# Incidence of four genera of fungi in organic and low-input farming conditions in/on the grain of bread wheat over a 13-year period in France

Bernard Rolland, Denise Deffains, Patrick Delarue, Stephane Gilles, Antonin

Le Campion, Alain Monnier, None Jean-Yves-Morlais, Hélène Navier,

Alexandre Pichard, Patrice Walczak, et al.

► To cite this version:

Bernard Rolland, Denise Deffains, Patrick Delarue, Stephane Gilles, Antonin Le Campion, et al. Incidence of four genera of fungi in organic and low-input farming conditions in/on the grain of bread wheat over a 13-year period in France. Organic Agriculture, 2023, Organic Agriculture, 3 (4), pp.503-511. 10.1007/s13165-023-00443-4. hal-04305725

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1 Title:

2 Incidence of four genera of fungi in organic and low-input farming conditions in/on the grain

3 of bread wheat over a 13-year period in France

4

5 Author information:

6 Bernard Rolland*,¹, Denise Deffains¹, Patrick Delarue¹, Stéphane Gilles², Antonin Le

7 Campion¹, Alain Monnier¹, Jean-Yves-Morlais¹, Hélène Navier¹, Alexandre Pichard², Patrice

8 Walczak³, Rémi Perronne*,¹

9 ¹ INRAE, Agrocampus Ouest, Université de Rennes, IGEPP, F-35650 Le Rheu, France

10 ² Agri-Obtentions, Ferme de Gauvilliers, 78660 Orsonville, France

11 ³ INRAE, UE FERLUS 1373, Fourrages Environnement Ruminants Lusignan, 150 route le

12 Chêne, CS 80006, 86600 Lusignan, France

13 *co-first authors

14

15 Corresponding author:

16 Rémi Perronne

17 remi.perronne@inrae.fr

18

19 ORCID number of authors:

20 Rémi Perronne: 0000-0002-5089-0510

21

22

23 **Abstract** Bread wheat can be infected and/or contaminated by several genera of mycotoxin-

24 producing fungi. In the European Union, several mycotoxins are subject to defined limits for

25 human consumption. Speculation has arisen about the potential higher contamination level of

26 mycotoxins produced by *Fusarium* species in organic compared to conventional production

27 systems. So far, many studies have focused on the level of mycotoxins, highlighting comparable

28 levels in organic and conventional farming. In this long-term study, we monitored, each year

29 over a 13-year period in several sites in France and for a set of bread wheat genotypes, the

30 incidence of four fungal genera on bread wheat grains from both conventional low-input and

31 organic farming. During this long period of monitoring, we used the same morphological

32 characterization of fungal colonies. The results obtained highlighted two general trends. First,

33 the incidence of the genus *Fusarium* in grains was generally lower than or equal to 1% in more

34 than 60% of ‘year × site’ combinations, both in low-input and organic farming conditions. In

35 contrast, the genus *Alternaria* was dominant in the vast majority of combinations. Second, the

36 main explanatory factors of the incidence of fungus on grains, independently of the genus and

37 the farming conditions, were the year and the ‘year × site’ interaction, suggesting the dominant

38 influence of the environmental conditions of the year and the site on the relative development

39 of the fungal genera in/on grains. According to these results, organic or low-input production

40 of bread wheat does not represent a significant risk for the development of *Fusarium* head blight

41 in France.

42

43 **Keywords** Fungal incidence. Morphological identification. *Fusarium*. *Alternaria*. *Epicoccum*

44 . *Microdochium*

45

46 Acknowledgements The authors acknowledge the teams from Institut national de la recherche

47 agronomique (INRA, currently INRAE) experimental units of Auzeville, Lusignan, Le Moulon,

48 Le Rheu, as well as the team of Agri-Obtentions for their involvement in these experiments.

49 Our work has been supported for 14 years by French Technical Institute for Organic farming

50 (Laurence Fontaine ITAB) and InterBio Bretagne as part of the State-Region (Brittany) Project
Contract (CPER). We would like to thank organic farmers who received INRA on-farm trials in Brittany (GAEC La Mandardière), Poitou-Charentes (MM. Pinelli and Ingrandes) and Ile-de-France (F. Chevalier) regions for 13 years, and for sharing their knowledge and perspectives on agricultural practices. The publication is in memory of Maxime Trottet who developed the procedure, initiated by Laurent Saur, of morphological characterization of fungal colonies in INRA Le Rheu. We thank the editor and the three anonymous reviewers who helped to improve the manuscript.

