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Perspective

How Maize Seed Systems Can Contribute to the Control of Mycotoxigenic Fungal Infection: A Perspective

by
P. Christiaan Biemond
1,2,
Tjeerd Jan Stomph
2,
P. Lava Kumar
3 and
Paul C. Struik
2,*
1
International Institute of Tropical Agriculture (IITA), IITA-Kano, PMB 3112, Sabo Bakin Zuwo Road, Kano 713103, Nigeria
2
Centre for Crop Systems Analysis, Plant Sciences Group, Wageningen University, P.O. Box 430, Bornsesteeg 48, 6708 PE Wageningen, The Netherlands
3
International Institute of Tropical Agriculture (IITA), PMB 5320, Oyo Road, Ibadan 200001, Nigeria
*
Author to whom correspondence should be addressed.
Agronomy 2021, 11(11), 2168; https://doi.org/10.3390/agronomy11112168
Submission received: 30 August 2021 / Revised: 22 October 2021 / Accepted: 25 October 2021 / Published: 28 October 2021
(This article belongs to the Special Issue Fungal Disease Management and Mycotoxin Prevention in Cereals)
Browse Figure
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Abstract

:
Mycotoxins are toxic secondary metabolites produced by fungi on agricultural produce. Mycotoxins can be cytotoxic, genotoxic, mutagenic, and teratogenic, and they are persistent threats to human and animal health. Consumption of mycotoxin-contaminated maize can cause cancer and even sudden death. Health hazards can also occur from consuming products from animals fed with mycotoxin-contaminated feed or forage. The main mode of spread of mycotoxigenic fungi is through air-borne spores originating from soil or plant debris, although some fungi can also spread through infected seed-to-seedling transmission, ultimately followed by contamination of the harvestable product. This perspective assesses opportunities to prevent mycotoxigenic fungal infection in maize seeds produced for sowing as an important starting point of crop contamination. A case study of Nigeria showed infection in all tested farmer-produced, seed company, and foundation seed samples. A schematic overview of the formal and informal seed systems is presented to analyze their contribution to fungal infection and mycotoxin contamination in the maize value chain, as well as to set criteria for successful control. We recommend an integrated approach to control mycotoxigenic fungal infection, including resistant varieties and other control methods during seed production, grain production, and grain storage, with an important role in maintaining seed health.

