Comparative genomics and stable isotope analysis reveal the saprotrophic-pathogenic lifestyle of a neotropical fungus.

In terrestrial forested ecosystems, fungi may interact with trees in at least three distinct ways: (i) associated with roots as symbionts; (ii) as pathogens in roots, trunks, leaves, flowers, and fruits; or (iii) decomposing dead tree tissues on soil or even on dead tissues in living trees. Distinguishing the latter two nutrition modes is rather difficult in Hymenochaetaceae (Basidiomycota) species. Herein, we have used an integrative approach of comparative genomics, stable isotopes, host tree association, and bioclimatic data to investigate the lifestyle ecology of the scarcely known neotropical genus Phellinotus, focusing on the unique species Phellinotus piptadeniae. This species is strongly associated with living Piptadenia gonoacantha (Fabaceae) trees in the Atlantic Forest domain on a relatively high precipitation gradient. Phylogenomics resolved P. piptadeniae in a clade that also includes both plant pathogens and typical wood saprotrophs. Furthermore, both genome-predicted Carbohydrate-Active Enzymes (CAZy) and stable isotopes (δ13C and δ15N) revealed a rather flexible lifestyle for the species. Altogether, our findings suggest that P. piptadeniae has been undergoing a pathotrophic specialization in a particular tree species while maintaining all the metabolic repertoire of a wood saprothroph. IMPORTANCE: This is the first genomic description for Phellinotus piptadeniae. This basidiomycete is found across a broad range of climates and ecosystems in South America, including regions threatened by extensive agriculture. This fungus is also relevant considering its pathotrophic-saprotrophic association with Piptadenia goanocantha, which we began to understand with these new results that locate this species among biotrophic and necrotrophic fungi.

Assaying Effector Cell-to-Cell Mobility in Plant Tissues Identifies Hypermobility and Indirect Manipulation of Plasmodesmata.

In plants, plasmodesmata establish cytoplasmic continuity between cells to allow for communication and resource exchange across the cell wall. While plant pathogens use plasmodesmata as a pathway for both molecular and physical invasion, the benefits of molecular invasion (cell-to-cell movement of pathogen effectors) are poorly understood. To establish a methodology for identification and characterization of the cell-to-cell mobility of effectors, we performed a quantitative live imaging-based screen of candidate effectors of the fungal pathogen Colletotrichum higginsianum. We predicted C. higginsianum effectors by their expression profiles, the presence of a secretion signal, and their predicted and in planta localization when fused to green fluorescent protein. We assayed for cell-to-cell mobility of nucleocytosolic effectors and identified 14 that are cell-to-cell mobile. We identified that three of these effectors are "hypermobile," showing cell-to-cell mobility greater than expected for a protein of that size. To explore the mechanism of hypermobility, we chose two hypermobile effectors and measured their impact on plasmodesmata function and found that even though they show no direct association with plasmodesmata, each increases the transport capacity of plasmodesmata. Thus, our methods for quantitative analysis of cell-to-cell mobility of candidate microbe-derived effectors, or any suite of host proteins, can identify cell-to-cell hypermobility and offer greater understanding of how proteins affect plasmodesmal function and intercellular connectivity. [Formula: see text] Copyright © 2024 The Author(s). This is an open access article distributed under the CC BY 4.0 International license.

Hyphal Growth and Conidia Germination Are Induced by Phytohormones in the Root Colonizing and Plant Growth Promoting Fungus Metarhizium guizhouense.

Beneficial associations are very important for plants and soil-dwelling microorganisms in different ecological niches, where communication by chemical signals is relevant. Among the chemical signals, the release of phytohormones by plants is important to establish beneficial associations with fungi, and a recently described association is that of the entomopathogenic ascomycete fungus Metarhizium with plants. Here, we evaluated the effect of four different phytohormones, synthetic strigolactone (GR24), sorgolactone (SorL), 3-indolacetic acid (IAA) and gibberellic acid (GA3), on the fungus Metarhizium guizhouense strain HA11-2, where the germination rate and hyphal elongation were determined at three different times. All phytohormones had a positive effect on germination, with GA3 showing the greatest effect, and for hyphal length, on average, the group treated with synthetic strigolactone GR24 showed greater average hyphal length at 10 h of induction. This work expands the knowledge of the effect of phytohormones on the fungus M. guizhouense, as possible chemical signals for the rapid establishment of the fungus-plant association.