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Competing interests The authors declare no competing interests.

60

**Author contribution** BR conceive and design the study. Material preparation and data collection were performed by DD, PD, SG, ALC, AM, JYM, HN, AP and PW. Morphological characterization of fungal colonies were performed by DD, PD and JYM. Statistical analyses were performed by RP. The first draft of the manuscript was written by RP and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

67

**Data availability** The datasets and metadata will be accessible on the publicly available Data INRAE repository at https://entrepot.recherche.data.gouv.fr/dataverse/inrae

70

**Supplementary Information**

**Online Resource 1** Coordinates of the sampling locations in conventional low-input and organic farming systems

**Online Resource 2** List of bread wheat genotypes retained for the statistical analyses in conventional low-input and organic farming systems

75
76 **Introduction**

77

78 The agricultural intensive production model is currently questioned because of agronomic,
79 environmental, public health and sometimes socio-economic issues (van der Werf 1996; Loyce
80 et al. 2012; Bourguet and Guillemaud 2016). In this context, reducing the reliance of agriculture
81 on external inputs constitutes a priority to achieve more sustainable models of production.
82 However, an alternative model such as organic farming has been questioned for several decades
83 about its ability to ensure food safety (Magkos et al. 2006; Lairon 2010; Garcia and Teixeira
84 2017). Currently, organic farming is characterized by an increasing consumer demand, which
85 requires paying attention to the sanitary quality of food production, including mycotoxin
86 contamination (Brodal et al. 2016).

87 This is particularly the case for bread wheat for which grain can be contaminated by several
88 genera of mycotoxin-producing fungi (Brodal et al. 2016), especially by different species of
89 *Fusarium* causing head blight. This plant disease results from a complex of species belonging
90 to the *Fusarium* genus (Parry et al. 1995). *Fusarium* head blight (FHB) leads to important
91 economic consequences worldwide, important yield losses and reduction in quality production
92 leading to the destruction of contaminated grain lots, as well as potential contamination by a
93 range of harmful mycotoxins to human and animal health (Reddy et al. 2010). These
94 mycotoxins, amongst others deoxynivalenol and zearalenone, are produced by several
95 *Fusarium* species, especially *Fusarium graminearum* (Reddy et al. 2010; Dean et al. 2012).
96 The mycotoxins are subject to government regulation in the EU, i.e., defined limits in cereals
97 for human consumption (Commission Regulation (EC) No 1881/2006).

98 Speculation has arisen about the potential higher contamination level of mycotoxins produced
99 by *Fusarium* species in organic compared to conventional production model, and a set of studies
100 have investigated this issue. However, in the current state of knowledge, organic farming seems
101 usually able to maintain a low level of contamination by mycotoxins, comparable or lower than
102 in conventional farming (Brodal et al. 2016). The hypothesis that several agricultural practices
103 would be less favourable for the development of *Fusarium* species causing FHB in organic
104 farming has been proposed. In fact, a low level of nitrogen supply and a crop sequence including
105 fewer cereals reduce the severity of FHB and the level of mycotoxins (Dill-Macky and Jones
106 2000; Lemmens et al. 2004; Heier et al. 2005; Bernhoft et al. 2012).

