molecules Article Co-Occurrence of Moniliformin and Regulated Fusarium Toxins in Maize and Wheat Grown in Italy Terenzio Bertuzzi 1,*, Paola Giorni 2 , Silvia Rastelli 1, Patrizia Vaccino 3 , Chiara Lanzanova 4 and Sabrina Locatelli 4 1 Department of Animal, Food and Nutrition Science—DIANA, Università Cattolica del Sacro Cuore, Via Emilia Parmense 84, 29122 Piacenza, Italy; [email protected] 2 Department of Sustainable Crop Production—DIPROVES, Università Cattolica del Sacro Cuore, via Emilia Parmense 84, 29122 Piacenza, Italy; [email protected] 3 Council for Agricultural Research and Economics (CREA)—Research Center for Cereal and Industrial Crops, Strada Statale, 11 per Torino km 2.5, 13100 Vercelli, Italy; [email protected] 4 Council for Agricultural Research and Economics (CREA)—Research Center for Cereal and Industrial Crops, Via Stezzano, 24, 24126 Bergamo, Italy; [email protected] (C.L.); [email protected] (S.L.) * Correspondence: [email protected] Academic Editor: Joselito P. Quirino Received: 23 April 2020; Accepted: 21 May 2020; Published: 23 May 2020 Abstract: The co-occurrence of moniliformin (MON), fumonisins (FBs), and deoxynivalenol (DON) was evaluated in maize, durum, and common wheat grown in different experimental fields located in several Italian regions. MON was quantified using a LC-MS/MS method adding lanthanum ions in the mobile phase. In maize, MON contamination was widespread and considerable; the toxin 1 was detected in almost all the samples (95.1%) and exceeded 500 and 1000 µg kg− in 42.0% and in 18.5% of samples, respectively. Significant positive correlation was found between MON and FB contamination levels. When there were not droughty climate conditions, a positive significant correlation was found between growing degree days (GDD) and MON values. In wheat, MON contamination was not widespread like in maize and it was lower in common wheat than in durum wheat. In durum wheat, MON was detected in 45.0% of the samples with only 6 samples (7.5%) 1 exceeding 500 µg kg− , while in common wheat the toxin was detected above the LOD in 18.7% of 1 samples exceeding 100 µg kg− in only two samples (2.5%). No correlation was found with DON contamination. Climate conditions influenced both MON and DON occurrence. Keywords: moniliformin; Fusarium mycotoxins; maize; wheat 1. Introduction Mycotoxins are one of the most important contaminants in cereals. They are toxic secondary metabolites usually produced, in favorable environmental conditions, by Aspergillus, Penicillium, Alternaria, and Fusarium fungi. Among these species, Fusarium are the most prevalent mycotoxin-producing fungi in Central and Southern Europe. Fusarium species are known as producers of several mycotoxins, including regulated ones fumonisins, trichothecenes, and zearalenone. Generally, in Italy, the most widespread mycotoxins for maize and wheat are fumonisins (FBs) and deoxynivalenol (DON), respectively. Besides these toxins, moniliformin (MON) is a not negligible emerging Fusarium mycotoxin occurring in cereals; generally, higher levels have been found in maize than in other crops. MON is mainly produced by F. subglutinans, F. temperatum, F. verticilloides, and F. proliferatum. Moreover, the last two fungal species are also able to produce FBs [1]. MON is a highly polar and acidic molecule (Figure1) and occurs as a water-soluble sodium or potassium salt [2]. Molecules 2020, 25, 2440; doi:10.3390/molecules25102440 www.mdpi.com/journal/molecules Molecules 2020, 25, 2440 2 of 13 Molecules 2020, 24, x 2 of 13 FigureFigure 1.1. ChemicalChemical structurestructure ofof moniliforminmoniliformin (X(X=H,=H, Na,Na, oror K).K). CardiotoxicityCardiotoxicity andand hepatotoxicityhepatotoxicity areare itsits majormajor adverseadverse healthhealth eeffects,ffects, asas indicatedindicated byby thethe PanelPanel onon ContaminantsContaminants inin thethe FoodFood ChainChain (CONTAM)(CONTAM) ofof thethe EuropeanEuropean FoodFood SafetySafety AuthorityAuthority (EFSA)(EFSA) [[3].3]. TheThe mainmain target of MON seems seems to to be be enzymes enzymes with with thiamine thiamine as as a cofactor. a cofactor. Since Since these these enzymes enzymes are arepart part of the of the respiratory respiratory chain, chain, any any impairment impairment of oftheir their activity activity results results in in a a shortage shortage of energy, respiratoryrespiratory stress,stress, and and myocardial myocardial loss loss of of functionality. functionality. Furthermore, Furthermore, MON MON can can reduce reduce the the activity activity of glutathioneof glutathione peroxidase peroxidase and and glutathione glutathione reductase, reductase, thus thus increasing increasing oxidative oxidative stress stress [ 4[4].]