang University, Fuzhou 350108, China
*
Author to whom correspondence should be addressed.
Agriculture 2025, 15(14), 1522; https://doi.org/10.3390/agriculture15141522
Submission received: 3 June 2025 / Revised: 9 July 2025 / Accepted: 9 July 2025 / Published: 15 July 2025
(This article belongs to the Section Crop Genetics, Genomics and Breeding)
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Abstract

Plant growth-promoting rhizobacteria (PGPR) are beneficial rhizosphere microorganisms for plants. They can promote plant absorption of nutrients, inhibit pathogenic microorganisms, enhance plant tolerance to abiotic and biotic stresses, and improve plant growth. Isolating new beneficial microbes and elucidating their promoting mechanisms can facilitate the development of microbial fertilizers. This study combined transcriptome sequencing and related experiments to analyze the mechanism by which the endophytic fungus ‘BF-F’ promotes the growth of Sesuvium portulacastrum. We inoculated the ‘BF-F’ fungus beside S. portulacastrum seedlings as the experimental group. Meanwhile, S. portulacastrum seedlings not inoculated with ‘BF-F’ were set as the control group. After inoculation for 0 d, 7 d, 14 d, 21 d, and 28 d, the plant height and the number of roots were measured. Furthermore, transcriptome sequencing on the roots and leaves of the S. portulacastrum was conducted. Differentially expressed genes were screened, and KEGG enrichment analysis was performed. Nitrogen metabolism-related genes were selected, and qRT-PCR was conducted on these genes. Furthermore, we analyzed the metabolomics of ‘BF-F’ and its hormone products. The results showed that inoculation of ‘BF-F’ significantly promoted the growth of S. portulacastrum. After ‘BF-F’ inoculation, a large number of genes in S. portulacastrum were differentially expressed. The KEGG pathway enrichment results indicated that the ‘BF-F’ treatment affected multiple metabolic pathways in S. portulacastrum, including hormone signal transduction and nitrogen metabolism. The auxin signaling pathway was enhanced because of a decrease in AUX expression and an increase in ARF expression. Contrary to the auxin signal transduction pathway, the zeatin (ZT) signaling pathway was suppressed after the ‘BF-F’ treatment. ‘BF-F’ increased the expression of genes related to nitrogen metabolism (NRT, AMT, NR, and GAGOT), thereby promoting the nitrogen content in S. portulacastrum. The metabolites of ‘BF-F’ were analyzed, and we found that ‘BF-F’ can synthesize IAA and ZT, which are important for plant growth. Overall, ‘BF-F’ can produce IAA and enhance the nitrogen use efficiency of plants, which could have the potential to be used for developing a microbial fertilizer.

