Volume 9, Issue 12, December – 2024 International Journal of Innovative Science and Research Technology

ISSN No:-2456-2165 https://doi.org/10.5281/zenodo.14608940

Smut Fungi: A Comprehensive Review

Sudhir Diwase1 Arvind Dhabe2
Department of Botany, Vasantrao Naik Mahavidyalaya, Department of Botany, Dr. B. A. M. University,
Aurangabad-431 003, India Aurangabad-431 004, India

Balasaheb Ughade3 Ashwini Biradar4

Department of Botany, Amdar Shashikant Shinde Department of Microbiology, Dr. B. A. M. University,
Mahavidyalaya, Medha, India Sub Campus Osmanabad, Osmanabad 413501, India

Tejswini Sontakke5 Dinesh Nalage6

Department of Zoology, MGV's, MPH Mahila College, Department of Biotechnology,
Malegaon, Dist. Nashik (MH), India Maulana Azad College of Arts, Science & Commerce,
Aurangabad 431001 (MH), India.

Abstract:- Smut fungi (Ustilaginales), obligate plant I. INTRODUCTION

pathogens within the Basidiomycota phylum, play critical
roles in ecology and agriculture. Known for their host Fungi represent one of the most significant components
specificity and production of black powdery teliospores, of Earth's biotic system, contributing immensely to
these fungi predominantly infect monocots, including ecological balance, biodiversity, and agricultural systems. An
economically vital crops like wheat, rice, maize, and estimated 1.5 million fungal species have evolved over
sugarcane. Their global distribution and adaptability to approximately one billion years; however, only about 5% of
diverse climates make them significant contributors to these species have been documented and explored, leaving
agricultural losses, impacting food security and trade. 95% of fungal diversity unknown and uncharacterized
Traditional methods for identifying smut fungi, such as (Vabeikhokhei et al., 2019). This massive gap underscores
morphological and cultural analyses, are now the importance of advancing research in the field of
complemented by molecular techniques like DNA mycology, particularly in regions with high biodiversity such
barcoding, PCR, and next-generation sequencing (NGS). as the tropics and subtropics.
These advancements have refined fungal taxonomy,
uncovered cryptic species, and elucidated evolutionary Fungi are eukaryotic microorganisms that thrive in
relationships, enhancing the accuracy of identification diverse ecosystems across the globe, including extreme
and ecological understanding. India, a biodiversity environments like the Arctic, Antarctic, African deserts, and
hotspot, reports 159 species of smut fungi, primarily deep-sea thermal vents (Mikryukov et al., 2023; Tedersoo et
targeting the Poaceae family. Despite advancements, gaps al., 2014). Their versatility stems from their ability to adapt
remain in understanding their biodiversity, pathogenic to diverse climatic and ecological conditions, playing key
mechanisms, and responses to climate change. Addressing roles in nutrient cycling, decomposition, and symbiotic
these challenges necessitates interdisciplinary research, relationships with plants and animals.
integrating modern molecular tools with traditional
approaches. This review underscores the importance of II. SYSTEMATIC CLASSIFICATION AND
smut fungi research for developing sustainable disease DIVERSITY OF FUNGI
management strategies. By fostering global collaboration
and leveraging advanced techniques, researchers can Fungal taxonomy has been refined through
mitigate the agricultural impact of smut fungi while morphological, biochemical, and molecular studies, leading
exploring their ecological and biotechnological potential. to a clearer understanding of their diversity and evolutionary
Comprehensive studies are crucial for ensuring history. Fungi are traditionally classified into four major
agricultural sustainability, biodiversity conservation, and phyla:
enhanced food security in the face of emerging global
challenges.  Chytridiomycota: Aquatic fungi with flagellated spores,
often found in water and soil environments.
Keywords:- Smut Fungi, Fungal Taxonomy, Plant Pathogens,  Zygomycota: Terrestrial fungi known for their role in
Molecular Identification, Agricultural Sustainability. food spoilage and industrial fermentation.
 Ascomycota: The largest fungal group, comprising yeasts,
molds, and filamentous fungi.
 Basidiomycota: Includes macroscopic fungi such as
mushrooms, bracket fungi, rust fungi, and smut fungi.