107 While many studies have focused on the level of mycotoxins in organic and conventional
108 farming (see e.g., Edwards 2009; Bernhoft et al. 2012; Brodal et al. 2016), only few have
109 considered the incidence of different fungal genera in/on the grain of bread wheat. These latter
110 studies have shown a low incidence of *Fusarium* species on organically produced grain, while
111 the fungal community was dominated by other fungal genera (Lazzaro et al. 2015; Lenc 2015).
112 However, these studies mainly relate to few years and a limited number of varieties, furthermore
113 not identifying the main explanatory factors of the *Fusarium* incidence in the different
114 production models.

115 In this study, we monitored, each year over a 13-year period in several sites in France and for
116 a set of bread wheat genotypes, the incidence of four fungal genera on grain of bread wheats
117 from both conventional and organic farming conditions.

118 More specifically, we addressed the following questions:

119 (1) What was the incidence of the four genera of fungi on the grain of bread wheat over the
120 period and between sites in both conventional and organic farming systems?

121 (2) To what extent do year, site, genotype and their interactions explain differences in incidence
122 of the genus *Fusarium* as well as other fungal genera in/on the grain of bread wheat in both
123 conventional and organic farming systems?

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125
126 **Material and methods**

127

128 Sample collection

129

130 Wheat samples were collected immediately after harvest from experimental field trials from
131 2007 to 2019 in three areas in France (Brittany, Ile-de-France and Poitou-Charentes) in both
132 conventional and organic farming systems. In our study, conventional farming systems
133 corresponded to low-input systems with no fungicide and growth regulator used, a lower sowing
134 rate and a reduction of nitrogen application (based on N balance sheet minus 60 kgN/ha) but
135 with herbicides used to suppress weeds (see Le Campion et al. 2014 for details).

136 For each site in low-input farming, when available, a site in organic farming located near the
137 conventional farming site was chosen to limit variation due to large-scale environmental
138 variables such as meteorological conditions (see Online Resource 1 for coordinates). However,
139 no organic farming site was repeatedly available near the low-input site in Poitou-Charentes,
140 so only two sites were monitored in organic farming conditions while three sites were monitored
141 in low-input farming conditions. In each site and each year, four repetitions were carried out
142 for each wheat genotype in plots of 8.5m² using a randomised block design.

143 Samples were made in conditions of natural contamination on a substantial list of genotypes
144 representative of the winter bread wheat varieties sown in low-input and organic farming over
145 the period considered, including susceptible to tolerant wheat genotypes to FHB. *Fusarium*
146 *graminearum* was the main species of *Fusarium* in France during the period studied. Given the
147 duration of the period studied, the genotypes monitored have been replaced over the years,
148 representing 34 wheat genotypes under low-input conditions and 14 wheat genotypes under
149 organic conditions, for a total of 289 wheat samples collected under low-input and 155 wheat
150 samples collected under organic conditions. Only wheat genotypes monitored for at least two
151 years were retained in this study. The kernels were harvested at maturity with 14% of moisture
152 (0.5-1kg per sample), and sub-samples of 100 kernels were chosen randomly and stored in paper
153 bags at room temperature with 13-15% humidity until analysed for about 6 months. Visible
154 FHB contamination on spikes was not observed in the field during any of the years concerned
155 in this study.

156

157 Morphological characterization of fungal colonies

158

159 To determine the incidence of the different fungal genera, one hundred kernels were randomly
160 chosen from each sub-sample, surface disinfected with 1% NaClO solution for 2 min, rinsed 4
161 times with running water, and dried for 12h under laminar flow hood. The use of running water
162 cannot exclude a contamination introducing fungal spores and/or bacteria on the grains. Ten
163 kernels were evenly placed into 10 separate Petri dishes (Ø 55 mm) containing potato dextrose
164 agar, and incubated for 5 days at room temperature under conventional lighting without day-
165 night cycle. Each colony was identified on cultural and morphological criteria to genus level
166 among four genera, i.e. *Alternaria*, *Epicoccum*, *Fusarium* and *Microdochium* based on
167 pigmentation of aerial mycelium and growth rate of mycelium, especially following the
168 descriptions proposed by Pitt and Hocking (1997). The incidence was considered as the
169 proportion of kernels infected by fungi of these four genera. During this long-term monitoring,
170 we used the same morphological characterization of fungal colonies. However, we point out
171 that the results of this study are relative to the method used. In particular, it is possible that some
172 fungal species can be overgrown by colonies of other fungal species growing more rapidly,
173 even if the incubation time was intended to limit this type of bias.