. Concerning Concerning 1 sub-acutesub-acute toxicitytoxicity inin malemale rats,rats, thethe relativerelative LD50LD50 hashas beenbeen setset at at 6 6 mg mg kg kg−−1 bwbw perper dayday forfor mortalitymortality 1 andand atat 1515 mgmg kgkg−−1 bw forfor cardiotoxicitycardiotoxicity [[5].5]. Due to thethe lowlow numbernumber ofof studiesstudies onon MONMON toxicity,toxicity, thethe EFSAEFSA CONTAM Panel Panel has has not not been been able able to toestablish establish a TDI a TDI for this for toxin. this toxin. Furthermore, Furthermore, a recent a review recent reviewreported reported an interactive an interactive toxicity toxicity of MON of and MON FBs and [6]. FBsTo date, [6]. Tono date,regulatory no regulatory limits have limits been have fixed been for fixedMON for and MON the andEFSA the has EFSA stated has statedthat further that further toxicity toxicity studies studies are needed, are needed, also alsorecommending recommending the thecollection collection of more of more data data on on MON MON occurrence occurrence [3]. [3]. Although Although MON MON can can contaminate severalseveral cerealcereal commodities,commodities, few few datadata areare availableavailable inin literatureliterature aboutabout itsits spreadspread andand thethe relationrelation withwith meteorologicalmeteorological conditions,conditions, growing growing season season and and area area has beenhas been poorly poorly investigated. investigated. Considering Considering the most the recent most studies, recent astudies, not negligible a not negligible MON contamination MON contamination was found was in cerealsfound in produced cereals produced both in Scandinavian both in Scandinavian countries andcountries in Southern and in Europe, Southern showing Europe, that showing MON can that be produced MON can in dibeff erentproduced climate in conditionsdifferent andclimate by severalconditionsFusarium and byspecies several [7– Fusarium10]. As regards species the [7–10]. Mediterranean As regards area, the considerableMediterranean MON area, contamination considerable 1 wasMON detected contamination in Serbian was maize detected produced in Serbian from maize 2016–2018 produced showing from values 2016–2018 up to showing 3856 µg kgvalues− [11 up]; into Italy3856 MONµg kg− was1 [11]; found in Italy in MON 75% of was 12 naturallyfound in 75% contaminated of 12 naturally winter contaminated wheat samples winter (maximum wheat samples value 1 80(maximumµg kg− )[ value12] and 80 inµg almost kg−1) [12] all 108and maize in almost samples all 108 grown maize in samples Northwestern grown Italy in Northwestern (maximum value Italy 1 2606(maximumµg kg− value)[13 ].2606 Beccari µg kg et−1) al. [13]. (2020) Beccari [14 et] showed al. (2020) that [14] durum showed wheat that durum cultivated wheat in Centralcultivated and in NorthernCentral and Italy Northern may be Italy subject may to beFusarium subject mycotoxinto Fusarium accumulation, mycotoxin accumulation, including MON; including in our MON; recent in studyour recent regarding study the regarding development the of development an alternative of LC-MS an /alternativeMS method LC-MS/MS for its determination, method for MON its wasdetermination, detected in 10MON/10 maize was detected and in 5/ 10in 10/10 wheat maize samples and [15 in]. 5/10 Finally, wheat Scarpino samples et al.[15]. (2020) Finally, [16] reportedScarpino aet weak al. (2020) decrease [16] of reported MON contamination a weak decrease after of di MONfferent contamination large-scale maize after dry-milling different processes.large-scale Inmaize this work,dry-milling MON occurrenceprocesses. inIn maizethis work, and wheatMON (commonoccurrence and in durum) maize and grown wheat in fields (common located and in di durum)fferent Italiangrown regionsin fields was located investigated in different and Italian possible regions correlation was investigated with FB and and DON possible contamination correlation and with with FB climaticand DON conditions contamination were evaluated. and with climatic conditions were evaluated. ThisThis studystudy took took into into consideration consideration the the occurrence occurrenc ofe moniliformin,of moniliformin, an emergingan emerging mycotoxin, mycotoxin, in the in principalthe principal cereals cereals cultivated cultivated in Italy—maize in Italy—maize and wheat—and and wheat—and its correlation its correlation with the mostwith commonthe most Fusariumcommon mycotoxins,Fusarium mycotoxins, fumonisins fumonisins and deoxynivalenol. and deoxynivalenol. Furthermore, Furthermore, influence of influence climate conditionsof climate duringconditions the growingduring the period growing of these period cereals of these was cereals evaluated. was evaluated. 2.2. ResultsResults andand DiscussionDiscussion