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ISSN No:-2456-2165 https://doi.org/10.5281/zenodo.14608940
Recent advancements in molecular techniques have V. INDIAN CONTEXT: DIVERSITY AND
uncovered new fungal lineages, leading to the identification DISTRIBUTION OF SMUT FUNGI
of emerging fungal groups that challenge the traditional
taxonomic hierarchy. India's unique geographic and agro-climatic diversity
makes it an ideal location for studying fungal biodiversity.
In the Indian context, fungal diversity is unparalleled, The country harbors eight out of twelve recognized climatic
with more than 27,000 species identified to date. India ranks zones, ranging from temperate to alpine regions, with
among the top biodiversity hotspots, with its diverse climatic significant variations in temperature, rainfall, and humidity.
zones fostering the growth of fungi across 103 orders, 484 These conditions support the growth of a diverse range of
families, and 4,979 genera(Punjabi et al., 2020; Singh, 2020). smut fungi, particularly those parasitizing economically
significant crops.
III. BASIDIOMYCOTA: THE ROLE
OF SMUT FUNGI  From an Indian Perspective:

Within the phylum Basidiomycota, basidiomycetes  159 species of smut fungi belonging to 18 genera have
represent approximately 30% of the total fungal diversity. been reported.
This group includes smut fungi, rust fungi, and other plant  These species parasitize 189 host plants spanning eight
pathogens that hold immense ecological and economic families, with Poaceae being the most affected(Gautam et
significance. Smut fungi alone constitute about 10% of the al., 2021).
Basidiomycota, with their characteristic black powdery  The genus Ustilago dominates Indian smut fungi,
spores forming on infected plant tissues. comprising 48 species (30.38% of the total reported
species). Other important genera include Sporisorium and
Smut fungi are obligate plant-parasitic microorganisms Anthracocystis.
within the order Ustilaginales. They are second only to rust
fungi in terms of species diversity and impact. These fungi  Lesser-Known Genera in India:
are predominantly known for infecting monocots, particularly
members of the Poaceae (grasses) and Cyperaceae (sedges)  Ahmadiago
families, although they also parasitize dicots and herbaceous  Bambusiomyces
plants.  Cintractia
 Clinoconidium
 Key Features of Smut Fungi:
 Farysia
 Macalpinomyces
 Production of black powdery spores (teliospores) on
 Melanopsichium
infected tissues.
 Moesziomyces
 Obligate biotrophic lifecycle, requiring a living host for
completion.  Pericladium
 Infection primarily targets reproductive organs (e.g.,
These genera often exhibit host specificity, targeting
flowers, seeds) and meristematic tissues.
specific crop species and ecosystems.
 Widespread presence in both temperate and tropical
climates.
VI. MODE OF INFECTION AND
LIFE CYCLE OF SMUT FUNGI
IV. GLOBAL DISTRIBUTION AND
IMPORTANCE OF SMUT FUNGI
Smut fungi are systemic pathogens that target specific
plant tissues, primarily reproductive organs. The life cycle of
Globally, smut fungi are distributed across all
smut fungi involves:
continents, with notable prevalence in temperate regions
where conditions such as 30°C temperature and 100%
 Teliospore Production:
relative humidity favor their proliferation(Gautam et al.,
Smut fungi produce teliospores (thick-walled,
2021). The ability of smut fungi to adapt to diverse
melanized spores) on infected plant tissues. These spores
ecological conditions contributes to their persistence and
serve as survival structures under adverse environmental
impact on agricultural systems. For example:
conditions.
 Ustilago cynodontis (Couch smut): Infects Cynodon  Spore Germination:
dactylon (turfgrass) and thrives in temperate climates like Under favorable conditions, teliospores germinate,
Australia and desert environments such as
producing basidiospores that initiate infection.
Egypt(García‐Guzmán & Burdon, 1997).
 Ustilago sporoboli-indici: Successfully invaded southeast  Infection Process:
Queensland in Australia, where it infects Sporobolus Basidiospores infect host tissues, leading to systemic
natalensis. Originally endemic to Africa and Asia, its colonization. Infection often begins in the seedling stage and
rapid spread exemplifies the invasive potential of smut progresses to the reproductive organs.
fungi(Steinrucken & Vitelli, 2023).