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175

Incidence of different fungal genera on wheat grains in low-input and organic farming conditions

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The average incidence of each genus, or the absence of aerial mycelium development, is graphically represented per year and site, considering all bread wheat genotypes combined. This graphical representation constitutes a synthesis of the useful data for low-input and organic farming, i.e., 13 years × 3 sites × 5-16 genotypes per year for low-input farming conditions and 13 years × 2 sites × 5-8 genotypes per year in organic farming conditions. This graphical representation has not been subjected to statistical analysis due to the unbalanced design of the data, i.e., the lack of data in certain years on certain sites. The statistical analyses described hereafter were conducted on a suitable sub-dataset.

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Sources of variability of the incidence of fungi on wheat grain per genus in low-input and organic farming conditions

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For each fungal genus and farming condition separately, we assessed the effects of year, site, genotype and their interactions on the incidence of fungi on wheat grains using linear models. First, some data were removed before applying statistical analyses, i.e., the genotypes tested in a single or two sites for low-input and a single site for organic farming conditions. The datasets focused on 7 years × 3 sites × 26 genotypes in low-input and 11 years × 2 sites × 13 genotypes in organic farming conditions (see Online Resource 2 for the list of genotypes).

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Second, we implemented a full additive linear model including year, site, genotype and all second-order interactions, and we compared this full model with all other simpler additive models, including only a subset of the environmental variables. The comparison was based on the second-order Akaike information criterion (AIC<sub>c</sub>; Sugiura 1978), and considering all the explanatory variables as factors. We checked for homogeneity of variances (Bartlett test, visual inspection), normality of the residuals (Shapiro test, visual inspection) and influential points (Cook's distance). Sum to zero contrasts were applied prior to fitting models. We applied a transformation (log<sub>10</sub>+1, Box-Cox+1, Box and Cox 1964) or not on the response variable due to asymmetry in the data distribution depending on the fungal genus. Assumptions were met after transformation or not for the genera *Fusarium*, *Epicoccum* and *Alternaria*.

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Third, the best model was retained, that corresponds to the most parsimonious model with the lowest AIC<sub>c</sub> (AIC<sub>best</sub>). The best model was compared with the intercept-only model using AIC<sub>c</sub> values, i.e., ΔAIC<sub>c</sub> = AIC<sub>0</sub> - AIC<sub>best</sub> in order to ensure the relevance of the best model (a value lower than 2 indicating that the best model was equivalent to the intercept-only model, Burnham and Anderson 2004). The goodness of fit of the models was estimated using an adjusted R<sup>2</sup> (R<sup>2</sup><sub>adj</sub>). We performed a type III ANOVA on the best model.

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Concerning the genus *Microdochium*, no transformation was relevant to validate the assumptions. This result is due to the very strong asymmetry in the data distribution due to the absence of *Microdochium* observed in most cases (70% in low-input conditions, 52% in organic conditions), making the application of a linear model unsuitable. We have chosen not to present the results for the genus *Microdochium* in this study. First, this asymmetry requires the use of another type of model that would not be directly comparable with the results of the linear models (e.g. quasi-binomial generalized linear model). Then, there was non-independence of the four fungal genera in our study, the development of the aerial mycelium of a given fungal genus excluding the development of another genus (except in very rare exceptions), so showing the results of the four genera would lead to overinterpreting the data.

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Statistical analyses were performed using R 4.0.1 (R Development Core Team 2022), its packages 'ggplot2' for graphical presentation, 'forecast' for Box-Cox transformation, 'AICcmodavg' for model selection based on AIC<sub>c</sub> and 'car' for type III ANOVA.