1. Introduction

1.1. Background

Mycotoxins are secondary metabolites produced by certain types of fungi, such as Alternaria, Aspergillus, Fusarium, and Penicillium spp., on agricultural produce, such as maize (Zea mays L.). Mycotoxins enter the food chain as results of preharvest and postharvest fungal infection. These mycotoxins are an important health hazard in developing countries, such as those in sub-Saharan Africa, which is receiving little but growing attention [1,2,3,4,5].
Most hazardous mycotoxins in human foods or animal feeds in sub-Saharan Africa include aflatoxins, ochratoxins, fumonisins, deoxynivalenol, and zearalenone [2,4]. These mycotoxins are very stable and, therefore, can remain present during crop production and harvest, during transport and storage, and even during processing and postprocessing events [2]. They also accumulate in animal products from animals fed with contaminated feed or forage [5].
Chronic exposure to mycotoxin-contaminated maize can cause cancer, while acute exposure can lead to sudden death [6]. Mycotoxin exposure is most common in developing countries with poor food handling, inadequate food storage, malnutrition, and weak regulations to prevent entry of food and feed products with mycotoxins beyond permissible limits for consumption [7].
Given the negative impacts of these fungal toxins, the mycotoxins have a large impact on nutrition security and livelihood, as well as affect the competitiveness of agricultural production in sub-Saharan Africa [2]. Despite increasing awareness of the problem, in many cases, the contamination with mycotoxins still exceeds the maximum tolerable threshold levels and, thus, continues to threaten public health [2]. Possible solutions for this health hazard are capacity building and value chain management.
However, for control of mycotoxins, the value chain is complicated and should not be taken lightly. For example, Kamika et al. [8] described the occurrence of aflatoxin contamination in maize throughout the food supply chain in the Democratic Republic of Congo. They demonstrated that aflatoxins are ubiquitous; in the preharvest period, 16 out of 50 samples tested were positive for aflatoxins. However, as the supply chain progressed, the contamination with aflatoxins went up, both in frequency and in intensity, until 100% of the collected maize samples contained aflatoxins at levels that were 300 times higher than the maximum limit of 10 μg/kg set by the World Health Organization [8]. Maximum levels observed at the end of the supply chain (in shops and on markets) were as high as 500 times this maximum tolerable level.
However, similar hazards can occur by consuming animal products in which mycotoxins have accumulated. Gruber-Droninger et al. [4] collected 74,821 samples of feed or feed raw materials from 100 countries across the globe during a period from 2008 until 2017 and analyzed these samples for various mycotoxins. They demonstrated that 88% of the samples were contaminated with at least one mycotoxin and many samples exceeded the health standards. However, they also observed large differences among regions and significant year-to-year variation in occurrence of mycotoxins in animal feed. These differences were very much related to climatic and weather factors, especially rainfall and temperature during sensitive phases of feed and forage production.
These findings cry for a stricter control of mycotoxins, but also suggest that it is not easy under the changing global conditions to maintain control over mycotoxins (see also [9]). Marroquin-Cardona et al. [9] made a plea to balance global mycotoxin standards with what they called “a realistic feasibility of reaching them, considering limitations of producers”.
High-income countries control the mycotoxin hazard with a combination of regulation and certification (Figure 1A). The Food and Drug Administration (FDA) [10] and the European Commission [11,12] determined maximum food contamination levels for specific mycotoxins to protect consumers from mycotoxin exposure. Certifications, such as the Hazard Assessment and Critical Control Point (HACCP), assist companies in the food value chain to prevent mycotoxin contamination and keep it within acceptable levels [13]. However, certification and enforcing food regulations are not compatible with smallholder farming and local or regional value chains in low-income countries [4,5,8,9], such as countries in sub-Saharan Africa. Farmers consume part of their own produce without market interference, making food safety control difficult to execute [6], while locally sold and purchased grains are also not covered by such controls.
Moreover, in many countries of sub-Saharan Africa, there is a substantial amount of regulation and legislation on the control of mycotoxins but without effective enforcement and oversight [2]. There is also a limiting economic factor: food safety controls would increase food prices where the majority of the population already spends up to 50% of their income on food [14].
An important control strategy to avoid mycotoxin contamination is to prevent toxigenic fungal infection, including genetic and agronomic approaches [15]. If awareness of the hazards is present, knowledge on control measures is available, and proper incentives are in place to carry out the proper measures, then it is possible to reduce the problem. However, an often ignored part of the supply chain and an overlooked part of the “contamination chain” is the seed production preceding the production of the marketable food or feed. It has been reported that mycotoxin contamination can start as seed-to-seedling transmission from infected seeds, resulting in infected plants and infested produce [16]. If this is a significant route of contamination, then the seed system should be taken into account as part of the supply chain. This research, therefore, proposes a conceptual framework to assess contributions of formal and informal seed systems to the propagation of the contamination with mycotoxins. We also analyze how seed health can be controlled to avoid or reduce mycotoxigenic fungal infection in developing countries.
Data on current mycotoxin threats in maize value chains in sub-Saharan Africa are rare and rather unbalanced between countries. Important research groups have published relevant datasets for countries such as Benin [5], Cameroon [5], Congo [3,8], Kenya [17,18], Mali [5], Nigeria [1,5,19], and South Africa [20]. For other countries identified by FAO statistics as growing maize as a major staple or feed crop on a large scale, e.g., Mozambique, Tanzania, Uganda, and Zimbabwe, such datasets are not to be found. The fact that just a few countries are mentioned in the reviewed literature is a reflection of the activity of research groups and, therefore, available literature rather than an indication of the extent of the problem. There are no reasons to assume the problem is smaller in other countries in sub-Saharan Africa (see, e.g., [2,4,5]) or in other developing economies across the globe with comparable institutional settings. The latter is confirmed by research reports from Haiti [21,22], Iran [23], and China [24,25]. In Haiti, aflatoxins were present in 55% of the maize kernel samples [21], but the frequency of infection strongly depended on locality and, therefore, on farming system, storage system, and weather conditions [22]. In Iran, a large diversity of Fusarium species was observed on maize kernels, and this diversity increased the risk of multi-toxin contamination, thus enhancing the risk of health hazards for humans and animals [23]. In China, a great diversity of Fusarium species was also found in maize kernels; however, this diversity depended on the region of origin of the samples [24]. In China, co-occurrence of various mycotoxins occurred in 60% of the maize kernel samples [25], thus increasing health risks. However, in high-income countries, issues with mycotoxins might also arise, e.g., in Belgium [26], Germany [27], and Spain [28]. In Belgium, it was observed that every maize silage, used for winter feed of dairy cattle, was contaminated with at least two different mycotoxins [26]. In Germany, researchers proved that infection of the maize crop could occur throughout the growing season, causing various types of diseases in vegetative and reproductive organs; Fusarium ear rot was particularly important for the toxigenic quality of ear-based maize products [27]. Lastly, in Spain, it was demonstrated that Fusarium could be transmitted through seed in very diverse agricultural and horticultural crops, including ornamentals [28].
In this paper, a case study from northern Nigeria is used to illustrate the infection levels of locally available maize seed as important risk factors in the “contamination chain”. A schematic overview of the seed system is presented to analyze the problem of mycotoxigenic fungal infection of seed. Potential control methods are discussed in relation to sustainable implementation in the formal and informal seed systems.