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Volume 9, Issue 12, December – 2024 International Journal of Innovative Science and Research Technology
ISSN No:-2456-2165 https://doi.org/10.5281/zenodo.14608940
 Host Tissue Modification: Under severe conditions, losses may reach up to 80%, with
Infected tissues develop tumors or galls filled with sugar content reduced by 20%.
fungal spores. For example, Ustilago maydis causes tumor
formation in maize kernels. VIII. HUMAN AND ANIMAL
HEALTH IMPLICATIONS
 Spore Dissemination:
Mature spores are released into the environment, While smut fungi primarily infect plants, their impact
completing the lifecycle and perpetuating infection. on human and animal health cannot be overlooked. The rice
false smut pathogen Ustilaginoidea virens produces toxic
 Unique Features of Smut Fungal Infection: metabolites such as ustiloxins and ustilaginoidins, which
cause:
 Smut fungi utilize effector proteins to suppress host
immunity and manipulate plant cellular processes.  Hepatotoxicity: Liver damage in humans and animals.
 They exhibit host specificity, infecting selected plant  Teratogenesis: Disruption of embryonic development in
species while remaining dormant in others. pregnant individuals(Zhou et al., 2024).

VII. IMPACT OF SMUT FUNGI  Identification Techniques for Smut Fungi

ON AGRICULTURE
A. Conventional Techniques
Smut fungi pose a significant threat to global agriculture
by reducing crop yield, quality, and economic value. Their  Morphological Analysis
ability to infect staple crops like wheat, rice, maize, Traditionally, morphological analysis has been the
sugarcane, and sorghum exacerbates challenges related to cornerstone of fungal identification. This approach relies on
food security and trade restrictions. the examination of physical characteristics such as spore
shape, size, ornamentation, coloration, hyphal structures, and
 Wheat Smuts reproductive organs(G. Fischer & Dott, 2002; Lücking et al.,
Wheat, a vital cereal crop grown on 215 million 2020). For smut fungi, the teliospore is often the most
hectares worldwide, is highly susceptible to smut fungi such diagnostic structure, and taxonomists have long depended on
as: microscopic observations to differentiate species.

 Tilletia indica: Causes Karnal bunt.  Advantages:

 Tilletia tritici and T. laevis: Cause loose smut and
stinking bunt, respectively.  Simplicity and Cost-Effectiveness: Morphological
analyses require only basic tools, such as a compound
Although Karnal bunt causes yield losses of only 0.5%, microscope and simple staining techniques. This makes
its economic impact is disproportionate due to quarantine them accessible and relatively inexpensive, which is
regulations in Europe and the US (Turgay et al., 2020). In important for laboratories with limited resources.
Germany, estimated financial losses due to Karnal bunt  Direct Examination of Material: The immediate
exceed €5 million, highlighting the trade-related observation of infected plant material and fungal
consequences of smut diseases. structures in situ provides a direct link between the
pathogen and the symptoms it causes, aiding in initial
 Rice Smuts diagnoses.
Rice (Oryza sativa), a staple food for over half the
world's population, is vulnerable to:  Limitations:

 Rice False Smut (Ustilaginoidea virens): Yield losses  Phenotypic Plasticity: Morphological traits can vary
exceed 75% in heavily affected regions. significantly depending on environmental conditions, host
 Rice Karnal Smut (Tilletia horrida): Incidence rates reach species, and the developmental stage of the fungus. Such
100% in China and 87% in Pakistan(Bishnoi et al., 2020). phenotypic plasticity often leads to misidentification and
confusion, especially when distinguishing closely related
 Corn Smut species.
Corn smut, caused by Ustilago maydis, infects maize  Subjectivity: Interpreting morphological characteristics
(Zea mays), leading to tumor-like galls on kernels and stems. can be subjective, relying heavily on the expertise and
Despite its destructive potential, corn smut has gained experience of the mycologist. Minor differences in spore
economic significance as a culinary delicacy known as dimensions or hyphal structures can be overlooked or
"huitlacoche" in Mexico. misread.

 Sugarcane Smut Despite these limitations, morphological analysis

Sugarcane (Saccharum officinarum), a major cash crop, remains a foundational technique and continues to be
suffers devastating yield losses from sugarcane smut caused valuable for preliminary identification and for guiding
by Ustilago scitaminea (syn. Sporisorium scitamineum). subsequent, more definitive methods.