1. Introduction

During the growth process of plants, they often encounter some uncertain environmental factors, such as drought, salinity, and high temperature, which greatly restrict plant growth [1,2]. The rhizosphere and roots of plants host many beneficial microorganisms, including fungi and bacteria, which can promote plant growth and improve plant tolerance to biotic and abiotic stresses. Especially, soil fungi play an important role in soil nutrient cycling and promoting plant growth [3]. Many studies have proved that plant growth-promoting fungi (PGPFs) can enhance plant growth, endurance to water deficit and salinity stresses, and plant resistance to diseases [4,5,6,7]. PGPFs promote plant growth in a variety of ways, including the enhancement of roots, solubilizing phosphate, producing IAA, siderophore, HCN, and ammonia [8,9,10,11,12]. Some PGPFs can synthesize plant hormones, including indole-3-acetic acid (IAA), cytokinin (CTK), and gibberellin (GA) [13]. These hormones can affect cell division and elongation, as well as physiological processes such as plant rooting and germination, thereby promoting plant growth. For example, the PGPF Penicillium olsonii isolated from the rhizosphere of Aeluropus littoralis was demonstrated to synthesize IAA and promote plant growth [14]. A survey of 46 PGPB Methylobacterium species and strains revealed that these species can produce 16 CK forms, abscisic acid (ABA), and IAA [15]. Genes related to plant growth promotion, such as IAA production, auxin biosynthesis, and nitrogen fixation, were detected in the genome of the PGPB strain DJ06, which was isolated from the roots of sugarcane [16]. In addition, growth-promoting bacteria can also improve plant resistance to salt stress and drought stress by synthesizing ABA and other substances [17].
Another main mechanism by which PGPFs promote plant growth is to promote the absorption of nutrients and minerals (N, P, K, and Fe) by plants [18,19,20]. Nitrogen (N) is a vital nutrient that is well known to enhance plant growth. N participates in various physiological and biochemical processes of plant growth. The deficiency of nitrogen in soil is one of the important global environmental problems, which seriously restricts the development of the agricultural and forestry economies. Various studies have shown that PGPFs can promote plant N absorption. For example, Trichoderma viride inoculation with trash mulch increased N, P, and K uptake and cane yield compared with uninoculated specimens [21]. Inoculation with the Trichoderma strain T. virens (GV41) increased the N use efficiency of lettuce and promoted the uptake of native N present in the soil of both lettuce and rocket [22].
Environmental problems, including heavy metal pollution and salinization of soils, seriously restrict agricultural development. In recent years, based on the advantages of low cost and green environmental protection, phytoremediation has been widely used in the remediation of heavy metals and salinization from soils. Sesuvium portulacastrum L. is a mangrove-associated plant belonging to Aizoaceae, which is resistant to salt and alkaline conditions, high temperatures, and heavy metals [23]. Recent studies have reported that S. portulacastrum can be used for heavy metal soil remediation [24,25,26], nitrogen and phosphorus removal from eutrophic water [27,28], etc., which is a potential remediation pioneer in coastal areas. Nowadays, to improve the efficiency of phytoremediation, more and more attention has been paid to plant–microorganism combined bioremediation. Many PRPBs play an important role in environmental remediation. For example, the growth-promoting rhizobacteria (PGPR) Enterobacter ludwigii can reduce cadmium pollution in sediments by interacting with submerged plants [27]. Our research group isolated an endophytic fungus strain of Cladosporium from the root of the S. portulacastrum, which can promote plant growth, including S. portulacastrum, Arabidopsis, and rice [29]. However, the growth-promoting mechanism of ‘BF-F’ fungi remains unclear.
In this study, we combined transcriptome sequencing to analyze the expression changes in genes in S. portulacastrum after a ‘BF-F’ treatment. The results demonstrated that ‘BF-F’ could synthesize IAA and up-regulate the auxin signal transduction pathway. The nitrogen content of S. portulacastrum treated with ‘BF-F’ increased, and the expression levels of nitrogen metabolism-related genes were up-regulated. This study initially clarified the mechanism by which ‘BF-F’ promotes plant growth. This will lay a theoretical foundation for the future application of ‘BF-F’ and S. portulacastrum in environmental remediation.

2. Materials and Methods

2.1. Plant and Fungal Material

The seeds of the S. portulacastrum used in this study were collected in Houhai, Putian, Fujian (N: 119°13′50.074″, E: 25°16′25.954″). Seedlings of S. portulacastrum were grown in a growth chamber under a 16 h light photoperiod at 25 °C. The plant growth-promoting fungus Cladosporium sp. ‘BF-F’ was isolated from the roots of S. portulacastrum in our previous studies [29]. The fungi Cladosporium sp. ‘BF-F’ was inoculated in a PDA medium and cultured at 28 °C for 7 d for subsequent use.

2.2. Fungal Inoculation and Plant Growth Analysis

The seeds of S. portulacastrum were sterilized on the surface and then sown on the MS solid medium. After being cultivated in a constant temperature and light incubator for 2 weeks, the seedlings with consistent growth were selected for the inoculation experiment. ‘BF-F’ was cut from the outer edge of the pre-cultured fungal colony using a 5 mm puncher and inoculated on the surface of the culture medium 3 cm away from the plant. At the same time, the plants that were not inoculated with ‘BF-F’ were used as controls. A total of 6 S. portulacastrum seedlings with the same growth condition were selected and used for inoculation, and the control group, respectively. The plant height and root number were counted every week.

2.3. RNA Extraction and Sequencing

The leaves and roots of S. portulacastrum after fungal ‘BF-F’ inoculation for two weeks were collected and frozen immediately in liquid nitrogen for RNA-seq. At the same time, the roots and leaves of S. portulacastrum without inoculation with fungus were selected as controls. Three biological replicates were set up for each sample. The experimental samples were sent to the biological company Novogene Co. (Beijing, China) for RNA extraction and transcriptome sequencing. The extraction of plant RNA is carried out using the RNAprep Pure Plant Plus Kit (TIANGEN, Beijing, China). RNA integrity and total concentrations were analyzed using an Agilent 2100 bioanalyzer. A mass of 1 g of RNA from each sample was taken for library construction. The prepared libraries were sequenced by an Illumina platform (HiSeq2000) to generate 150 bp paired-end reads. The reads with adapters, reads containing N, and low-quality reads (reads with a qphred ≤ 20 base number) were removed from the raw data to obtain clean data. Raw data obtained by RNA-seq were submitted to NCBI (PRJNA1262651).