1.2. Mycotoxins

Mycotoxins are defined as natural products with low molecular weight, produced as secondary metabolites by filamentous fungi. They are toxic to vertebrates in low concentrations and differ widely in biosynthetic origin, chemical structure, and toxicity [7,17,18,20,26,29,30]. The symptoms of mycotoxin poisoning depend on the type and amount of mycotoxin, duration of exposure, and the age, sex, health, and nutritional status of the victim [7,18]. An example of fatal mycotoxin poisoning was the aflatoxicosis outbreak in Kenya in 2004. Over 300 people got acute hepatic failure after consumption of aflatoxin-contaminated maize, which eventually killed 125 people [31]. However, the literature not only reports on contaminated food, but also puts emphasis on the contamination of animal feed with mycotoxins and the subsequent contamination of animal products [17,20,29].
The most prevalent fungi that can produce mycotoxins belong to the genera Alternaria, Aspergillus, Fusarium, and Penicillium. Control measures differ in effectiveness between genera. Avoiding grain damage during harvest, fast drying to low moisture levels, and adequate storage methods can be effective against Alternaria and Aspergillus species. These “storage fungi” produce mycotoxins primarily during storage, in contrast to Fusarium and Penicillium species which produce mycotoxins mostly under field conditions [32].
Optimal storage conditions do not solve the problem of preharvest mycotoxin production; anyway, they are difficult to implement for developing countries. Agronomic practices such as crop rotation, tillage, irrigation, and fertilizer application do not provide sufficient protection either, and available varieties do not have sufficient levels of resistance against all mycotoxigenic organisms. Mycotoxigenic fungal infection in maize is a persistent problem in developing countries [15]. Especially Fusarium verticillioides (Sacc.) Nirenberg is problematic. This fungus is a seed-borne species in maize and results in systemic infection in the plant. Neither seed treatments with fungicides nor chemical control in the field are suitable control measures under the conditions of smallholder farmers, for example because these farmers may not have access to these chemical crop protectants or cannot afford such treatments, or because they may not have enough yield incentives to warrant the application of such treatments, while not being awarded for keeping their produce mycotoxin-free. Biological control strategies are developed involving pre- or postharvest applications of biocontrol agents [16]. Such strategies could involve biopriming of the seeds with Trichoderma harzianum Rifai [33,34,35], T. gamsii Samuels & Druzhin. [36], or Pseudomonas fulva Iizuka & Komagata [37].
As it is unlikely that resource-poor farmers will pay for an extra treatment without benefits such as higher yield or increased market price for mycotoxin-free maize [3], biocontrol should always have multiple effects. Seed health is not only an important aspect in the control of F. verticillioides, but can also contribute to the control of other seed-borne, mycotoxigenic fungi, e.g., Fusarium oxysporum Schlecht. emend. Snyder & Hansen, Fusarium solani (Mart.) Sacc., and Penicillium oxalicum Currie, J.N.; Thom, C. [38].