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Volume 9, Issue 12, December – 2024 International Journal of Innovative Science and Research Technology
ISSN No:-2456-2165 https://doi.org/10.5281/zenodo.14608940
 Cultural Techniques  Requirement for Specialized Assays: Biochemical tests
Cultural techniques involve isolating the fungus from may demand specialized reagents, equipment, and
infected tissues and growing it on artificial media. By doing expertise, adding complexity and cost to the identification
this, researchers can observe colony morphology, growth process.
rates, pigmentation, and other cultural characteristics under
controlled conditions(Afifah & Saputro, 2020; Humber, As with cultural methods, biochemical tests are often
2012; Mendoza-martínez et al., 2020; Singh & Sharma, 2020; integrated with other techniques to strengthen the accuracy of
Uikey et al., 2020). species identification.

 Advantages:  Pathosystem Studies

Pathosystem studies focus on the interaction between
 Isolation and Maintenance of Pure Cultures: Culturing the the fungus and its host plant. Observing disease symptoms,
fungus allows the development of stable reference strains, host specificity, and infection processes provides a deeper
essential for further studies, including genetic analyses ecological and evolutionary context(Hu et al., 2022;
and pathogenicity tests. Mapuranga et al., 2022; Nirmalkar et al., 2020; Sharma,
 Characterization of Growth Traits: Colony characteristics, 2021; Vorob’eva & Toropova, 2020).
such as texture, growth rate, and color, can provide
supplementary clues for identification.  Advantages:

 Limitations:  Ecological and Biological Relevance: Studying the host-

pathogen dynamics reveals information about virulence
 Obligate Biotrophy: Many smut fungi are obligate factors, infection strategies, and life cycle stages, which
biotrophs, meaning they rely on a living host for nutrition can complement morphological and molecular data.
and may not grow readily on artificial media. This makes  Confirming Pathogenic Identity: When smut fungi are
culturing challenging or impossible for certain species. identified based on their pathogenicity and host range, it
 Overlapping Morphologies: Even if a fungus grows in can help differentiate them from non-pathogenic,
culture, variations in nutrient media and conditions can morphologically similar fungi.
lead to phenotypic changes that are not reliable for
accurate species-level identification.  Limitations:

Cultural techniques, while useful, are often employed as  Time-Consuming: Such studies are often protracted, as
a complement to morphological and molecular methods, the fungus must be inoculated onto host plants, and the
rather than serving as a standalone identification tool. development of disease symptoms may take weeks or
months.
 Biochemical Tests  Controlled Conditions Required: Maintaining appropriate
Biochemical profiling involves assessing enzyme environmental conditions and selecting suitable host
activities, metabolic products, and other physiological traits plants can be challenging, limiting the practical feasibility
that can help differentiate species. Some smut fungi may of using pathosystem studies as a routine identification
exhibit distinct enzyme activity patterns or utilize certain technique.
substrates more efficiently, providing a biochemical
“fingerprint” for identification(Jaswal et al., 2020; Pathosystem studies are invaluable for understanding
Schirawski et al., 2021; Steins et al., 2023; Uikey et al., 2020; the biology and ecology of smut fungi but are not typically
Xia et al., 2020). the first line of identification due to the logistical challenges
involved.
 Advantages:
B. Molecular Techniques
 Additional Data Layer: Biochemical tests add another With the advent of molecular biology, more precise,
dimension to classification, helping distinguish species reliable, and rapid identification methods have emerged.
that appear morphologically similar. Molecular techniques target DNA or RNA sequences,
 Metabolic Insights: Understanding the metabolic providing stable, heritable markers that are less influenced by
capabilities of a fungus can shed light on its ecological environmental factors and phenotypic plasticity(Haddrill,
role and host interactions. 2021; Hasnain & Mehvish, 2020; Kartavtsev, 2021; Kasper
et al., 2020; Kumawat et al., 2021; Yali, 2022).
 Limitations:
 DNA Barcoding and Sequencing
 Overlap of Biochemical Traits: Many smut fungi share DNA barcoding involves using standardized genomic
similar biochemical characteristics, limiting the regions as universal identifiers. In fungi, the Internal
discriminatory power of such tests. Two or more closely Transcribed Spacer (ITS) region of the ribosomal RNA gene
related species may exhibit nearly identical enzyme cluster has become the primary barcode due to its high level
activity profiles. of interspecific variability and ease of
amplification(Santamaria, 2011; Seifert, 2009).

