Accepted Manuscript Crop molds and mycotoxins: alternative management using biocontrol Phuong-Anh Nguyen, Caroline Strub, Angélique Fontana, Sabine Schorr- Galindo PII: S1049-9644(16)30199-2 DOI: http://dx.doi.org/10.1016/j.biocontrol.2016.10.004 Reference: YBCON 3497 To appear in: Biological Control Received Date: 20 July 2016 Revised Date: 10 October 2016 Accepted Date: 18 October 2016 Please cite this article as: Nguyen, P-A., Strub, C., Fontana, A., Schorr-Galindo, S., Crop molds and mycotoxins: alternative management using biocontrol, Biological Control (2016), doi: http://dx.doi.org/10.1016/j.biocontrol. 2016.10.004 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. Crop molds and mycotoxins: alternative management using biocontrol Phuong-Anh Nguyen*, Caroline Strub, Angélique Fontana, Sabine Schorr-Galindo UMR Qualisud (Université Montpellier), Place Eugene Bataillon, 34095 Montpellier Cedex 5, France * Corresponding author: Email: [email protected] Phone number: +33 4 67 14 33 12 Fax number: +33 4 67 14 42 92 Abstract Phytopathogenic and/or mycotoxigenic filamentous fungi are involved in a great number of plant diseases that cause yield and quality losses of crops. Besides the economic damages, these fungi produce mycotoxins that present health risks for humans and animals who consume contaminated foods. The most dangerous mycotoxins in the agriculture and the food industry that are regulated in European Union (trichothecenes especially deoxynivalenol, fumonisins, aflatoxins and ochratoxin A) are produced by three main fungal genera (Fusarium, Aspergillus and Penicillium). Many approaches have been applied to prevent and manage the phytopathogenic and/or mycotoxigenic fungi. However, these methods involve the use of chemical inputs that are harmful for humans, animals and environment. In a concern of sustainable development, the application of biocontrol has been considered for addressing this problem in a more environmentally friendly way. This review considered the incidence of the three fungal genera and their mycotoxins in crops and in foodstuff. The impacts of the fungal contamination and the toxin accumulation were reported. Besides, the biological control means against these pathogens were reviewed. Among them, organic amendments showed to be effective in both producing antifungal activities and reinforcing plant health. Keywords: Filamentous fungi; mycotoxins; phytopathogenesis; biocontrol agents; organic amendments 1 Introduction Fungi take an important part in the microorganism world. They might have benefices in sciences, industries and technology. Nevertheless, filamentous fungi appear to be a potential harm for humans, animals and crops. In fact, many of them are phytopathogenic and/or mycotoxigenic. Their occurrence leads to many soil-borne diseases for plants, thereby causing various food and feed- borne mycotoxicoses for humans and animals through the consumption of contaminated products. Thus, these filamentous fungi damaged not only human and animal health but also the international economy. The main targets of molds are cereals, grains, fruits and vegetables. The major toxins that are associated with the contamination are deoxynivalenol (DON) (or nivalenol in some areas), fumonisins, zearalenone, aflatoxins and ochratoxin A (OTA) (Miller, 2008). These are the most important mycotoxins (Pitt, 2000) produced mainly by species of Aspergillus, Fusarium and Penicillium. Cereals constitute a staple food for all over the world as well as the main source of animal feed (Von Braun, 2007). So, research for protecting crops from molds and their mycotoxins has become indispensable. For decades, various agricultural practices have been applied. However, the current approaches dealing with the fungal phytopathogens were based on the use of chemical agents that are reported to be acutely and chronically hazardous to humans, animals and ecosystems. Within the context of the “organic farming” and the sustainable development concern, alternative practices have to be developed, notably the biological solutions that maintain the quality and the abundance of crops with respecting the ecosystems and human and animal health. In this context, this review describes: i) the main phytopathogenic and mycotoxigenic filamentous fungi and their mycotoxins, ii) the main strategies of biological control applied to these molds with emphasis to the application of organic amendments. 