1.3. Informal and Formal Seed Systems

Seed health, i.e., the absence of any pathogens causing seed deterioration or plant diseases after germination, can only be controlled through the source of seed, i.e., the seed system [39]. A seed system can be defined as all activities related to seed production, seed storage, seed management, seed dissemination, and seed use. A sustainable seed system can ensure that high-quality seeds of a wide range of varieties and crops are produced and fully available in time and affordable to farmers and other stakeholders. In the literature, a distinction is made between “formal seed systems” and “informal seed systems”. The latter are also called “local seed systems”, “farmers’ seed systems”, or “traditional seed systems”.
The formal seed system consists of government bodies, NGOs, and private companies involved in breeding, seed multiplication, external quality control, and dissemination of seed (Figure 1B) [40]. Seed certification is an essential part of the formal seed system. Government bodies and NGOs run public breeding programs, while some seed companies also develop new varieties. Responsible authorities test varieties for Distinctness, Uniformity, and Stability (DUS) criteria for varietal registration. The new varieties are multiplied, tested for seed quality, certified, and sold to farmers.
The informal seed system consists of farmers, usually smallholder farmers, producing seed for their own use, and often selling or exchanging seed within their local community, including neighbors, friends, families, or even local markets [40,41,42,43,44]. There is no formal oversight in informal seed systems. Informal seed systems are often more flexible and diverse, accepting or even creating more genetic diversity (such as mixtures, landraces). Nevertheless, in general, farmers try to maintain some level of purity and seed quality, but they are not able to test it. Excess seed is used for own consumption or sold as grain on the market. Therefore, seed and grain (or seed and ware) often cannot be clearly distinguished.
Both seed systems interact. The informal seed system depends on the formal seed system to access new varieties and for occasional seed renewal, while the formal seed system uses the informal seed system for farmer participatory breeding, sourcing additional genetic diversity, varietal testing, or seed multiplication [42,43,44]. Farmers involved in grain production can buy seed from the formal seed system for a relatively high price, purchase seed locally from the informal seed system for a relatively low price [44], or recycle seed for several years, before replenishing from other sources.
Using locally produced seed or recycling one’s own seed can result in a buildup of mycotoxigenic fungi in the seed, provided such fungi are present in the fields in the area. Seed treatment of local or recycled seed can improve seed health and, therefore, mitigate the contamination with mycotoxins, but will only be implemented if it coincides with other incentives, such as higher yields or better quality of food, feed, or animal products, as already indicated above.

2. Maize Seed Health in Nigeria

2.1. Maize Seed Systems

Since the informal seed system lacks access to required infrastructure, seed-producing farmers do not test seed health, despite being very aware of the risks of seed-borne diseases [3]. Recent research results from Nigeria showed that farmer-produced seed samples were heavily infected with a range of mycotoxigenic fungi [45]. All samples were infected with Fusarium verticillioides with a median infection incidence of 55.2% (Table 1). The fungus can produce fumonisins that are classified as potentially carcinogenic to humans causing esophageal cancer. Avoiding fumonisin contamination may prevent 1,000,000 HIV transmissions in sub-Saharan Africa annually [46]. The most frequently occurring Aspergillus fungus was Aspergillus niger van Tieghem, occurring in 61% of the samples, which can produce the mycotoxins ochratoxin A (OTA) and fumonisin B2 [47]. Ochratoxin A is classified as possible human carcinogen and shows immunotoxic properties [48]. Penicillium oxalicum was identified in 29% of farmer-produced seed samples. The fungus can produce the mycotoxin secalonic acid D [49], which dramatically increases the chance of cleft palate, a common birth defect [50]. Soil-borne Aspergillus flavus Link, producing aflatoxins, occurred in 38% of the farmer-produced seed samples. Chronic aflatoxin exposure can lead to stunted growth of children, liver cancer among adults, and reduced life expectance, while acute aflatoxicosis can be lethal within weeks [6]. The seed company and foundation seed samples were also heavily infected with various mycotoxigenic fungi (Table 1) [45]. The fact that mycotoxigenic fungi appear in seed company samples raises the question whether seed treatment should be made mandatory to control seed-borne mycotoxigenic fungi.
It should be noted that control of mycotoxigenic fungi does not stand alone. Chalivendra et al. [51] demonstrated that there is a strong interaction with insect damage. Lowering mycotoxin levels might actually increase insect damage. This stresses the need for integral pest and disease management strategies in seed systems and complicates breeding for resistance against mycotoxigenic fungi and subsequent variety selection. On the other hand, breeding for increased levels of phlobaphenes in the seed could be a powerful strategy to improve grain quality by reducing mycotoxin accumulation [52]. Breeding for such varieties might limit the spread of seed-borne mycotoxigenic fungi through seed systems in the “mycotoxin chain”. Lastly, Gao et al. [53] reported on opportunities to make use of antagonistic mechanisms against Fusarium verticillioides enhancing seed health by stimulating the endophyte Sarocladium zeae (W. Gams & D.R. Sumner) Summerbell.
The results of maize seed were compared with maize grain meant for consumption. Several studies collected maize samples from local markets in African countries and analyzed fungal infection. The dominance of F. verticillioides infection in Nigerian maize was confirmed in these reports [56]. Evidence from southwest Nigeria showed a maize grain infection frequency of 89.3% and an infection incidence of 49.4% for F. verticillioides, while infection incidences of other identified fungi varied from 1.3–14.7% [57]. The seed samples of the current research showed similar results with high infection frequency (100% of farmer produced seed) and incidence (55.2%) for F. verticillioides, in combination with low infection incidences for all other identified fungi. The list of identified fungi differed between southwest and northern Nigeria [45], probably due to environmental differences. Maize grain samples in South Africa showed similar infection levels of F. verticillioides (identified in 87.5% of the samples), A. flavus (42.5%), A. niger (25.0%), and P. oxalicum (27.5%) [58]. It appears that seeds have similar infection levels compared with maize grain meant for human consumption.