Drought Stress Exacerbates Fungal Colonization and Endodermal Invasion and Dampens Defense Responses to Increase Dry Root Rot in Chickpea.

Drought plays a central role in increasing the incidence and severity of dry root rot (DRR) disease in chickpea. This is an economically devastating disease, compromising chickpea yields particularly severely in recent years due to erratic rainfall patterns. Macrophomina phaseolina (formerly Rhizoctonia bataticola) is the causal agent of DRR disease in the chickpea plant. The infection pattern in chickpea roots under well-watered conditions and drought stress are poorly understood at present. This study provides detailed disease symptomatology and the characteristics of DRR fungus at morphological and molecular levels. Using microscopy techniques, the infection pattern of DRR fungus in susceptible chickpea roots was investigated under well-watered and drought-stress conditions. Our observations suggested that drought stress intensifies the progression of already ongoing infection by weakening the endodermal barrier and overall defense. Transcriptomic analysis suggested that the plant's innate immune defense program is downregulated in infected roots when subjected to drought stress. Furthermore, genes involved in hormonal regulation are differentially expressed under drought stress. These findings provide hints in terms of potential chickpea genes to target in crop improvement programs to develop climate-change-resilient cultivars.[Formula: see text] Copyright © 2022 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.

Comparative Genomics of Fusarium circinatum Isolates Used to Screen Southern Pines for Pitch Canker Resistance.

Pitch canker, caused by the fungal pathogen Fusarium circinatum, is a global disease affecting many Pinus spp. Often fatal, this disease causes significant mortality in both commercially grown and natural pine forests and is an issue of current and growing concern. F. circinatum isolates collected from three locations in the U.S. state of Florida were shown to be virulent on both slash and loblolly pine, with two of the isolates causing equivalent and significantly larger lesions than those caused by the third isolate during pathogenicity trials. In addition, significant genetic variation in lesion length in the pedigreed slash pine population was evident and rankings of parents for lesion length were similar across isolates. Experimental data demonstrate that both host and pathogen genetics contribute to disease severity. High-quality genomic assemblies of all three isolates were created and compared for structural differences and gene content. No major structural differences were observed among the isolates; however, missing or altered genes do contribute to genomic variation in the pathogen population. This work evaluates in planta virulence among three isolates of F. circinatum, provides genomic resources to facilitate study of this organism, and details comparative genomic methods that may be used to explore the pathogen's contribution to disease development.[Formula: see text] Copyright © 2022 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.

Arabidopsis GOLD36/MVP1/ERMO3 Is Required for Powdery Mildew Penetration Resistance and Proper Targeting of the PEN3 Transporter.

The Arabidopsis PENETRATION 3 (PEN3) ATP binding cassette (ABC) transporter contributes to penetration resistance against nonadapted powdery mildew fungi and is targeted to papillae deposited at sites of interaction with the fungus. Timely recruitment of PEN3 and other components of penetration resistance to the host-pathogen interface is important for successful defense against this biotrophic pathogen. A forward genetic screen was previously carried out to identify Arabidopsis mutants that mistarget the PEN3 transporter or fail to accumulate PEN3 at sites of attempted powdery mildew penetration. This study focuses on PEN3 mistargeting in the aberrant localization of PEN3 4 (alp4) mutant and identification of the causal gene. In the alp4 mutant, PEN3 accumulates within the endomembrane system in an apparently abnormal endoplasmic reticulum and is not exported into papillae at powdery mildew penetration sites. This targeting defect compromises defenses at the host-pathogen interface, resulting in increased penetration success by a nonadapted powdery mildew. Genetic mapping identified alp4 as an allele of GOLGI DEFECTS 36 (GOLD36), a gene encoding a GDSL-lipase/esterase family protein that is involved in maintaining normal morphology and organization of multiple endomembrane compartments. Genetic complementation confirmed that mutation in GOLD36 is responsible for the PEN3 targeting and powdery mildew penetration resistance defects in alp4. These results reinforce the importance of endomembrane trafficking in resistance to haustorium-forming phytopathogens such as powdery mildew fungi.[Formula: see text] Copyright © 2022 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.

