Proteomics analysis of the phytopathogenic fungus Sclerotinia sclerotiorum: a narrative review : Journal of Bio-X Research

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Proteomics analysis of the phytopathogenic fungus Sclerotinia sclerotiorum: a narrative review

Otun, Oluwatobi Saraha,*; Achilonu, Ikechukwua; Ntushelo, Khayalethub

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doi: 10.1097/JBR.0000000000000130
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Abstract

Introduction

Sclerotinia sclerotiorum (S. sclerotiorum) is a necrotrophic plant pathogen that causes extensive infections in approximately 700 plant hosts around the world.[1]S. sclerotiorum utilizes cell wall–degrading enzymes, effectors, and oxalic acid as its pathogenic and virulence factors.[2] This fungus is responsible for several disease symptoms, such as wilt, drop, watery soft rot, white mold, and the formation of black sclerotia on infected stems and leaves of host plants.[3] Increased disease prevalence is due to environmental conditions such as heavy rainfall or irrigation, but a higher frequency of vulnerable hosts in crop rotation can help the pathogen create resistance and a protective structure known as “sclerotia.”[4] Canola, rape seed oil, sunflower, soybean, peanuts, potatoes, and tomatoes are among the economically important crops commonly affected by S. sclerotiorum, and infection often results in a major loss of agricultural productivity.[5,6] In the United States, S. sclerotiorum causes an estimated $200 million annually in agricultural yield losses.[4] Similarly, approximately $600 million and AUS$59 million in losses were reported, respectively, in Canada and Australia due to S. sclerotiorum infection of the canola crop in 2010.[7,8] In addition, Sclerotinia disease in soybean caused an estimated $560 million in losses in the United States, where it was reported as the second (out of 23) most common plant disease.[9] The impact of canola stem rot disease caused by S. sclerotinia received significant attention in South Africa in 2014 because of the higher disease incidence that occurred during that season compared with previous years.[10] During the 2013/2014 season, South Africa experienced an epidemic of S. sclerotiorum in sunflowers and soybean that resulted in crop losses of up to 60% to 65%, respectively.[11] Unfortunately, there is yet to be an effective and long-term solution to this global problem. The lack of complete knowledge and understanding of molecular composition and mechanism of action of its pathogenic proteins complicates the pathogenicity of S. sclerotiorum. Like any plant pathogen, various measures have been used to study S. sclerotiorum. Initial efforts relied on genomic techniques,[12–14] while later applications have involved transcriptomics analysis[15,16] and proteomic analysis using mass spectrometry (MS)[16–19] to decipher the pathogen.

To discover the molecular composition and mechanisms of action of S. sclerotiorum pathogenic proteins, MS-based proteomics, which is a reliable, accurate, convenient, high-throughput, and robust platform, has been used to detect and quantify proteins, identify its disease pathways, define pathways involved in modulation of the host immune response, and discover new management approaches.[17] Changes in protein abundance, in particular, can be studied simultaneously from the perspectives of both the host and the pathogen.[20] Protein quantification methods include label-free quantification, metabolic labeling, and isobaric tags for relative and absolute quantification.[21] Proteomics technologies have a wide range of applications and the procedures for sample preparation, quantification, and bioinformatic processing are likewise diverse, allowing for individualized and powerful profiling of biological systems.

There have been several MS-based proteomics studies on the ubiquitous fungal diseases caused by S. sclerotiorum. We began by discussing fungal pathogen, their virulence factors, proteins, and the mechanism of host suppression. In addition, we examined several recent proteomic studies and extrapolated findings to improve the detection and functional classification of S. sclerotiorum proteins. The objective of this review is to highlight recent discoveries in proteomic composition and characterization that are associated with the pathogenicity of S. sclerotiorum and it will contribute to developing a lasting solution to the global problem caused by this pathogen.

Database retrieval strategy

The literature review was done electronically utilizing the Google Scholar database. Relevant articles were initially included using the following keyword combinations: fungal pathogenesis, MS-based proteomics, plant pathogen, Sclerotinia sclerotiorum, virulent proteins, proteomic analysis of S. sclerotiorum. Majority of the included articles (80% of all references) were published between 2016 and 2022. Given its relevance in the phytopathology of S. sclerotiorum, an old publication from 1978 was added.