2.2. Relevance of the Different Fungi

Although the seed samples were not tested for mycotoxins, it is highly unlikely that the identified fungi solely contain atoxigenic strains. Atoxigenic strains are not able to produce mycotoxins, in contrast with toxigenic strains. Results from Portuguese maize showed that 14% of the A. niger isolates could produce ochratoxin A and 39% fumonisin B [59], while a report of maize in Argentina showed that 25% of the A. niger strains were toxigenic [60]. A search for atoxigenic A. flavus strains in Kenya showed that only 33% of the analyzed isolates were atoxigenic, while the majority could produce aflatoxins [61]. An experiment in Kansas, USA, could not identify any atoxigenic strains of F. verticillioides, and isolates with relatively low fumonisin production in vitro did not show a consistently low level of fumonisin production in vivo [54]. All four cases have in common that atoxigenic strains were absent or accompanied by toxigenic strains, leaving the risk of mycotoxin production. Another aspect to judge the relevance of the identified fungi is their ability to transmit the fungus from seed to seedling, so-called seed-borne pathogens. Seed-borne infections are an important infection source for F. verticillioides [16]. The other two Fusarium species, A. niger and P. oxalicum, are also seed-borne diseases, but A. flavus is most likely only soil-borne or occurs as a surface contaminant [38].

3. Control

3.1. Control Methods

The case study of maize seed in Nigeria showed that both formal and informal seed systems struggle with mycotoxigenic fungal infection, but there are several control methods that can reduce infection. Important control methods of the formal seed system are integrated approaches, including postharvest processing and storage methods, seed health testing to test and avoid heavily contaminated stocks and prevention through resistant varieties (breeding) where available, and application of biocontrol methods (use of atoxigenic strains and antagonists). However, seed companies may not have the infrastructure themselves or cannot charge higher seed prices to cover seed health testing costs. Breeding programs have reported sources of resistance against A. flavus preventing aflatoxin contamination [62] and against F. verticillioides preventing fumonisin production, but varieties resistant to all mycotoxigenic fungi are currently not available [63]. Insect resistance is also a valuable trait to avoid infection, because insect damage facilitates the entry of fungi into and subsequent infection of maize plants [8]. Farmers may easily adopt these varieties when combined with other beneficial traits such as tolerance to low soil fertility and drought, resistance to the parasitic weed Striga spp., or higher market value of the product. Research is already going on to optimize the dissemination of improved varieties by the formal and informal seed systems [44], as well as increase adoption of improved maize varieties by smallholder farmers [64,65]. However, earlier in this paper, we reported that there is a tradeoff between lowering the mycotoxin level and reducing insect damage [51].
The growing season offers ample opportunities to farmers, seed companies, and foundation seed producers to avoid mycotoxigenic fungal infection. Seed treatment with fungicides might reduce infection with A. flavus and A. niger, as well as simultaneously enhance germination [66], but whether it can stop seed-to-seedling transmission of F. verticillioides is debated [16]. Another control method is foliar agrochemical application which may not be feasible to smallholder farmers and may not be ecofriendly. Insecticides reduce insect damage to the plant, preventing airborne spores of mycotoxigenic fungi such as F. verticillioides from entering and infecting the plant. A combination of insecticide and fungicide can reduce infection with F. verticillioides, Fusarium ear rot incidence, and fumonisin contamination [67].
Although agrochemicals can enhance yields and production quality, high costs and adverse health effects for farmers can hamper the adoption. Biological control agents form an alternative to agrochemicals. Preharvest application of Bacillus subtilis avoids fumonisin production, because the biocontrol agent competes for the same niche as F. verticillioides [16]. Another biological control method is the application of atoxigenic strains of A. flavus to the soil surface. The atoxigenic strains colonize the soil, infect the plant, and compete for the same niche with toxic A. flavus strains [61]. A similar strategy might be feasible with atoxigenic Fusarium spp. strains to combat mycotoxigenic Fusarium spp. [68]. In addition to effectiveness against mycotoxins, biological controls lack additional benefits that lead to a financial incentive for farmers, which will most likely hamper adoption. Harvest and storage practices also form potential control options. Avoiding seed damage during harvest can avoid further fungal infection.
There are also ample opportunities to control mycotoxigenic fungi post harvest [1,19]. Fast drying of maize after harvest to a final moisture content <14% is important to prevent fungal growth during storage [1] but can be difficult to achieve in humid areas with labor scarcity at harvest time. Creating optimal storage conditions with low humidity, protection against insects, and an absence of infected plant material can avoid new infection [69]. For seed, hermetic storage bags are potentially relevant. The use of PICS bags provides a good option [70]. The use of plant extracts or essential oils and other natural compounds during storage to reduce infection has been widely investigated and recommended [71,72,73,74]. However, it is questionable whether smallholder farmers have the resources to treat seed differently from grain. Nevertheless, it is important to educate these farmers about the risks and possible routes of contamination and possible control strategies [1].
It is important to design a set of good practices during the entire supply chain with balanced attention for conditions and practices during primary production, including crop rotation, use of fungicides and insecticides, use of resistant varieties, and careful harvesting and conditions and practices after harvesting, as well as during storage, processing, and marketing, equally paying attention to mass flow and information flow. However, we make a plea to take the production, storage, and use of seed into account and not merely focus on the production of food, feed, or forage.
In addition to seed treatments based on chemical fungicides, there is a growing body of literature showing options to treat seeds using biological control agents. Work on strains of the fungus Trichoderma harzianum has shown promise both in the lab [33,34,36,75] and in the field [33,35]. Moreover, strains of bacteria from the genera Pseudomonas and Lactobacillus have been found to reduce contamination either in the field (contamination of Fusarium [37]; contamination of Aspergillus [76]) or post harvest (contamination of Aspergillus [77]). Much more field work under soil and disease pressure conditions typical to smallholder farmers in low- and middle-income countries will be needed, and input value chains will need to be developed. An important under-researched aspect is what the direct economic benefits of such seed treatments would be for smallholder farmers with different resource endowments in low- and middle-income countries, as consumer health including their own is not a sufficient incentive for seed treatment [2,3].