A Conserved Hypothetical Gene Is Required but Not Sufficient for Ptr ToxC Production in Pyrenophora tritici-repentis.

The fungus Pyrenophora tritici-repentis causes tan spot, an important foliar disease of wheat worldwide. The fungal pathogen produces three necrotrophic effectors, namely Ptr ToxA, Ptr ToxB, and Ptr ToxC to induce necrosis or chlorosis in wheat. Both Ptr ToxA and Ptr ToxB are proteins, and their encoding genes have been cloned. Ptr ToxC was characterized as a low-molecular weight molecule 20 years ago but the one or more genes controlling its production in P. tritici-repentis are unknown. Here, we report the genetic mapping, molecular cloning, and functional analysis of a fungal gene that is required for Ptr ToxC production. The genetic locus controlling the production of Ptr ToxC, termed ToxC, was mapped to a subtelomeric region using segregating biparental populations, genome sequencing, and association analysis. Additional marker analysis further delimited ToxC to a 173-kb region. The predicted genes in the region were examined for presence/absence polymorphism in different races and isolates leading to the identification of a single candidate gene. Functional validation showed that this gene was required but not sufficient for Ptr ToxC production, thus it is designated as ToxC1. ToxC1 encoded a conserved hypothetical protein likely located on the vacuole membrane. The gene was highly expressed during infection, and only one haplotype was identified among 120 isolates sequenced. Our work suggests that Ptr ToxC is not a protein and is likely produced through a cascade of biosynthetic pathway. The identification of ToxC1 is a major step toward revealing the Ptr ToxC biosynthetic pathway and studying its molecular interactions with host factors.[Formula: see text] Copyright © 2022 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.

The Endophytic Fungus Cyanodermella asteris Influences Growth of the Nonnatural Host Plant Arabidopsis thaliana.

Cyanodermella asteris is a fungal endophyte from Aster tataricus, a perennial plant from the northern part of Asia. Here, we demonstrated an interaction of C. asteris with Arabidopsis thaliana, Chinese cabbage, rapeseed, tomato, maize, or sunflower resulting in different phenotypes such as shorter main roots, massive lateral root growth, higher leaf and root biomass, and increased anthocyanin levels. In a variety of cocultivation assays, it was shown that these altered phenotypes are caused by fungal CO2, volatile organic compounds, and soluble compounds, notably astins. Astins A, C, and G induced plant growth when they were individually included in the medium. In return, A. thaliana stimulates the fungal astin C production during cocultivation. Taken together, our results indicate a bilateral interaction between the fungus and the plant. A stress response in plants is induced by fungal metabolites while plant stress hormones induced astin C production of the fungus. Interestingly, our results not only show unidirectional influence of the fungus on the plant but also vice versa. The plant is able to influence growth and secondary metabolite production in the endophyte, even when both organisms do not live in close contact, suggesting the involvement of volatile compounds.[Formula: see text] Copyright © 2021 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.

EffectorP 3.0: Prediction of Apoplastic and Cytoplasmic Effectors in Fungi and Oomycetes.

Many fungi and oomycete species are devasting plant pathogens. These eukaryotic filamentous pathogens secrete effector proteins to facilitate plant infection. Fungi and oomycete pathogens have diverse infection strategies and their effectors generally do not share sequence homology. However, they occupy similar host environments, either the plant apoplast or plant cytoplasm, and, therefore, may share some unifying properties based on the requirements of these host compartments. Here, we exploit these biological signals and present the first classifier (EffectorP 3.0) that uses two machine-learning models: one trained on apoplastic effectors and one trained on cytoplasmic effectors. EffectorP 3.0 accurately predicts known apoplastic and cytoplasmic effectors in fungal and oomycete secretomes with low estimated false-positive rates of 3 and 8%, respectively. Cytoplasmic effectors have a higher proportion of positively charged amino acids, whereas apoplastic effectors are enriched for cysteine residues. The combination of fungal and oomycete effectors in training leads to a higher number of predicted cytoplasmic effectors in biotrophic fungi. EffectorP 3.0 expands predicted effector repertoires beyond small, cysteine-rich secreted proteins in fungi and RxLR-motif containing secreted proteins in oomycetes. We show that signal peptide prediction is essential for accurate effector prediction, because EffectorP 3.0 recognizes a cytoplasmic signal also in intracellular, nonsecreted proteins.[Formula: see text] Copyright © 2022 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.