Definition of the fungal pathogen Sclerotinia sclerotiorum

S. sclerotiorum, a pathogen that infects a wide range of plants, belongs to the phylum Ascomycota, class Discomycetes, order Helotiales, family Sclerotiniaceae, and genus Sclerotinia.[3] The fungus causes approximately 40 disease symptoms (ie, white mold, wilt, stem rot) in approximately 600 plants, including economically important crops such as potatoes, beans, carrots, lettuce, tomatoes, and sunflower.[4,22,23] Recently, over 90% of sugar beet plants in Minnesota (USA) are infected with S. sclerotiorum, although the impact of the disease on yield and quality is difficult to estimate.[24]S. sclerotiorum diseases are difficult to control and cause increasing losses to economically important crops around the world.[25] Various reasons for the occurrence of this disease include but are not limited to (i) the lack of safe and effective fungicides, (ii) S. sclerotiorum has a unique life cycle that includes the development of survival structures (sclerotia) that are resistant to chemical and biological degradation, and (iii) the lack of sufficient data on the mechanism of action of its virulent factors.[23,26] Hence, continued research to fully comprehend the mechanism of the virulence factors associated with its pathogenicity is warranted.

Virulence factors

S. sclerotiorum swiftly adapts by creating specialized virulence factors to help it survive and reproduce in its plant host.[26,27]S. sclerotiorum is a necrotrophic fungus that feeds on dead cells by releasing several cell wall–degrading enzymes and toxins (oxalic acid).[28,29] This fungus has a two-phase infection process in which it first bypasses or neutralizes host defenses before growing in the apoplast.[28,30] In the host plant tissue, oxalic acid intercepts host processes and causes cell death.[31] The pathogen produces a variety of cell wall–degrading enzymes, as well as several proteases and hydrolases, which degrades the cell tissues to release nutrients, causing the host plant’s cells to die.[28,29,32] Sclerotinia’s extensive spectrum of enzymes (proteinases, cutinase, glucanases, etc) aids its adaptability and hence its large range of hosts.[30] Surprisingly, recent research has shown that genetically characterized mutants lacking oxalic acid but accumulating fumaric acid can cause infections in a range of plants, indicating that acidic pH, not necessarily oxalic acid, is essential for the development of S. sclerotiorum disease.[33] Many questions remain, however, about the fungus techniques for avoiding the host immune response, as well as the host’s defenses against invading pathogens and their clearance.

Virulence proteins and host defense suppression

Effector proteins are important virulence components of S. sclerotiorum.[14,34] Traditionally, fungal effectors have been defined as small proteins which affect the host cell to aid infection; however, they now encompass a broader variety of proteins and chemicals involved in the disease occurrence and progression.[14,22,35] Furthermore, bioinformatics approaches applied to the S. sclerotiorum genome sequence revealed a myriad of genes encoding virulence-related secretory effector proteins.[12]S. sclerotiorum may produce around 400 proteins, with about 80 candidate virulence proteins.[14,23] For example, the new effector protein SsERP1 (ethylene pathway repressor protein 1) can block ethylene signaling to promote S. sclerotiorum infection.[36] Furthermore, the characterization of SsYCP1 (YML079-like cupin protein) from S. sclerotiorum suggests that SsYCP1 is a possible effector protein of S. sclerotiorum.[37] Similarly, the Sclerotiorum secreted integrin-like protein SsITL, suppresses host defenses early during pathogenicity by interacting with the chloroplast-localized CAS protein of the plant chloroplast, which is a key regulator of salicylic acid signaling and Sclerotinia resistance.[32]