3.2. Adoption Constraints

Adoption of these control strategies in sub-Saharan Africa is constrained by a lack of financial incentives and lack of awareness of the health hazard. Farmers and consumers cannot discriminate between mycotoxin-contaminated maize samples and a safe product by visible inspection [78], making it highly unlikely that contaminated maize samples are sold for lower prices. Therefore, there is no financial incentive for farmers to invest in avoiding or reducing mycotoxin contaminations. Even if there was a clear financial incentive, socioeconomic constraints could still hamper adoption by smallholder farmers, as what happened for fertilizer application [79].
Another aspect is the sustainable implementation of control measurements in the seed systems. To inform millions of smallholder farmers in remote areas and convince them to make financial investments in control methods might be the biggest constraint of the informal seed system. The formal seed system consists of a relatively small number of actors, but adoption may be constrained by weak government institutions, development and enforcement of regulation, and market failure. At the same time, if farmers are using self-saved seeds (i.e., recycled seeds), simultaneous intervention in their seed production and grain production might be relatively easy and productive, once awareness has been created. Further development of biocontrol systems that can be based on locally produced antagonists or biorationals and enhance both productivity and quality is worth investigating. These could turn out to be low-cost and locally reproducible systems. These developments can be supported by stakeholders as there is some prospect of awareness, followed by action, as demonstrated by [2], as smallholder farmers are not merely driven by financial incentives.
Successful control strategies against mycotoxigenic fungal infection combine (a) effectiveness, (b) additional financial benefits beyond mycotoxigenic fungi prevention, and (c) easy and sustainable implementation in seed systems. Breeding resistant varieties is an important control method meeting these three criteria. Seed treatments, agrochemical spraying, avoiding seed damage at harvest, and storage technologies only meet the two criteria (effectiveness and additional financial benefits), but encounter important implementation problems in seed systems. Application of biological control or atoxigenic strains is effective and may have additional financial benefits, but is difficult to implement in a seed system. However, the use of biocontrol options deserves to be further explored and exploited.