2.4. Differential Expression Analysis

Trinity (v2.5.1) [30] and RSEM (v1.2.15) software were used for transcriptome assembly and the statistics of gene read count, respectively [31]. Subsequently, the read count of genes was converted to FPKM (fragments per kilobase of transcript per million fragments mapped). Differential expression genes were selected using the R package of DESeq2 (v1.20.0) based on padj < 0.05 and |log2FoldChange| > 1 [32]. The KEGG pathway enrichment analysis of the differential expression genes was conducted using KOBAS (v2.0.12) software. Gene functional annotation was performed using the following six databases: the Non-Redundant Protein Sequence Database (Nr), the Nucleotide Sequence Database (Nt), the Protein family (Pfam), Clusters of Orthologous Groups of proteins (KOG/COG), Swiss-Prot, the Kyoto Encyclopedia of Genes and Genomes (KEGG), and the Gene Ontology (GO).

2.5. Quantitative Real-Time PCR (qRT-PCR)

RNA extraction of samples from S. portulacastrum was carried out using an Omega Plant RNA Kit (Omega, Norcross, GA, USA). The RNA extraction method was based on the manual of the kit. Then, 1 μg RNA was used to synthesize the first strand of cDNA with the FastKing RT Kit (TIANGEN, Beijing, China). The qRT-PCR analysis was carried out using the method in our previous study [33]. The qRT-PCR analysis was carried out in a 20 μL volume of reaction buffer, containing 0.8 μL of each primer, 1 μL of cDNA previously synthesized, 10 μL of 2×SYBR Premix Ex Taq (Takara, Kyoto, Japan), and 7.4 μL deionized water. Reactions were run under the amplification program of 95 °C for 3 min, then 95 °C for 10 s, 60 °C for 15 s, 72 °C for 20 s, for 45 cycles. qRT-PCR was performed on an iCycler iQ5 thermal cycler (Bio-Rad, Hercules, CA, USA). The 2−ΔΔc(t) method was used to calculate gene relative expression levels [34]. The primers used in this study are listed in Supplementary Table S1.

2.6. Statistical Analysis

Experimental data in this study were derived from three biological replicates. Data sorting and calculation are carried out in Excel 2019 software. Data plotting was carried out using OriginPro 9.1 and Adobe Illustrator CC 2018. The significance of difference analysis on data was performed using IBM SPSS Statistics 21.0 based on a one-factor ANOVA test (Tukey’s HSD test) at the p < 0.05 (*) and p < 0.01 (**) levels.

3. Results

3.1. Cladosporium sp. ‘BF-F’ Promotes the Growth of S. portulacastrum

In a previous study, our research group isolated an endophytic fungus ‘BF-F’ from the roots of the S. portulacastrum [29]. To demonstrate the effect of ‘BF-F’ on plants, ‘BF-F’ was inoculated near the S. portulacastrum seedlings that had been grown for two weeks, while uninoculated seedlings were used as controls. Compared with control plants, inoculation with ‘BF-F’ significantly promoted the growth of S. portulacastrum (Figure 1A). After 28 d of fungal inoculation, the plant height of the S. portulacastrum reached 5.40 cm, while the plant height of the control plant was 2.28 cm. Meanwhile, ‘BF-F’ inoculation significantly increased the number of S. portulacastrum roots compared with the control (Figure 1B).

3.2. Inoculation of ‘BF-F’ Affected the Expression of Genes in S. portulacastrum

To reveal the molecular mechanism by which ‘BF-F’ promotes plant growth, the root and aboveground part samples of S. portulacastrum were collected for transcriptome sequencing after 14 d of ‘BF-F’ inoculation. Uninoculated plants in the same growth period were used as controls. A total of 75.6 G of screening data were obtained, of which at least 91.35% had a data quality of Q30 or higher (Supplementary Table S2). Since the genome of the S. portulacastrum has not yet been published, the reads were mapped to the transcriptome assembled with Trinity (v2.5.1). BUSCO assessment showed that the comparison rate of complete transcripts (single copy and duplicated copies) reached 60.7% (Supplementary Table S3). The correlation coefficient (r2) was calculated using all the genes to evaluate the correlation between different samples. The results showed that the root and aboveground part samples were clustered separately, and three biological replicates within each group of samples were clustered together (Figure 1C). To analyze the effect of ‘BF-F’ inoculation on gene expression in S. portulacastrum, differentially expressed genes (DEGs) were screened. A total of 9584 DEGs were identified in the root, including 3743 down-regulated genes and 5841 up-regulated genes. Compared with the root, the number of DEGs in the aboveground part of S. portulacastrum was significantly reduced. A total of 2704 DEGs were identified in the aboveground part samples, including 1404 down-regulated genes and 1300 up-regulated genes (Figure 1D). These results indicated that inoculation of ‘BF-F’ significantly affected the expression of genes in S. portulacastrum.

