Distribution of mycotoxin-producing fungi across major rice production areas of China
Introduction
China is the world's largest producer and consumer of rice (Oryza sativa L.). In 2019, China produced more rice annually than any other country, accounting for 28% of global rice production according to the Food and Agriculture Organization (FAO, http://www.fao.org/faostat/zh/#data/QCL). Rice is the world’s third largest cereal crop in terms of both production and planting area, and over 65% of the Chinese population consumes rice as a staple food (Sun et al., 2017). The safety of rice and rice products is essential for food security and human health. However, rice is easily contaminated by toxigenic fungi that may resulted in fungal secondary metabolite accumulation (Fokunang et al., 2006). In particular, mycotoxins produced by toxigenic fungi carry significant health risks and cause toxic carcinogenic, mutagenic teratogenic, and estrogenic effects (Arenas-Huertero et al., 2019; Fokunang et al., 2006).
Rice grains have evolved with diverse fungal communities during seed development, maturation, and harvest periods, including some harmful toxigenic fungi (Nelson, 2004). The composition and distribution of grain-associated fungi can affect mycotoxin production, thereby resulting in food safety issues (Mannaa & Kim, 2017; Ok et al., 2014; Tralamazza et al., 2016). According to FAO estimates, more than 25% of global food crops are contaminated by mycotoxins (Eskola et al., 2020). The major mycotoxin contaminants in rice grain are aflatoxins (AFTs), ochratoxins, citrinin, and deoxynivalenol (DON), which are primarily produced by Aspergillus species, Penicillium species, and Fusarium species, respectively (Frisvad et al., 2019; Ok et al., 2014; Reddy et al., 2008; Zhao et al., 2019). Among these, the AFTs produced by Aspergillus species are the most harmful and carcinogenic toxins found in rice grains and can provoke tumor formation or even rapid death (Ding et al., 2015; Massey et al., 1995). In recent years, the AFT contamination of rice grains and rice products has become an alarming global problem (Ferre, 2016; Zhao et al., 2019).
The structures and distributions of microbial communities are strongly associated with the climate conditions of different geographic locations (Edwards, 2017; Edwards et al., 2015). The large latitude span of the northern and southern regions of China formed different temperate zones and the climate conditions of different temperate zones vary greatly (Li et al., 2014). The substantial climatic differences and different geographic locations could result in varied compositions and distributions of toxigenic fungi. In the northeastern region, the suitable climate conditions, soil properties, and sufficient sunlight make it the best rice-producing area of China. While, in the southern region, the high temperatures and humidity during rice-growing seasons lead to favorable growth conditions for toxigenic fungi (Sun et al., 2017). For example, A. flavus and other fungal species favor high temperatures and high relative humidity conditions in tropical and subtropical regions (Giorni et al., 2009). The production of mycotoxins is strongly associated with the prevalence of toxigenic fungi, environmental factors, and the interaction networks between different fungal species (Ding et al., 2015). For example, A. flavus can significantly reduce the toxin production capacity of Fusarium graminearum and F. verticillioides (Giorni et al., 2019). Hence, a better understanding of the relationships between fungal communities and the presence of mycotoxins may provide an important guideline for the precise prevention of mycotoxins in rice grains.
Achieving food self-sufficiency is important for the food security of China, which, however, is a challenge due to the contamination of mycotoxins and lack of farmland. Revealing the diversity, composition, distribution of rice grain-associated fungal communities will could help to provide an in-depth understanding the relationships between toxigenic fungi and mycotoxins, which could reduce the potential toxigenic fungi caused rice spoilage (Sun et al., 2017). Previous studies related to rice mainly focused on the bacterial community and the rhizosphere microbiota of rice (Edwards et al., 2015; Zhou et al., 2020a). Despite the importance of rice grain-associated contamination of mycotoxins, the structure and distribution of rice fungal communities in relation to grain-associated mycotoxins were rarely reported. Understanding the compositions and distributions of toxigenic fungi can provide basic information for the precise prevention of mycotoxin contamination, which is essential for guaranteeing food security of China and all other countries. In this study, we collected rice grain samples from the major rice-producing provinces of China, which encompass more than 50% of the total rice production in China. The objectives of this study were to: 1) characterize the fungal communities of rice grains across different geographic locations in China using high-throughput sequencing (HTS); 2) determine the environmental factors that shape the structure of these fungal communities and evaluate the relationships between fungal communities and mycotoxin contamination; 3) identify areas with high possibility of toxigenic fungi and contamination of mycotoxins among major rice producing areas of China.