Sclerotinia-induced triggering and management of host cell death require the Cu/Zn superoxide dismutase SsSOD1 and the Ca-binding SsCAF1 protein.[7] On release of Ss-Cmu1 (chorismate mutase enzyme), the amount of salicylic acid produced by the host is reduced.[22] In another example, SsSSVP1 (cysteine-rich secreted protein) produced by S. sclerotiorum causes the death of host plant cells by interacting with plant QCR8, a subunit of the mitochondrial respiratory chain cytochrome b-c1 complex, and disrupting QCR8 localization in mitochondria.[38] In the Sclerotinia-Brassica pathosystem, S. sclerotiorum metabolizes harmful isothiocyanates produced by the plant through a hydrolase, allowing it to increase its development and virulence in plants producing glucosinolates.[39] SsATG8, a key component of the autophagy system, and its interactor SsNBR1, an autophagy receptor, have been found to be critical for vegetative growth, sclerotial formation, oxalic acid generation, appressoria development, and virulence.[40] Furthermore, the proteins found in sclerotial exudates play a role in the development of sclerotia and host cell necrosis induced by S. sclerotiorum.[19] Sclerotial exudates can break down plant cell walls, releasing sugars that fuel fungal growth and may aid in the formation of the fungal cell wall in sclerotia in development. Consequently, we have shaped our knowledge of the morphogenesis and pathogenicity of other sclerotia-forming fungi. These examples demonstrate how the Sclerotinia effector employs several ways to alter or avoid host cell functions, contributing to the disease’s broad host range and plant pathogen effectiveness. Further functional identification of these Sclerotinia virulence components (Fig. 1) could lead to a novel control strategy that directly targets the pathogen and/or indirectly targets its host.

F1
Figure 1.:
Mass spectrometry-based proteomics for the in vitro profiling of Sclerotinia sclerotiorum. Highlighted mechanisms define virulence factors such as cell wall–degrading enzymes, oxalic acid, acidic pH, effectors, and extracellular vesicles.

Proteomic profiling of Sclerotinia sclerotiorum

The proteomics research conducted by Tian et al[19] revealed critical virulence factors that include cell wall–degrading enzymes, oxalic acid, acidic pH, effectors, and extracellular exudates. For example, the relevance of exudates in the sclerotial growth of the organism was studied.[19] A total of 258 proteins were identified, 193 were GO-annotated, and 54 were classified using Kyoto Encyclopedia of Genes and Genomes analysis. Four proteins linked to plant cell wall degradation were further confirmed by measuring the related enzymatic activity of sclerotial exudates and/or evaluating gene expression during sclerotial development. Sclerotial exudate proteins appear to aid in the establishment of sclerotia and contribute to S. sclerotiorum-caused host cell necrosis, according to the findings. As a result, it was hypothesized that sclerotial exudates can break down plant cell walls and produce carbohydrates that help the fungus grow and possibly aid in the production of sclerotia cell walls. The morphology and pathogenicity of other sclerotia-forming fungi were also revealed in the study.[19]

Similarly, Otun and Ntushelo[23] profiled the proteome of in vitro germinated S. sclerotiorum (Fig. 2). Sodium dodecyl-sulfate polyacrylamide gel electrophoresis (SDS-PAGE) was used to separate proteins extracted from 5-day-old S. sclerotiorum, and the AB Sciex TripleToF 6600 mass spectrometer was used to annotate peaks, while MASCOT, SEQUEST, and Proteome Discoverer were used to search and analyze resulting data. There were 1471 proteins identified, including 45 kinases. Furthermore, the functional classification of the 78 proteins (with >50% similarity to the S. sclerotiorum protein database) revealed that 62% were involved in molecular functions, 25% involved in biological processes, and the remaining 13% involved in cellular functions. The significance of this study was to identify the hypothetically carcinogenic proteins (tripeptidyl-peptidase and ochratoxin) produced by S. sclerotiorum.

F2
Figure 2.:
Proteomic analysis of Sclerotinia sclerotiorum workflow. (1) Mycelia samples are collected from a 5-day-old culture. (2) On sample collection, proteins are extracted via mechanical (eg, grinding) and chemical (eg, detergent) cell lysis. (3) Digestion of proteins into peptides with sequence-specific enzymes (eg, trypsin and Lysine). (4) Peptides are separated by SDS-PAGE. (5) Peptides are then ionized (eg, electrospray ionization) and measured on a mass spectrometer (eg, liquid chromatography-tandem mass spectrometry). (6) Data analysis using a suite of bioinformatics platforms (eg, MaxQuant, Perseus). The acquired data can be input into a variety of downstream applications, including pathway analysis, protein–protein networks, functional characterization, and construction of repositories for data sharing. Created with BioRender.com. LC-MS/MS=liquid chromatography with tandem mass spectrometry, SDS-PAGE=sodium dodecyl-sulfate polyacrylamide gel electrophoresis.