3.3. Inoculation of “BF-F” Affected Hormone Signaling Transduction in S. portulacastrum

An enrichment analysis of metabolic pathways was performed with the KEGG to analyze the effect of ‘BF-F’ inoculation on metabolic pathways in S. portulacastrum. By analyzing the DEGs in the root of S. portulacastrum after “BF-F” inoculation, 30 metabolic pathways were enriched, including zeatin biosynthesis, plant hormone and signal transduction, nitrogen metabolism, indole alkaloid biosynthesis, fatty acid degradation, alpha-linolenic acid metabolism, etc. (Figure 2A). The DEGs in the aboveground part of the S. portulacastrum after ‘BF-F’ inoculation were mainly enriched in pathways including zeatin biosynthesis, plant hormone and signal transduction, plant–pathogen interaction, nitrogen metabolism, alpha-linolenic acid metabolism, etc. (Figure 2B).
Considering the importance of auxin and cytokinin in plant growth, the changes in DEG expression levels were analyzed. After ‘BF-F’ inoculation for 14 d, DEGs related to auxin signal transport inhibitor response 1 (TIR1), auxin response factor (ARF), and SAUR family protein (SAUR) were significantly up-regulated in the root of S. portulacastrum. While the auxin influx carrier (AUX1) and auxin-responsive protein IAA (IAA) were down-regulated in the root (Figure 2C). ‘BF-F’ inoculation can up-regulate the auxin signal transduction pathway in the roots of S. portulacastrum. However, in the leaves of S. portulacastrum, the auxin signaling pathway was significantly inhibited after ‘BF-F’ inoculation. Cytokinin plays an important role in cell division and shoot initiation. DEGs related to cytokinin signal transduction, including Arabidopsis histidine kinase 2/3/4 (AHK2_3_4), histidine-containing phosphotransfer protein (AHP), and two-component response regulator ARR-A family (ARR-A), were up-regulated in the roots of S. portulacastrum after ‘BF-F’ inoculation. Among them, type A ARRs act as negative regulators of cytokinin signaling. Type A ARRs can inhibit the activity of type B ARRs. While the positive regulator ARR-B family gene (ARR-B) was down-regulated. In the leaves of S. portulacastrum, ARR-A genes were significantly up-regulated after ‘BF-F’ inoculation (Figure 2D). Overall, Cladosporium sp. ‘BF-F’ inoculation suppressed cytokinin signaling in S. portulacastrum.

3.4. Cladosporium sp. ‘BF-F’ Inoculation Promotes Nitrogen Uptake in S. portulacastrum

Nitrogen is the fundamental constituent element of plant chlorophyll, genetic material, protein, and other major organic molecules. Nitrogen plays an important role in plant growth. KEGG enrichment analysis showed that ‘BF-F’ inoculation had an effect on the nitrogen metabolism pathway of S. portulacastrum (Figure 2A,B). Therefore, the expression changes in genes involved in nitrogen metabolism were analyzed. A total of 13 nitrogen transport-related genes are differentially expressed in the roots of S. portulacastrum after ‘BF-F’ inoculation. In the roots of S. portulacastrum, four nitrate transporters (NTRs), one ammonium transporter (AMT), one glutamine synthetase (GSs), four glutamate synthase (GOGATs), and one nitrate reductase (NR) were up-regulated after ‘BF-F’ inoculation (Table 1). In leaves, three GOGATs were differentially expressed in the aboveground part of S. portulacastrum (Table 1).
The nitrogen contents in the root and aboveground part were detected to demonstrate whether ‘BF-F’ inoculation improved nitrogen uptake and nitrogen assimilation efficiency in S. portulacastrum. The results showed that ‘BF-F’ inoculation could significantly increase the contents of total nitrogen (TN), ammonia nitrogen (NH3+-N), and nitrate nitrogen (NO3−-N) in the roots of S. portulacastrum. In the aboveground part of S. portulacastrum, the contents of TN and NH3+-N were increased (Figure 3A). The RT-PCR results showed that the expression levels of the SpNTR1, SpNTR2, SpNTR3, SpGOGAT1, SpGOGAT2, and SpNR1 genes in the roots of S. portulacastrum inoculated with ‘BF-F’ were significantly higher than those in the control group (Figure 3B).

3.5. Cladosporium sp. ‘BF-F’ Promotes the Growth of S. portulacastrum by Synthesizing IAA and ZT

Previous studies have reported that many growth-promoting fungi promote plant growth by synthesizing hormone-like substances. Considering that the fungus promotes the growth of S. portulacastrum without direct contact with plants, we speculate that it may play a role in promoting growth through metabolites. Therefore, we performed a sequencing analysis of the fungal metabolome. The enrichment result of GO found that the ‘BF-F’ metabolites are mainly involved in amino acid metabolism, carbohydrate metabolism, nucleotide metabolism, lipid metabolism, metabolism of cofactors and vitamins, and biosynthesis of other secondary metabolism (Figure 4A). Combined with metabolome data and substance content detection experiments, we found that Cladosporium sp. ‘BF-F’ can produce IAA and ZT, which play significant roles in the growth of plants. (Figure 4B).