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ISSN No:-2456-2165 https://doi.org/10.5281/zenodo.14608940
 Advantages: Such analyses have redefined fungal systematics, often
leading to the discovery of cryptic species complexes and the
 High Accuracy and Reliability: ITS sequences allow for rearrangement of genera and families, thereby providing a
the differentiation of closely related species, including more robust taxonomic framework.
cryptic species that appear identical morphologically.
 Global Standardization: Due to the widespread use of ITS  Next-Generation Sequencing (NGS) and Genomic
as a fungal barcode, large reference databases (e.g., Approaches
GenBank, UNITE) facilitate rapid species identification. The rapid advancement of sequencing technologies has
ushered in a new era of fungal identification. Next-
Example Applications: Studies have employed ITS Generation Sequencing (NGS) techniques allow for whole-
sequencing to resolve taxonomic ambiguities among smut genome sequencing and metagenomic analyses that can
fungi. For example, Seifert, 2009 and Fischer & Hirschhorn, characterize complex fungal communities, including those
2018 demonstrated how ITS sequencing has clarified containing unculturable or rare species(Ahrendt et al., 2018;
relationships within the Ustilaginaceae, revealing new Araujo & Sampaio-Maia, 2018; James et al., 2020; Nalage et
lineages and correcting previous misclassifications. Such al., 2024; Patil et al., 2023b, 2023a; Sangal et al., 2014;
work underscores the power of DNA barcoding to refine Sontakke et al., 2023).
fungal taxonomy and improve the accuracy of
identification(Tiknaik et al., 2019).  Advantages:

 PCR-Based Methods  High-Throughput Identification: NGS can process

Polymerase Chain Reaction (PCR) techniques enable thousands of samples simultaneously, making it ideal for
the amplification of specific DNA fragments from minute large-scale biodiversity surveys and environmental
amounts of fungal tissue(Eberhardt, 2012; Hosoya et al., monitoring.
2012). By designing taxon-specific primers that target unique  Comprehensive Genomic Insights: Whole-genome
genomic regions, PCR-based methods can rapidly confirm a sequencing unveils genes involved in pathogenicity, host
fungus’s identity. specificity, and other functional traits, thereby deepening
our understanding of smut fungi biology.
 Advantages:  Metagenomics: By analyzing environmental DNA
(eDNA) samples, NGS can detect smut fungi that are not
 Rapid and Sensitive: PCR can detect and amplify fungal easily cultured or observed, broadening the known
DNA even from very small samples, including those diversity of these pathogens(Nalage et al., 2023; Sontakke
obtained from infected plant tissue or environmental et al., 2022).
samples.
 Direct Application to Field Samples: Samples collected in NGS-based techniques are still relatively costly and
the field can be processed without the need for culturing, require bioinformatics expertise. However, as these
accelerating the identification process. technologies become more accessible and affordable, they
will likely become a standard tool for smut fungal
PCR techniques are often combined with DNA identification and research.
sequencing for definitive species identification, making them
a critical component of modern diagnostic and taxonomic IX. INTEGRATING MULTIPLE APPROACHES
workflows(Balajee et al., 2009; Erlich et al., 1991).
Each identification technique has its strengths and
 Phylogenetic Analysis weaknesses. A robust identification strategy often integrates
Beyond just identifying species, molecular data enable multiple approaches, leveraging the simplicity and cost-
researchers to reconstruct phylogenetic trees that illustrate effectiveness of morphological or cultural techniques with
evolutionary relationships. By comparing gene sequences the precision and reliability of molecular methods(Nalage et
(e.g., ITS, LSU, EF1-α) across multiple taxa, mycologists can al., 2024). For example, a field researcher might initially rely
discern patterns of divergence, speciation, and host on morphological characteristics and disease symptoms to
adaptation(Castelle & Banfield, 2018; Fitzpatrick et al., identify a suspected smut fungus. Subsequently, DNA
2006; McCarthy & Fitzpatrick, 2017; Rahayu et al., 2021). barcoding and PCR-based tests can confirm the
identification, while phylogenetic analyses and NGS data can
 Advantages: provide deeper evolutionary and ecological insights.