In another proteomic study of S. sclerotiorum, MS was used to determine how SsNsd1 affected the development of the appressorium. Two-dimensional electrophoresis was used to perform a proteomic analysis on the wild-type and SsNsd1 mutant (2-DE). Forty-three proteins were found to be differentially expressed (threefold change), in which 77% were downregulated and 14% were upregulated, while the mutants completely lost four protein sites. Furthermore, MS was used to analyze the peptide mass of these protein sequences and 40 functionally annotated proteins were obtained, of which only 17 proteins (38%) had known functions in energy production, metabolism, protein production, stress response, cell organization, and cell growth, and division. The remaining 23 proteins (56%) were classified as hypothetical proteins and 4 (17%) contained signal peptides. Finally, the differentially expressed proteins identified in this study included SsNsd1 mutant-mediated appressorium deficiency, which can be explored in future studies to better understand SsNsd1 signaling in S. sclerotiorum.[41]

From the perspective of the host, the proteome changes in Sunflower stem tissues in response to S. sclerotiorum infection were studied. Partially resistant and susceptible sunflower lines with two true leaves were exposed using an S. sclerotiorum culture filtrate. At 24, 48, and 72 hours following treatment, two-dimensional electrophoresis was performed on the stems of treated and untreated plants. Matrix-assisted laser desorption/ionization-time of flight MS was used to observe 20 locations that had a larger than 1.5-fold change in abundance. Carbohydrate and energy metabolism (25%), stress response (15%), plant cell wall biogenesis (10%), photosynthesis (10%), protein metabolism (10%), unclear function (10%), and redox homeostasis (10%) were the most common (10%). The expression of proteins that are involved in carbohydrate metabolism and plant innate immunity (malate dehydrogenase and peroxidase), metabolic activities (adenosine kinase), cell redox homeostasis regulation (disulfide isomerase), and lignin biosynthesis (lignin biosynthetic process) was found to be upregulated in this study (laccase). When both sunflower lines were exposed to S. sclerotiorum culture filtrate, the expression of pyrroline-5-carboxylate reductase, which is involved in proline biosynthesis, was significantly altered. Proteins that were only upregulated in partially resistant lines could be important in mediating Sclerotinia defenses and could be exploited to develop resistance to this harmful fungus.[42]

Limitations

In the last few years, there have been a lot of advancements in the field of fungi proteomics. This is because of advancements in sample preparation, high-resolution protein separation techniques, MS software for effective protein identification and characterization, and bioinformatics. There are, nevertheless, a variety of technical obstacles to overcome. For instance, the amplification of low-abundance proteins is crucial, because there is no protein equivalent to PCR, hence a detection range of one to several million molecules per cell is required. Also, generic approaches are challenging to build and implement because proteins have features resulting from their folded shapes, and analyzing and interpreting these post-translational modifications is a huge challenge. Finally, certain technological procedures, such as protein separation and analysis, are skill-intensive and difficult to automate.[43]

Conclusion and future directions

In this review, key findings that have shaped this paradigm and our current understanding of virulent factors and the pathogenesis of S. sclerotiorum are presented and discussed. We anticipate that this overview will help improve our understanding of the S. sclerotiorum infection process and will lead to a better understanding of the intricacies that underlie, that is, the interactions of aggressive necrotrophic pathogens. Although in the accessible protein database of S. sclerotiorum, many of the proteins deposited were unidentified, predicted or hypothetical proteins with unknown/uncertain functions, therefore more functional characterization research is needed to define their roles in disease initiation or progression. Furthermore, based on the review of the literature, the latest statistical studies investigating the economic impact of S. sclerotiorum were published over 5 years ago. Therefore, there is an urgent need to conduct further research in several regions of the world. These data would help formulate policy and encourage more biotechnological research. Finally, in addition to agricultural importance, the medical relevance of these proteins should be investigated.

Acknowledgment

The authors acknowledge the support from Prof Ntushelo’s research group at the University of South Africa, Science campus-Florida.

Author contributions

OSO wrote the manuscript; KN conceptualized and proofread the manuscript; and IA advised and reviewed the manuscript. All authors approved the final version of the manuscript.

Financial support

This work was supported by the South African National Research Foundation (NRF; No. TTK170413227119) and the SARChI program of the Department of Science and Technology and the National Research Foundation for post-doctoral fellowship funding.

Conflicts of interest

The authors declare that there are no conflicts of interest.

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Keywords:

fungal pathogenesis; mass spectrometry–based proteomics; plant pathogen; Sclerotinia sclerotiorum; virulent proteins

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