4. Discussion

With the continuous increase in population, the issue of food security has become increasingly prominent. The current agricultural activities are overly dependent on applying chemical fertilizers, which will lead to soil degradation, nutrient imbalance, and other environmental problems [35]. Plant growth-promoting rhizobacteria (PGPR) refer to beneficial microorganisms that live in the rhizosphere of plants and can significantly enhance plant growth and stress resistance through various means, such as promoting nutrient absorption by plants and regulating and modulating plant hormones. As an important component of the plant rhizosphere ecological environment, PGPR contributes to soil health and sustainable agricultural development [36]. Our research group previously isolated a plant growth-promoting fungus named ‘BF-F’ from the rhizosphere of the halophyte S. portulacastrum. Subsequently, we conducted strain identification and genomic analysis on ‘BF-F’ [29]. The results show that ‘BF-F’ was possibly a new Cladosporium species that was most homologous to C. angulosum. ‘BF-F’ can promote the growth of various plants, including S. portulacastrum, Arabidopsis thaliana, and rice [37]. This implies that ‘BF-F’ might apply to the development of microbial fertilizers.
We conducted subsequent studies to further elucidate the mechanism by which ‘BF-F’ promotes plant growth. This study initially expounds on how the endophytic fungus ‘BF-F’ in the root system of S. portulacastrum promotes plant growth. By inoculating ‘BF-F’ into the rhizosphere of the tissue culture seedlings of S. portulacastrum, we found that ‘BF-F’ could significantly promote the growth of plants (Figure 1A,B). To clarify the influence of ‘BF-F’ on the expression of S. portulacastrum genes, we conducted transcriptome sequencing on the roots and leaves of the experimental group and the control group (Figure 1C,D). By conducting metabolic pathway enrichment analysis on the DEGs, it was found that multiple pathways related to plant growth were enriched, including zeatin biosynthesis, plant hormone and signal transduction, nitrogen metabolism, and indole alkaloid biosynthesis (Figure 2A). Therefore, in our subsequent research, we focused on the effects of ‘BF-F’ inoculation on genes related to S. portulacastrum dentate nitrogen metabolism and genes related to hormone signal transduction.
Plant hormones are a group of small signaling molecules that regulate plant growth. They affect various physiological processes in plants at extremely low concentrations, such as cell elongation, tissue differentiation, and cell division [38]. Many studies have shown that PGPRs regulate plant growth by modulating hormone levels. Indole-3-acetic acid (IAA) is an important plant hormone that can significantly promote the growth of the shoots and roots of plants. Previous studies found that many PGPR can secrete large amounts of IAA, which promotes the development of plant roots and enhances the utilization efficiency of water and nutrients by plants [39]. For example, four PGPR isolated from sandy soil, Streptomyces cinereoruber strain P6-4, Priestia megaterium strain P12, Rossellomorea aquimaris strain P22-2, and Pseudomonas plecoglossicida strain P24, can produce considerable amounts of IAA [39]. Our study also detected that ‘BF-F’ can produce IAA (Figure 4B). The production of IAA by PGPR can influence hormone signal transduction in plants, thereby affecting plant growth and development. For example, the PGPR Serratia marcescens PLR screened from the Arabidopsis rhizosphere induced the IAA biosynthesis genes in plants and could synthesize IAA [37]. After the PLR treatment, 80% of the auxin-related genes were enhanced. In our study, after treatment with ‘BF-F’ in the roots, many genes related to auxin signal transduction changed their expression. The expression levels of TIR genes, ARF genes, and SAUR genes were up-regulated. Meanwhile, the expression levels of most AUX genes decreased (Figure 2C). In the auxin signal transduction pathway, ARF family proteins and Aux/IAA family proteins form heterodimers and do not have transcriptional regulatory functions. When the auxin content increases, the TIR1/AFB receptor binds to auxin and tightly binds to the Aux/IAA protein family, mediating its ubiquitination. The Aux/IAA protein is degraded by the 26S proteasome, thereby releasing ARF. ARF forms homodimers to promote or inhibit the transcription of downstream genes, thereby generating the auxin response. In our results, the decrease in AUX expression and the increase in ARF expression imply that the auxin signaling pathway is enhanced after the ‘BF-F’ treatment. The auxin synthesized by ‘BF-F’ might trigger this. Contrary to the auxin signal transduction pathway, the key positive regulatory gene B-ARR in the cytokinin signal pathway shows a decrease in its expression level. While type A-ARRs act as negative regulators of cytokinin signaling, their expression levels increase (Figure 2D). Type A ARRs can inhibit the activity of type B-ARRs. Cytokinin can activate the ARR1 gene and the ARR2 gene. These two B-ARRs can inhibit the expression of the LAX2 gene, whose product is an auxin transport protein, thereby suppressing the differentiation of roots. This might explain why ‘BF-F’ can promote the differentiation of S. portulacastrum roots and increase the number of roots (Figure 1B).
Another important mechanism by which plant growth-promoting fungi promote plant growth is to facilitate the absorption of minerals and nutrients (N, P, K, and Fe) by plants. For example, Trichoderma viride BHU-2953-treated soybeans had longer root length and higher physiological use efficiency of N and P [40]. Among the various nutrients in plants, nitrogen is particularly crucial for their growth. Nitrogen is the fundamental component of plant chlorophyll, genetic material, protein, and other major organic molecules. Plant growth largely depends on applying nitrogen fertilizers, so improving plant nitrogen use efficiency (NUE) is the key to sustainable agricultural development [41]. In this study, we found that the nitrogen metabolism pathway was significantly enriched in the KEGG analysis (Figure 2A,B). This indicates that the ‘BF-F’ fungus affects the nitrogen metabolism of plants. We further analyzed the effect of ‘BF-F’ fungal inoculation on the nitrogen content of S. portulacastrum. The results showed that inoculation of ‘BF-F’ can promote the contents of total nitrogen, nitrate nitrogen, and ammonia nitrogen in S. portulacastrum (Figure 3A). Plant nitrogen use is inherently complex because multiple interacting genetic and environmental factors control each step, including nitrogen uptake, transport, assimilation, and remobilization. Plants primarily acquire inorganic nitrogen forms, NO3− and NH4+, from the soil. The NO3− transporter (NRT) and NH4+ transporter (AMT) family proteins are generally responsible for the uptake of NO3− and NH4+ in roots [42]. This study found that ‘BF-F’ can promote the expression of NRT and AMT genes in the roots of S. portulacastrum (Table 1, Figure 3B). Therefore, ‘BF-F’ can promote plant absorption of NO3− and NH4+. Furthermore, ‘BF-F’ inoculation significantly increased the number of roots, which is also an essential reason for enhancing the nitrogen absorption capacity of plants (Figure 1B). In addition to N acquisition, efficient nitrogen assimilation is crucial for yield and thus N utilization. In plants, NO3− is reduced to nitrite by NO3− reductase (NR) and then to NH4+ by nitrite reductase (NiR) [43]. NH4+ directly transported into the plants or derived from other sources is metabolized through the glutamine synthetase (GS)/glutamate oxidase (GOGAT) cycle for amino acid and protein metabolism. In the roots of S. portulacastrum, inoculation of ‘BF-F’ promoted the expression of GOGAT and NR genes (Table 1, Figure 3B). This is conducive to enhancing the N assimilation.