Cell-to-Cell Communication During Plant-Pathogen Interaction.

Being sessile, plants are continuously challenged by changes in their surrounding environment and must survive and defend themselves against a multitude of pathogens. Plants have evolved a mode for pathogen recognition that activates signaling cascades such as reactive oxygen species, mitogen-activated protein kinase, and Ca2+ pathways, in coordination with hormone signaling, to execute the defense response at the local and systemic levels. Phytopathogens have evolved to manipulate cellular and hormonal signaling and exploit hosts' cell-to-cell connections in many ways at multiple levels. Overall, triumph over pathogens depends on how efficiently the pathogens are recognized and how rapidly the plant response is initiated through efficient intercellular communication via apoplastic and symplastic routes. Here, we review how intercellular communication in plants is mediated, manipulated, and maneuvered during plant-pathogen interaction.[Formula: see text] The author(s) have dedicated the work to the public domain under the Creative Commons CC0 "No Rights Reserved" license by waiving all of his or her rights to the work worldwide under copyright law, including all related and neighboring rights, to the extent allowed by law, 2022.

The Impact of Elsinoë ampelina Infection on Key Metabolic Properties in Vitis vinifera 'Red Globe' Berries via Multiomics Approaches.

Grape anthracnose caused by Elsinoë ampelina (Shear) is one of the most serious fungal diseases that lead to the quality reduction and yield losses of grape (Vitis vinifera 'Red Globe') berries. In the present study, metabolome and transcriptome analyses were conducted using grape berries in the field after infection with E. ampelina at 7, 10, and 13 days to identify the metabolic properties of berries. In total, 132 metabolites with significant differences and 6,877 differentially expressed genes were detected and shared by three comparisons. The analyses demonstrated that phenylpropanoid, flavonoid, stilbenoid, and nucleotide metabolisms were enriched in E. ampelina-infected grape berries but not amino acid metabolism. Phenolamide, terpene, and polyphenole contents also accumulated during E. ampelina infection. The results provided evidence of the enhancement of secondary metabolites such as resveratrol, α-viniferin, ε-viniferin, and lignins involved in plant defense. The results showed the plant defense-associated metabolic reprogramming caused by E. ampelina infection in grape berry and provided a global metabolic mechanism under E. ampelina stimulation.[Formula: see text] Copyright © 2021 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.

Functional Annotation of circRNAs in Tea Leaves After Infection by the Tea Leaf Spot Pathogen, Lasiodiplodia theobromae.

Tea leaf spot, caused by Lasiodiplodia theobromae, is an important disease that can seriously decrease the production and quality of tea (Camellia sinensis (L.) O. Kuntze) leaves. The analysis of circular RNA (circRNA) in tea leaves after infection by the pathogen could improve understanding about the mechanism of host-pathogen interactions. In this study, high-performance sequencing of circRNA from C. sinensis Fuding-dabaicha leaves that had been infected with L. theobromae was conducted using the Illumina HiSeq 4000 platform. In total, 192 and 153 differentially expressed circRNAs from tea leaves were significantly up- and downregulated, respectively, after infection with L. theobromae. A gene ontology analysis indicated that the differentially expressed circRNA-hosting genes for DNA binding were significantly enriched. The genes with significantly differential expressions that were annotated in the specified database (S genes) were σ factor E isoform 1, triacylglycerol lipase SDP1, DNA-directed RNA polymerase III subunit 2, WRKY transcription factor WRKY24, and regulator of nonsense transcripts 1 homolog. A Kyoto Encyclopedia of Genes and Genomes analysis indicated that the significantly enriched circRNA-hosting genes involved in the plant-pathogen interaction pathway were Calmodulin-domain protein kinase 5 isoform 1, probable WRKY transcription factor 33, U-box domain-containing protein 35, probable inactive receptor-like protein kinase At3g56050, WRKY transcription factor WRKY24, mitogen-activated protein kinase kinase kinase YODA, SGT1, and protein DGS1. Functional annotation of circRNAs in tea leaves infected by L. theobromae will provide a valuable resource for future research on host-pathogen interactions.