1. Phytopathogenic and mycotoxigenic fungi 1.1. The genus Fusarium 1.1.1. Phytopathogenesis 2 Fusarium is a large group of ascomycete fungi that belongs to the class of Sordariomycetes and to the family of Nectriaceae. Fusarium is one of the most important phytopathogenic group (Booth, 1971). The occurrence of Fusarium can be found in all types of plant tissues, soil debris and soils in many cereal crops. The most affected cereal by the pathogenic Fusarium are corn (Aboul-Nasr and Obied- Allah, 2013; Sreenivasa et al., 2013; Becker et al., 2014; Liu et al., 2014), wheat (Cui et al., 2013; Lindblad et al., 2013; Tittlemier et al., 2013), barley (Oliveira et al., 2012; Běláková et al., 2014), sorghum (Sreenivasa et al., 2013; Divakara et al., 2014; Kange et al., 2015) and oat (Kiecana et al., 2012; Fredlund et al., 2013; Kiecana et al., 2014). The Fusarium species responsible for these contaminations are Fusarium graminearum, F. sporotrichioides, F. poae, F. avenaceum, F. culmorum, F. accuminatum, F. langsethiae, F. verticillioides, F. proliferatum, F. oxysporum, F. anthophilum and F. paranaense. Fusarium graminearum is the most common species in the infections. The Fusarium pathogens were also found in various vegetables and fruits, i.e. soybeans (Arias et al., 2013; Chang et al., 2015; Costa et al., 2016), chili (Sundaramoorthy et al., 2012; Jalaluldeen et al., 2014) and tomato (Bharat and Sharma, 2014; Loganathan et al., 2014). Fusarium spp. are the major soil-borne and seed-borne pathogens causing damage to a wide range of crops and they are responsible for various diseases. The most frequent diseases in cereal crops is Fusarium Head Blight – FHB that can lead to enormous loss of yield and low quality of crops (Zhang et al., 2013). Fusarium spp. are causative agents for rot disease in many plants: root rot in soybean (Arias et al., 2013; Chang et al., 2015), stalk rot in maize (Kaur et al., 2014), root and steam rots in cucumber (Pavlou and Vakalounakis, 2005). Fusarium oxysporum f. sp. cucumerum J.H.Owen caused the Fusarium wilt that has been reported as one of the most severe diseases in cucumber (Qiu et al., 2012). Fusarium oxysporum caused also the wilt in banana (Ploetz, 2006) and melon (Ma et al., 2014; Cohen et al., 2015). A newly soil-borne pathogen strain of F. oxysporum, which was identified as F. oxysporum f. sp. citri, caused diseases on seedling of citrus trees (Hannachi et al., 2015). The loss of yield and the severity of diseases is linked to the extent of the Fusarium infection (Chang et al., 2015). Fusarium infections are also reported in both humans and animals (Zhang et al., 2006; Antonissen et al., 2014). 1.1.2. Toxinogenesis The majority of the Fusarium species are able to produce mycotoxins and are involved in the accumulation of toxins in food and feed which leads to human and animal intoxications. These mycotoxins produced by Fusarium sp. are called fusariotoxins and are characterized by their acute 3 and/or chronic toxicity. There are three groups of fusariotoxins: trichothecenes, zearalenone and fumonisins. Some species can produce several mycotoxins at the same time like F. graminearum which is considered as the most virulent among the Fusarium genus producing trichothecences. F. graminearum can produce also the zearalenone and some other secondary metabolites such as culmorin, sambucinol, dihydroxycalconectrin, butenolide and fusarin C which are more or less toxic (Farber and Sanders, 1986; Wang and Miller, 1988; Lysøe et al., 2006). • Trichothecenes Trichothecenes are a group of mycotoxins formed on the basis of their chemical structure and produced by various Fusarium spp. This group constitutes more than 200 chemical derivatives classed in 4 types A, B, C and D in which the 2 types A and B are mostly issued from Fusarium spp. and prevalent in the nature. The predominant trichothecenes in crops are DON and its derivatives, nivalenol, T-2 and HT-2 toxin and diacetoxy-scirpenol (DAS) produced mainly by Fusarium graminearum, F. sporotrichioides, F. poae, F. culmorum, F. asiaticum, F. crookwellense, F. equiseti, F. langsethiae and F. accuminatum (Golinski et al., 1988; Bottalico and Perrone, 2002; Zhang et al., 2010; Gale et al., 2011). Trichothecenes appear essentially in the food commodities based on maize and wheat such as flour, pasta and other cereals in which DON is the most found. DON was present in 85-90% of wheat samples with incidence of 500-15,000 µg/kg in China (Cui et al., 2013) and up to 4700 µg/kg in Canada (Tittlemier et al., 2013). In malting barley of Czech, DON was found at 2213.5 µg/kg with other trichothecenes as toxins T-2 and HT-2 (Běláková et al., 2014). Trichothecenes were also detected in oat, including T-2, HT-2, DAS and DON (127 µg/kg) with acetylated derivatives as 3- Acetyldeoxynivalenol (3-AcDON) and 15-Acetyldeoxynivalenol (15-AcDON) (Kiecana et al., 2012). The toxins contribute to the diseases in crops such as FHB and wilts (Bottalico and Perrone, 2002; Dedeurwaerder et al., 2014; Aoki et al., 2015; Touati-Hattab et al., 2016). They decrease the germination of grains in the water sensitivity and the accumulation of mycotoxins thus reduce the quality and the yield of crops productions (Oliveira et al., 2012). The toxin levels are positively correlated with the pathogen occurrence (Lindblad et al., 2013).