5. Conclusions

Our research group isolated an endophytic fungus ‘BF-F’ from the root of the S. portulacastrum. This study aims to preliminarily analyze the mechanism by which ‘BF-F’ promotes plant growth. Based on the transcriptome of S. portulacastrum and fungal metabolome data, we think that the growth-promoting effect of ‘BF-F’ mainly comes from two aspects: 1. ‘BF-F’ promotes the plant nitrogen use efficiency of S. portulacastrum by increasing the expression of nitrogen metabolism-related genes; 2. ‘BF-F’ promotes plant growth by producing IAA and ZT, which affect auxin and ZT signal transduction in S. portulacastrum, and promote plant growth (Figure 5).

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/agriculture15141522/s1, Table S1: sequences of the primers used in this study; Table S2: summary of RNA-seq data for each sample; Table S3: BUSCO-summary.

Author Contributions

Conceptualization, X.W. and D.W.; methodology, W.Z.; validation, D.C. and W.Z.; formal analysis, D.W.; investigation, D.W.; resources, X.W.; data curation, D.W.; writing—original draft preparation, D.W.; writing—review and editing, X.W.; supervision, X.W.; funding acquisition, X.W. and D.W.; All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Science and Technology Project of the Fuzhou Institute of Oceanography (2025F22), the University-Industry Cooperation Project of Fujian Province (2023N5016), and the Fuzhou Science and Technology Project (2024-Y-024).

Institutional Review Board Statement

Not applicable.

Data Availability Statement

The original contributions presented in this study are included in the article. Further inquiries can be directed to the corresponding author.