Host Adaptation Through Hybridization: Genome Analysis of Triticale Powdery Mildew Reveals Unique Combination of Lineage-Specific Effectors.

The emergence of new fungal pathogens through hybridization represents a serious challenge for agriculture. Hybridization between the wheat mildew (Blumeria graminis f. sp. tritici) and rye mildew (B. graminis f. sp. secalis) pathogens has led to the emergence of a new mildew form (B. graminis f. sp. triticale) growing on triticale, a man-made amphiploid crop derived from crossing rye and wheat, which was originally resistant to the powdery mildew disease. The identification of the genetic basis of host adaptation in triticale mildew has been hampered by the lack of a reference genome. Here, we report the 141.4-Mb reference assembly of triticale mildew isolate THUN-12 derived from long-read sequencing and genetic map-based scaffolding. All 11 triticale mildew chromosomes were assembled from telomere-to-telomere and revealed that 19.7% of the hybrid genome was inherited from the rye mildew parental lineage. We identified lineage-specific regions in the hybrid, inherited from the rye or wheat mildew parental lineages, that harbor numerous bona fide candidate effectors. We propose that the combination of lineage-specific effectors in the hybrid genome is crucial for host adaptation, allowing the fungus to simultaneously circumvent the immune systems contributed by wheat and rye in the triticale crop. In line with this, we demonstrate the functional transfer of the SvrPm3 effector from wheat to triticale mildew, a virulence effector that specifically suppresses resistance of the wheat Pm3 allelic series. This transfer is the likely underlying cause for the observed poor effectiveness of several Pm3 alleles against triticale mildew and exemplifies the negative implications of pathogen hybridizations on resistance breeding.[Formula: see text] Copyright © 2021 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.

Context-Dependent Effects of Trichoderma Seed Inoculation on Anthracnose Disease and Seed Yield of Bean (Phaseolus vulgaris): Ambient Conditions Override Cultivar-Specific Differences.

Root colonizing Trichoderma fungi can stimulate plant immunity, but net effects are strain × cultivar-specific and changing ambient conditions further contribute to variable outcomes. Here, we used four Trichoderma spp. to inoculate seeds of four common bean (Phaseolus vulgaris) cultivars and explored in three different experimental setups the effects on fungal anthracnose after leaf inoculation with Colletotrichum lindemuthianum. Plants growing in pots with field soil under greenhouse conditions exhibited the highest and those in the open field the lowest overall levels of disease. Among 48 Trichoderma strain × bean cultivar × setup combinations, Trichoderma-inoculation enhanced disease in six and decreased disease in ten cases, but with the exception of T. asperellum B6-inoculated Negro San Luis beans, the strain × cultivar-specific effects on anthracnose severity differed among the setups, and anthracnose severity did not predict seed yield in the open field. In the case of Flor de Mayo beans, Trichoderma even reduced yield in anthracnose-free field plots, although this effect was counterbalanced in anthracnose-infected plots. We consider our work as a case study that calls for stronger emphasis on field experiments in the early phases of screenings of Trichoderma inoculants as plant biostimulants.

Computational Structural Genomics Unravels Common Folds and Novel Families in the Secretome of Fungal Phytopathogen Magnaporthe oryzae.