3.3. Integrated Approach

Mycotoxins are here to stay and, therefore, we need to set strict control regimes and regulations [9]. We recommend an integrated approach to develop optimal mycotoxigenic fungal infection control. This approach consists of mycotoxigenic fungi- and insect-resistant varieties in combination with effective control measures during seed production, grain production, and storage that also have additional financial benefits beyond mycotoxin control and are in balance with measures preventing insect damage. Proper drying after harvest and improved storage methods should certainly be part of the integrated approach, e.g., through the use of hermetic storage bags such as PICS bags. If mycotoxigenic fungal control is still insufficient, other effective control measures can also be applied, even when they do not provide additional benefits other than control of mycotoxigenic fungi. The optimal mix may differ among regions and countries as a result of agroecological, socioeconomic, and sociopolitical differences. This strategy might also be relevant for mycotoxin contamination in other crops. Further research is recommended to test combinations of control measurements for different climatic zones, crops, and countries, as well as test their effectiveness, additional financial benefits, and sustainable implementation in the seed system. Public research programs are recommended to breed mycotoxigenic fungi resistance into varieties popular among farmers and to develop new methods to control mycotoxigenic fungal infection.

4. Conclusions and Recommendations

Mycotoxin-contaminated maize is a known human health hazard in developing countries, but the potential link between infected seed and preharvest infection is understudied. Similarly, a seed system approach to control this hazard requires more research. Maize seed samples are heavily infected with mycotoxigenic fungi, as illustrated by the Nigerian case study. A schematic overview of the formal and informal seed systems was presented to visualize the risks of mycotoxigenic fungal infection and mycotoxin contamination, as well as potential control measures. We recommend an integrated approach combining resistant varieties with other methods to prevent mycotoxigenic fungal infection, with special attention to sustainable integration in formal and informal seed systems. Further research is recommended to determine the optimal combination of control measures for different climate zones, socioeconomic conditions, and crops, as well as to breed varieties with resistance to all mycotoxigenic fungi.

Author Contributions

Conceptualization, P.C.B., T.J.S., P.L.K., and P.C.S.; methodology, P.C.B.; validation, P.C.B.; formal investigation, P.C.B.; resources, P.C.B., T.J.S., P.L.K. and P.C.S.; data curation, P.C.B.; writing—original draft preparation, P.C.B., T.J.S. and P.C.S.; writing—review and editing, P.C.B., T.J.S., P.L.K. and P.C.S.; visualization, P.C.B.; supervision, T.J.S. and P.C.S.; project administration, P.C.B. and P.L.K.; funding acquisition, P.C.B., T.J.S., P.L.K. and P.C.S. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Conflicts of Interest

The authors declare no conflict of interest.