Acknowledgments

The authors would like to thank Jianjun Chen for reviewing this article.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Cladosporium sp. ‘BF-F’ promotes the growth of S. portulacastrum. (A) Compared with the control plant (Mock), inoculation of ‘BF-F’ significantly promoted the growth of S. portulacastrum. Bar = 1 cm. (B) Statistics of plant height and root length. The significance of difference analysis on data was performed using SPSS based on Tukey’s HSD test at the p < 0.01 (**) levels. (C) Hierarchical clustering of 12 samples based on the correlation coefficient (r2) from RNA-seq. F_AP and F_R were samples from the aboveground part and root of the S. portulacastrum 14 d after ‘BF-F’ inoculation, respectively. CK_AP and CK_R were samples from the aboveground part (AP) and root of the control plant. (D) Statistics of DEG numbers in the roots and aboveground part.
Figure 1. Cladosporium sp. ‘BF-F’ promotes the growth of S. portulacastrum. (A) Compared with the control plant (Mock), inoculation of ‘BF-F’ significantly promoted the growth of S. portulacastrum. Bar = 1 cm. (B) Statistics of plant height and root length. The significance of difference analysis on data was performed using SPSS based on Tukey’s HSD test at the p < 0.01 (**) levels. (C) Hierarchical clustering of 12 samples based on the correlation coefficient (r2) from RNA-seq. F_AP and F_R were samples from the aboveground part and root of the S. portulacastrum 14 d after ‘BF-F’ inoculation, respectively. CK_AP and CK_R were samples from the aboveground part (AP) and root of the control plant. (D) Statistics of DEG numbers in the roots and aboveground part.
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Figure 2. Inoculation of ‘BF-F’ affected hormone signaling transduction in S. portulacastrum. (A,B) KEGG analysis of DEGs in the root and aboveground parts. (A) The top 30 pathways were significantly enriched in roots after 14 d of ‘BF-F’ inoculation. (B) The top 30 pathways were significantly enriched in the aboveground part after 14 d of ‘BF-F’ inoculation. Expression analysis of DEGs involved in IAA and ZT signaling pathway after ‘BF-F’ inoculation; (C) Expression analysis of DEGs in roots of S. portulacastrum and aboveground part involved in IAA signaling pathway after 14 d of ‘BF-F’ inoculation. (D) Expression analysis of DEGs in roots of S. portulacastrum and the aboveground part involved in ZT signaling pathway after 14 d of ‘BF-F’ inoculation.
Figure 2. Inoculation of ‘BF-F’ affected hormone signaling transduction in S. portulacastrum. (A,B) KEGG analysis of DEGs in the root and aboveground parts. (A) The top 30 pathways were significantly enriched in roots after 14 d of ‘BF-F’ inoculation. (B) The top 30 pathways were significantly enriched in the aboveground part after 14 d of ‘BF-F’ inoculation. Expression analysis of DEGs involved in IAA and ZT signaling pathway after ‘BF-F’ inoculation; (C) Expression analysis of DEGs in roots of S. portulacastrum and aboveground part involved in IAA signaling pathway after 14 d of ‘BF-F’ inoculation. (D) Expression analysis of DEGs in roots of S. portulacastrum and the aboveground part involved in ZT signaling pathway after 14 d of ‘BF-F’ inoculation.
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Figure 3. Nitrogen content detection and related gene expression analysis after inoculation of ‘BF-F’. (A) The contents of total nitrogen (TN), ammonia nitrogen (NH3+-N), and nitrate nitrogen (NO3−-N); CK_AP and CK_R mean samples from the aboveground part (AP) and roots of the control group. F_AP and F_R mean samples from the aboveground part (AP) and roots of the ‘BF-F’ inoculation group. (B) Expression analysis of DEGs involved in nitrogen uptake. The error bars were calculated from three biological replicates. Mean differences were analyzed based on Tukey’s HSD test at p < 0.05 (*) and p < 0.01 (**) levels.
Figure 3. Nitrogen content detection and related gene expression analysis after inoculation of ‘BF-F’. (A) The contents of total nitrogen (TN), ammonia nitrogen (NH3+-N), and nitrate nitrogen (NO3−-N); CK_AP and CK_R mean samples from the aboveground part (AP) and roots of the control group. F_AP and F_R mean samples from the aboveground part (AP) and roots of the ‘BF-F’ inoculation group. (B) Expression analysis of DEGs involved in nitrogen uptake. The error bars were calculated from three biological replicates. Mean differences were analyzed based on Tukey’s HSD test at p < 0.05 (*) and p < 0.01 (**) levels.