Structural biology has the potential to illuminate the evolution of pathogen effectors and their commonalities that cannot be readily detected at the primary sequence level. Recent breakthroughs in protein structure modeling have demonstrated the feasibility to predict the protein folds without depending on homologous templates. These advances enabled a genome-wide computational structural biology approach to help understand proteins based on their predicted folds. In this study, we employed structure prediction methods on the secretome of the destructive fungal pathogen Magnaporthe oryzae. Out of 1,854 secreted proteins, we predicted the folds of 1,295 proteins (70%). We showed that template-free modeling by TrRosetta captured 514 folds missed by homology modeling, including many known effectors and virulence factors, and that TrRosetta generally produced higher quality models for secreted proteins. Along with sensitive homology search, we employed structure-based clustering, defining not only homologous groups with divergent members but also sequence-unrelated structurally analogous groups. We demonstrate that this approach can reveal new putative members of structurally similar MAX effectors and novel analogous effector families present in M. oryzae and possibly in other phytopathogens. We also investigated the evolution of expanded putative ADP-ribose transferases with predicted structures. We suggest that the loss of catalytic activities of the enzymes might have led them to new evolutionary trajectories to be specialized as protein binders. Collectively, we propose that computational structural genomics approaches can be an integral part of studying effector biology and provide valuable resources that were inaccessible before the advent of machine learning-based structure prediction.[Formula: see text] Copyright © 2021 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.

Complete Genome Sequence of the Plant-Pathogenic Fungus Colletotrichum lupini.

Colletotrichum is a fungal genus (Ascomycota, Sordariomycetes, Glomerellaceae) that includes many economically important plant pathogens that cause devastating diseases of a wide range of plants. In this work, using a combination of long- and short-read sequencing technologies, we sequenced the genome of Colletotrichum lupini RB221, isolated from white lupin (Lupinus albus) in France during a survey in 2014. The genome was assembled into 11 nuclear chromosomes and a mitochondrial genome with a total assembly size of 63.41 Mb and 36.55 kb, respectively. In total, 18,324 protein-encoding genes have been predicted, of which only 39 are specific to C. lupini. This resource will provide insight into pathogenicity factors and will help provide a better understanding of the evolution and genome structure of this important plant pathogen.[Formula: see text] Copyright © 2021 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.

Telomere to Telomere Genome Assembly of Fusarium musae F31, Causal Agent of Crown Rot Disease of Banana.

Fusarium musae causes crown rot of banana and it is also associated to clinical fusariosis. A chromosome-level genome assembly of F. musae F31 obtained combining Nanopore long reads and Illumina paired-end reads resulted in 12 chromosomes plus one contig with overall N50 of 4.36 Mb, and is presented together with its mitochondrial genome (58,072 bp). The F31 genome includes telomeric regions for 11 of the 12 chromosomes representing one of the most complete genomes available in the Fusarium fujikuroi species complex. The high-quality assembly of the F31 genome will be a valuable resource for studying the pathogenic interactions occurring between F. musae and banana. Moreover, it represents an important resource for understanding the genome evolution in the F. fujikuroi species complex.[Formula: see text] Copyright © 2021 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.

Fumonisin B1 induced aggressiveness and infection mechanism of Fusarium proliferatum on banana fruit.

Mycotoxins are increasingly considered as micropollutants in the environment. Fumonisins, as one of the most important mycotoxins, cause potential health threats to humans and animals due to their ubiquitous contamination on cereals, fruit, vegetables and other environmental samples around the world. However, the contribution of fumonisins to the interaction of fungi with plant hosts is not still fully understood. Here, we investigated the effect of fumonisin B1 (FB1) on the infection of Fusarium proliferatum on banana fruit and the underlying mechanisms from the host perspective. Our results found that FB1 treatment increased the aggressiveness of F. proliferatum on banana fruit and inhibited the defense ability of banana fruit via decreasing phenylalanine ammonia lyase (PAL), ß-1,3-glucanase (GLU) and chitinase (CHI) activities. Meanwhile, FB1 accelerated cell death, indicated by higher relative conductivity, MDA content and higher transcripts of cell death-related genes. FB1 treatment resulted in higher hydrogen peroxide (H2O2) content possibly due to MaRBOHs induction. These consequences accelerated the ROS-dependent cell death, which subsequently result in reduction of disease resistance of banana fruit. Additionally, energy metabolism and MaDORN1s-mediated eATP signaling might involve in FB1-meidiated suppression of banana defense responses. Collectively, results of the current study indicated that FB1 contamination triggered the cell death of banana peel, subsequently instigating the invasion and growth of F. proliferatum on banana fruit. In summary, for the first time, we demonstrated a previously unidentified role of fumonisins as a potential virulence factor of F. proliferatum in modulating fruit defense response, which provides new insight on the biological roles of fumonisins.