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## Results

Incidence of different fungal genera on wheat grain in low-input and organic farming conditions

Data is based on 289 wheat samples collected under low-input and 155 wheat samples collected under organic farming conditions. Several main trends can be drawn from these long-term time monitoring. As stated above, it should be noted that the results are relative to the method used to characterize the fungal colonies.

First, the incidence of the genus *Fusarium* in bread wheat grains was generally low to nil, with a few rare exceptions (Fig. 1, Fig. 2). Indeed, the incidence of *Fusarium* was higher than 10% only in 2008 in organic conditions and in 2010 in low-input conditions, while lower than or equal to 1% in 61% of ‘year × site’ combinations in organic conditions and 64% of ‘year × site’ combinations in low-input conditions.

Second, the absence of aerial mycelium on bread wheat grain was not the most frequently observed case. Indeed, we observed a single combination with more than 50% of grains without fungal development in low-input conditions and no combination in organic farming conditions (Fig. 1, Fig. 2). On average, 89% of wheat grains were characterized by a fungal development in both low-input and organic conditions, with significant variability between ‘year × site’ combinations.

Third, in the vast majority of combinations considered, the genus *Alternaria* was dominant on wheat grains, i.e., in 89% of combinations in low-input conditions and 92% of combinations in organic conditions. The other genera showed a high incidence only in certain years and in certain sites. For instance, the genus *Microdochium* showed substantial development in Ile-de-France in 2016, while the genus *Epicoccum* was characterized by a higher incidence in 2012 (Fig. 1, Fig. 2).

<figure><img src="image_2.png" /></figure>
<figure><img src="image_3.png" /><figcaption>**Fig. 2** Average incidence of the four different fungal genera on bread wheat grain in organic farming between 2007 and 2019 at two sites are represented by the following shades of gray from bottom to top: *Fusarium* in black, *Microdochium* in dark gray, *Epicoccum* in gray, *Alternaria* in light gray, and absence of aerial mycelium observed in white. All bread wheat genotypes per year and site have been used to compute the average incidence, i.e., between 5 and 8 genotypes depending on the year considered. NA indicates an absence of data monitored concerning the particular ‘year × site’ combination. Bri = Brittany, IdF = Ile-de-France</figcaption></figure>

Sources of variability of the incidence of fungi on wheat grain per genus in low-input and organic farming conditions

Considering the relevant sub-datasets and after confirmation that the prerequisites were met, a best model was identified for each case studied. This best model was always much more relevant than the intercept-only model, confirming that at least some explanatory variables are significantly explanatory for each case (Table 1). Moreover, $R^2_{adj}$ was between 0.62 and 0.92, highlighting medium to high accuracies, depending on the model (Table 1). The statistical analyses carried out underlined that, for all the models tested, regardless of the fungal genus and the farming conditions, the year and the ‘year × site’ interaction had a large effect on the incidence of fungi on wheat grain. In contrast, the site effect was often non-significant or weakly significant, especially under organic conditions, and a low genotype effect was observed only for *Alternaria* in organic conditions (Table 1). It should be noted that a bias of the statistical analysis was related to the replacement of genotypes studied over time. Indeed, the long-term
281 monitoring did not always characterize the same genotypes, this effect being then partially
282 confused with the year effect, potentially explaining why the year effect is usually the only one
283 significant in the analysis.