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Figure 4. Analysis of Cladosporium sp. ‘BF-F’ metabolites. (A) GO annotation analysis of Cladosporium sp. ‘BF-F’ metabolites; (B) Hormone content in different media was measured 14 d after Cladosporium sp. ‘BF-F’ inoculation.
Figure 4. Analysis of Cladosporium sp. ‘BF-F’ metabolites. (A) GO annotation analysis of Cladosporium sp. ‘BF-F’ metabolites; (B) Hormone content in different media was measured 14 d after Cladosporium sp. ‘BF-F’ inoculation.
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Figure 5. ‘BF-F’ promotes S. portulacastrum growth by enhancing nitrogen utilization efficiency and regulating hormone signal transduction. The blue arrow and the red arrow, respectively, represent a decrease or an increase in gene expression.
Figure 5. ‘BF-F’ promotes S. portulacastrum growth by enhancing nitrogen utilization efficiency and regulating hormone signal transduction. The blue arrow and the red arrow, respectively, represent a decrease or an increase in gene expression.
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Table 1. Expression of nitrogen transport-related genes in roots of S. portulacastrum after. Cladosporium sp. ‘BF-F’ inoculation.
Table 1. Expression of nitrogen transport-related genes in roots of S. portulacastrum after. Cladosporium sp. ‘BF-F’ inoculation.
Gene IDLog2FoldChangeDescription
DEGs expressed in roots
Cluster-1879.215943.61High-affinity nitrate transporter 2.5 OS = Arabidopsis thaliana
Cluster-1879.228142.62High-affinity nitrate transporter 2.5 OS = Arabidopsis thaliana
Cluster-1879.230371.59Probable peptide/nitrate transporter At3g43790 OS = Arabidopsis thaliana
Cluster-1879.393511.15Probable peptide/nitrate transporter At3g43790 OS = Arabidopsis thaliana
Cluster-1879.56503−1.84High-affinity nitrate transporter 2.6 OS = Arabidopsis thaliana
Cluster-1879.56504−1.64High-affinity nitrate transporter 2.4 OS = Arabidopsis thaliana
Cluster-1879.265021.49Ammonium Transporter Family/Translocation protein Sec62
Cluster-1879.625581.48Glutamine synthetase type III N terminal
Cluster-1879.412761.79Glutamate synthase 1 [NADH], chloroplastic-like isoform X3 [Chenopodium quinoa]
Cluster-1879.286315.68Glutamate synthase 1 [NADH], chloroplastic [Vitis vinifera]
Cluster-1879.388373.81PREDICTED: Chenopodium quinoa glutamate synthase 1 [NADH], chloroplastic-like (LOC110728845), transcript variant X1, mRNA
Cluster-1879.430222.64PREDICTED: Beta vulgaris subsp. vulgaris ferredoxin-dependent glutamate synthase, chloroplastic (LOC104889481), mRNA
Cluster-1879.356152.20Nitrate reductase [NADH] OS = Spinacia oleracea OX = 3562 GN = NIA PE = 2 SV = 1
DEGs expressed in the aboveground part
Cluster-1879.412761.79Glutamate synthase 1 [NADH], chloroplastic OS = Arabidopsis thaliana
Cluster-1879.388373.81Glutamate synthase 1 [NADH], chloroplastic OS = Arabidopsis thaliana
Cluster-1879.286315.68Glutamate synthase 2 [NADH], chloroplastic OS = Oryza sativa subsp. japonica
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Wang, D.; Zhang, W.; Cao, D.; Wei, X. Transcriptome Analysis Elucidates the Mechanism of an Endophytic Fungus Cladosporium sp. ‘BF-F’ in Enhancing the Growth of Sesuvium portulacastrum. Agriculture 2025, 15, 1522. https://doi.org/10.3390/agriculture15141522

AMA Style

Wang D, Zhang W, Cao D, Wei X. Transcriptome Analysis Elucidates the Mechanism of an Endophytic Fungus Cladosporium sp. ‘BF-F’ in Enhancing the Growth of Sesuvium portulacastrum. Agriculture. 2025; 15(14):1522. https://doi.org/10.3390/agriculture15141522

Chicago/Turabian Style

Wang, Dan, Wenbin Zhang, Dinging Cao, and Xiangying Wei. 2025. "Transcriptome Analysis Elucidates the Mechanism of an Endophytic Fungus Cladosporium sp. ‘BF-F’ in Enhancing the Growth of Sesuvium portulacastrum" Agriculture 15, no. 14: 1522. https://doi.org/10.3390/agriculture15141522

APA Style

Wang, D., Zhang, W., Cao, D., & Wei, X. (2025). Transcriptome Analysis Elucidates the Mechanism of an Endophytic Fungus Cladosporium sp. ‘BF-F’ in Enhancing the Growth of Sesuvium portulacastrum. Agriculture, 15(14), 1522. https://doi.org/10.3390/agriculture15141522

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