 Evolutionary Insights: Phylogenetic analyses help This integrative strategy ensures that identifications are
interpret how smut fungi have evolved, migrated, and both accurate and informative, supporting effective disease
adapted to different hosts or environmental conditions. management plans in agriculture and contributing to a more
 Refinement of Taxonomy: When morphological traits complete understanding of smut fungal diversity and
conflict with traditional taxonomy, molecular phylogenies evolution.
can guide the reclassification of species into more
accurate lineages.

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Volume 9, Issue 12, December – 2024 International Journal of Innovative Science and Research Technology
ISSN No:-2456-2165 https://doi.org/10.5281/zenodo.14608940
X. GAPS IN RESEARCH AND  Global Research Collaboration:
FUTURE PERSPECTIVES
 Addressing these gaps requires international cooperation,
Despite significant advancements in fungal taxonomy data sharing, and joint research initiatives.
and molecular identification techniques, several gaps persist  Platforms such as global fungal databases and research
in smut fungi research. Addressing these challenges requires networks can facilitate collaboration among scientists
global collaboration, interdisciplinary approaches, and worldwide.
innovative technologies:
XI. CONCLUSION
 Unexplored Biodiversity:
Smut fungi, as obligate plant pathogens, hold significant
 While smut fungi diversity has been well-studied in ecological, economic, and scientific importance. While they
certain regions, large portions of the world, particularly pose substantial threats to global agriculture by reducing crop
tropical and subtropical zones, remain underexplored. yields and quality, they also offer opportunities to advance
 Countries with high biodiversity, such as those in Africa, scientific knowledge and biotechnological applications.
Southeast Asia, and South America, lack comprehensive Despite notable progress in fungal taxonomy and molecular
surveys of smut fungi. identification, large gaps remain in understanding their
biodiversity, pathogenic mechanisms, and environmental
 Taxonomic Ambiguity: impacts.The need for interdisciplinary research and global
collaboration cannot be overstated. By combining traditional
 Morphologically similar species and cryptic species methods with modern molecular techniques, researchers can
complexes pose challenges to accurate identification. unlock the full potential of smut fungi studies. Addressing
 Integrating molecular phylogenetics with traditional these gaps will not only enhance disease management
taxonomy can resolve ambiguities and refine fungal strategies but also contribute to broader ecological and
classification. evolutionary research.As climate change and emerging
agricultural challenges continue to shape the future,
 Host-Pathogen Interaction Mechanisms: comprehensive research on smut fungi will be essential for
ensuring food security, protecting biodiversity, and fostering
 Limited understanding of the molecular mechanisms sustainable agricultural practices.The identification of smut
governing host specificity, effector proteins, and fungal fungi has evolved from a reliance on traditional, morphology-
adaptation to host plants. based methods to a more holistic approach that incorporates
 Research into fungal effectors and their role in host molecular and genomic techniques. Although conventional
immune suppression is critical for developing targeted methods remain valuable for initial screenings and certain
control strategies. diagnostic contexts, DNA barcoding, PCR-based techniques,
phylogenetic analyses, and next-generation sequencing have
 Impact of Climate Change: revolutionized fungal taxonomy, delivering higher resolution,
greater accuracy, and deeper insights into the biology and
 Climate change is altering fungal distribution and diversity of these pathogens.As these advanced techniques
pathogenicity, yet little research has been conducted on become more accessible and user-friendly, the field of smut
how these changes impact smut fungi. fungal identification will continue to progress, facilitating
 Predictive models and field studies are needed to assess more effective disease management strategies, guiding
future risks to global agriculture. quarantine measures, and enhancing our overall
understanding of fungal biodiversity and evolution. In this
 Biotechnological Applications: dynamic landscape, the integration of multiple identification
techniques is key, ensuring that taxonomic conclusions are
 Smut fungi, particularly Ustilago maydis, have shown well-grounded and that the resulting knowledge can be
applied for the benefit of agricultural sustainability,
potential in industrial applications such as bioconversion
biosecurity, and fundamental mycological research.
and bioremediation.
 Further research can unlock their utility in sustainable
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