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Agronomy 11 02168 g001 550
Figure 1. (A) Maize value chains in high- and low-income countries. Regulation by, e.g., the FDA and certifications such as HACCP avoid mycotoxin contamination in maize in high-income countries. Low-income countries lack sufficient regulations or implementation systems to avoid mycotoxin contamination in maize. A relatively large share of the maize production is consumed without industrial processing, resulting in a shorter value chain compared with the chains in high-income countries. (B) An idealized picture of the effects of formal and informal seed systems on mycotoxigenic fungal infection, mycotoxin production, and control methods in low-income countries. The formal seed system consists of government bodies, NGOs, and private companies involved in breeding, seed multiplication, external quality control, and dissemination of seed, while the informal seed system only consists of seed-producing farmers. In the formal seed system, contamination should not occur as seed health is maximized and seed treatment is standard practice to avoid survival of any possible pathogen, including mycotoxigenic fungi. Our case study (see text) demonstrates that a suboptimally functioning formal seed system may also result in seed stocks with some contamination. Arrows show flows of maize seed or grain. Control methods to avoid or reduce mycotoxigenic fungal infection include breeding insect- and mycotoxigenic fungi-resistant varieties (1), seed health testing (2), seed treatment with fungicides or biological control agents (3), atoxigenic strains (4), agrochemical application (5), biological control (6), avoiding seed damage (7), fast drying to <14% moisture (8), and clean and dry storage (9). An important question remains whether mycotoxin-producing fungi are ubiquitous in soils where maize is grown.
Figure 1. (A) Maize value chains in high- and low-income countries. Regulation by, e.g., the FDA and certifications such as HACCP avoid mycotoxin contamination in maize in high-income countries. Low-income countries lack sufficient regulations or implementation systems to avoid mycotoxin contamination in maize. A relatively large share of the maize production is consumed without industrial processing, resulting in a shorter value chain compared with the chains in high-income countries. (B) An idealized picture of the effects of formal and informal seed systems on mycotoxigenic fungal infection, mycotoxin production, and control methods in low-income countries. The formal seed system consists of government bodies, NGOs, and private companies involved in breeding, seed multiplication, external quality control, and dissemination of seed, while the informal seed system only consists of seed-producing farmers. In the formal seed system, contamination should not occur as seed health is maximized and seed treatment is standard practice to avoid survival of any possible pathogen, including mycotoxigenic fungi. Our case study (see text) demonstrates that a suboptimally functioning formal seed system may also result in seed stocks with some contamination. Arrows show flows of maize seed or grain. Control methods to avoid or reduce mycotoxigenic fungal infection include breeding insect- and mycotoxigenic fungi-resistant varieties (1), seed health testing (2), seed treatment with fungicides or biological control agents (3), atoxigenic strains (4), agrochemical application (5), biological control (6), avoiding seed damage (7), fast drying to <14% moisture (8), and clean and dry storage (9). An important question remains whether mycotoxin-producing fungi are ubiquitous in soils where maize is grown.
Agronomy 11 02168 g001
Table
Table 1. Overview of mycotoxigenic fungi identified in maize seed samples obtained from farmers (N = 87), a seed company outlet (N = 6), and a foundation seed producer (N = 6). Samples were collected in 2009 and 2010 in Nigeria. Fungal growth in each sample was determined for 500 undamaged, surface sterilized seeds after 4 days of incubation on agar. The infection frequency, i.e., the percentage samples with at least one infected seed, and the median infection incidence, i.e., the median of the percentage of seeds infected per sample based on infected samples only, are shown for seed samples from farmers, a seed company, and a foundation seed producer.
Table 1. Overview of mycotoxigenic fungi identified in maize seed samples obtained from farmers (N = 87), a seed company outlet (N = 6), and a foundation seed producer (N = 6). Samples were collected in 2009 and 2010 in Nigeria. Fungal growth in each sample was determined for 500 undamaged, surface sterilized seeds after 4 days of incubation on agar. The infection frequency, i.e., the percentage samples with at least one infected seed, and the median infection incidence, i.e., the median of the percentage of seeds infected per sample based on infected samples only, are shown for seed samples from farmers, a seed company, and a foundation seed producer.
Farmers
(N = 87)		Seed Company Outlets
(N = 6)		Foundation Seed Producer
(N = 6)
Mycotoxigenic fungiMycotoxins Produced **Seed-BorneInfection
Frequency
(%)		Infection
Incidence
(%)		Infection
Frequency
(%)		Infection
Incidence
(%)		Infection
Frequency
(%)		Infection
Incidence
(%)
Aspergillus flavusAflatoxin aU e380.6170.8830.4
Aspergillus nigerOchratoxin A bY e610.6830.61001.0
Fusarium oxysporumDeoxynivalenol cY e531.4675.1333.8
Fusarium solaniDeoxynivalenol cY e50.90- ***170.8
Fusarium verticillioides *Fumonisins aY e10055.210048.710045.1
Penicillium oxalicumSecalonic acid D dY e290.6500.2671.4
* Synonym: Fusarium moniliforme Sheldon. ** a [54]; b [47]; c [55]; d [49]; e [38]; U = unlikely, Y = yes. *** No organism identified in samples. Data are derived from [45].
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Biemond, P.C.; Stomph, T.J.; Kumar, P.L.; Struik, P.C. How Maize Seed Systems Can Contribute to the Control of Mycotoxigenic Fungal Infection: A Perspective. Agronomy 2021, 11, 2168. https://doi.org/10.3390/agronomy11112168

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Biemond PC, Stomph TJ, Kumar PL, Struik PC. How Maize Seed Systems Can Contribute to the Control of Mycotoxigenic Fungal Infection: A Perspective. Agronomy. 2021; 11(11):2168. https://doi.org/10.3390/agronomy11112168

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Biemond, P. Christiaan, Tjeerd Jan Stomph, P. Lava Kumar, and Paul C. Struik. 2021. "How Maize Seed Systems Can Contribute to the Control of Mycotoxigenic Fungal Infection: A Perspective" Agronomy 11, no. 11: 2168. https://doi.org/10.3390/agronomy11112168

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Biemond, P. C., Stomph, T. J., Kumar, P. L., & Struik, P. C. (2021). How Maize Seed Systems Can Contribute to the Control of Mycotoxigenic Fungal Infection: A Perspective. Agronomy, 11(11), 2168. https://doi.org/10.3390/agronomy11112168

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