Section snippets
Grain samples
A large-scale survey of rice grain (rough rice with shells) fungal communities was conducted in 2019. A total of 90 rice grain samples collected from 27 different locations were surveyed across 10 major rice-producing provinces in the southwestern, southeastern, and northeastern regions of China (Fig. 1A). Detailed information regarding the geographic location for each rice sample is shown in Table S1. About 1.0 kg of new harvest rice grain was collected for each sample from the grain depot at
Rice fungal community diversity
After quality control of the ITS DNA sequences and chimera removal, a total of 6,477,244 fungal ITS sequences were obtained from 90 rice grain samples. The clean sequences were then clustered into ASVs after the removal of non-fungal sequences (e.g., chloroplast and mitochondria) and those ASVs with <10 sequences. The remaining ASVs comprised 90.48% of the total sequences and 2136 ASVs representing an average of 69,181 sequences per sample (range: 65,115–71,114). Rarefaction curve analysis
Discussion
Geographic location is an important factor that influences the composition and structures of rice-associated bacterial communities (Zhou et al., 2020a). In this study, rice grains fungal communities were characterized over a relatively large sampling scale comprising the major rice production areas of China for the first time. The fungal communities could be separated into three distinct groups representing the NE, SE, and SW regions of China. Compared with the SE (29 specific ASVs) and SW (20
Conclusions
This study is the first to report the relationship between the fungal communities of rice grains and AFT concentrations, using HTS data to evaluate rice-associated fungal community composition in major rice-producing areas of China. The most important environmental factors affecting rice grains fungal communities were WMT, MAP, and HMW. The main potentially toxigenic fungal taxa that could produce AFTs within the surveyed Chinese rice grains were A. flavus and A. parasiticus. Northeastern
CRediT authorship contribution statement
Zhihui Qi: performed the experimental work and wrote the paper. Xin Zhou: Formal analysis, specifically Visualization/ data presentation, and wrote part of the paper. Lin Tian: Formal analysis. Haiyang Zhang: collected all samples used during the paper and helped with all the experimental work. Lei Cai: revised and edited the paper and supervised the experimental work. Fang Tang: formulated the overarching research goals and revised the paper.
Declaration of competing interest
We declare that we have no financial and personal relationships with other people or organizations that can inappropriately influence our work, there is no professional or other personal interest of any nature or kind in any product, service and/or company that could be construed as influencing the position presented in, or the review of, the manuscript entitled, “Distribution and characteristics of mycotoxin-producing fungal taxa across major rice production areas of China”.
Acknowledgments
This work was financially supported by the National Key R & D Program of China (2016YFD0401003-2) and the Biological Resources Programme, Chinese Academy of Sciences (KFJ-BRP-009).
References (52)
- et al.
Structure and function of the bacterial root microbiota in wild and domesticated barley
Cell Host & Microbe
(2015) Worldwide occurrence of mycotoxins in rice
Food Control
(2016)- et al.
Diversity of the endophytic fungi associated with the ancient and narrowly endemic neotropical plant Vellozia gigantea from the endangered Brazilian rupestrian grasslands
Biochemical Systematics and Ecology
(2017) Integrated management of the risks of stored grain spoilage by seedborne fungi and contamination by storage mould mycotoxins – an update
Journal of Stored Products Research
(2017)- et al.
Taxonomy of Aspergillus section Flavi and their production of aflatoxins, ochratoxins and other mycotoxins
Studies in Mycology
(2019) - et al.
Environmental factors modify carbon nutritional patterns and niche overlap between Aspergillus flavus and Fusarium verticillioides strains from maize
International Journal of Food Microbiology
(2009) - et al.
Occurrence of four mycotoxins in cereal and oil products in Yangtze Delta region of China and their food safety risks
Food Control
(2014) - et al.
Mycobiota and natural occurrence of aflatoxin, deoxynivalenol, nivalenol and zearalenone in rice freshly harvested in South Korea
Food Control
(2014) - et al.
Potential of botanicals and biocontrol agents on growth and aflatoxin production by Aspergillus flavus infecting rice grains
Food Control
(2009) - et al.
Fungal diversity and natural occurrence of deoxynivalenol and zearalenone in freshly harvested wheat grains from Brazil
Food Chemistry
(2016)
Mycotoxin contamination and presence of mycobiota in rice sold for human consumption in China
Food Control
Involvement of ahr pathway in toxicity of aflatoxins and other mycotoxins
Frontiers in Microbiology
Extreme rainfall affects assembly of the root-associated fungal community
New Phytologist
Cochliobolus phylogenetics and the origin of known, highly virulent pathogens, inferred from ITS and glyceraldehyde-3-phosphate dehydrogenase gene sequences
Mycologia
Improved selection of internal transcribed spacer-specific primers enables quantitative, ultra-high-throughput profiling of fungal communities
Applied and Environmental Microbiology
Microbial biogeography of wine grapes is conditioned by cultivar, vintage, and climate
Proceedings of the National Academy of Sciences
Plant compartment and biogeography affect microbiome composition in cultivated and native Agave species
New Phytologist
Variation in fungal microbiome (mycobiome) and aflatoxin in stored in-shell peanuts at four different areas of China
Frontiers in Microbiology
Influence of climatic factors on fusarium species pathogenic to cereals
European Journal of Plant Pathology
Muscle: Multiple sequence alignment with high accuracy and high throughput
Nucleic Acids Research
Uparse: Highly accurate OTU sequences from microbial amplicon reads
Nature Methods
Impact of agronomic and climatic factors on the mycotoxin content of harvested oats in the United Kingdom
Food Additives & Contaminants Part A Chem Anal Control Expo Risk Assess
Structure, variation, and assembly of the root-associated microbiomes of rice
Proceedings of the National Academy of Sciences
Challenges facing the biological control strategy for eliminating aflatoxin contamination
World Mycotoxin Journal
Worldwide contamination of food-crops with mycotoxins: Validity of the widely cited 'FAO estimate' of 25
Critical Reviews in Food Science and Nutrition
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Zhihui Qi and Xin Zhou contributed equally to this work.