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285

286 **Table 1** Results of the best additive linear models indicating the effect of year, site, genotype and year × site
287 second-order interaction on the incidence of the genera *Fusarium*, *Epicoccum* and *Alternaria* in both low-input
288 and organic farming conditions considered separately. Box-Cox+1 and log₁₀+1 refer to the Box-Cox
289 transformation (transformation parameter λ = -1) and the base 10 logarithm after adding a constant (+1) to the raw
290 values, respectively. AIC₀ - AICbest corresponds to the difference of AICc between the best model and the intercept-
291 only model. The goodness of fit of the models was estimated using an adjusted R² (R²adj). P-value estimation is
292 based on F-test, *P* < 0.05, ***P* < 0.001, n.s., not significant. / indicates that the explanatory variable was not
293 included in the best model. Degrees of freedom (df) vary between models applied on datasets in low-input and
294 organic farming conditions

<table><thead><tr><th rowspan="2">Farming conditions</th><th rowspan="2">Fungal genus</th><th rowspan="2">Transformation</th><th rowspan="2">AIC<sub>0</sub> - AIC<sub>best</sub></th><th rowspan="2">R<sup>2</sup><sub>adj</sub></th><th colspan="4">F-test (P-value)</th></tr><tr><th>Intercept</th><th>Year</th><th>Site</th><th>Genotype</th><th>Year × Site</th></tr></thead><tbody><tr><td rowspan="3">Low-input</td><td><i>Fusarium</i></td><td>Box-Cox+1</td><td>140.03</td><td>0.66</td><td>216.46***</td><td>22.67***</td><td>22.15***</td><td>/</td><td>4.39***</td></tr><tr><td><i>Epicoccum</i></td><td>log<sub>10</sub>+1</td><td>129.40</td><td>0.64</td><td>371.00***</td><td>16.68***</td><td>8.30***</td><td>/</td><td>8.92***</td></tr><tr><td><i>Alternaria</i></td><td>none</td><td>120.74</td><td>0.62</td><td>854.01***</td><td>15.62***</td><td>0.80n.s.</td><td>/</td><td>6.63***</td></tr><tr><td rowspan="3">Organic</td><td><i>Fusarium</i></td><td>log<sub>10</sub>+1</td><td>167.79</td><td>0.77</td><td>48.06***</td><td>18.78***</td><td>6.65*</td><td>/</td><td>5.71***</td></tr><tr><td><i>Epicoccum</i></td><td>log<sub>10</sub>+1</td><td>101.37</td><td>0.62</td><td>95.68***</td><td>19.03***</td><td>1.74n.s.</td><td>/</td><td>6.36***</td></tr><tr><td><i>Alternaria</i></td><td>none</td><td>279.47</td><td>0.92</td><td>519.28***</td><td>66.46***</td><td>2.54n.s.</td><td>2.94**</td><td>14.66***</td></tr></tbody></table>

295

Discussion

296

297 This long-term study focusing on the incidence of four fungal genera on bread wheat grain over
298 a 13-year period in several sites on hundred samples collected in both conventional low-input
299 and organic farming conditions led to conclude two general trends.

300 First, the incidence of the genus *Fusarium* in bread wheat grains was generally low to nil, both
301 in low-input and organic farming conditions, as observed in previous studies (Lazzaro et al.
302 2015; Lenc 2015). In the vast majority of situations studied, the genus *Alternaria* was dominant
303 on wheat grain, while the other genera studied were generally few or not observed, except in
304 atypical years, sometimes only in one site. In our case, these particular results could be
305 explained by meteorological conditions favourable to the development of fungal genera
306 associated with maize as preceding crop (van der Velde et al. 2020), as also observed in other
307 studies during part of the period considered here (Giraud et al. 2010; Chandelier et al. 2011). It
308 should be noted that in 2008 in low-input conditions in Brittany, i.e., 1km away from the organic
309 trial characterized by a incidence near 50% of the genus *Fusarium*, considering a similar sowing
310 period but faba bean as preceding crop, the incidence of *Fusarium* was under 5%.

311 Second, the main explanatory factors of the incidence of fungi on wheat grain, independently
312 of the genus and the farming conditions, were the year and the ‘year × site’ interaction, while
313 the site and the genotype were less explanatory. These results appear consistent with the trends
314 observed on the graphical representations, suggesting the dominant influence of the
315 environmental conditions of the year and the site on the relative development of the fungal
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