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Article

Weeds in Cereal Crop Rotations May Host Fusarium Species That Cause Fusarium Head Blight and Grain Weight Losses in Wheat

by
Neringa Matelionienė
1,
Skaidrė Supronienė
1,
Arman Shamshitov
1,
Evelina Zavtrikovienė
1,
Sigita Janavičienė
2 and
Gražina Kadžienė
3,*
1
Microbiology Laboratory, Institute of Agriculture, Lithuanian Research Centre for Agriculture and Forestry, Instituto al. 1, Akademija, LT-58344 Kėdainiai, Lithuania
2
Department of Plant Pathology and Protection, Institute of Agriculture, Lithuanian Research Centre for Agriculture and Forestry, Instituto al. 1, Akademija, LT-58344 Kėdainiai, Lithuania
3
Department of Soil and Crop Management, Institute of Agriculture, Lithuanian Research Centre for Agriculture and Forestry, Instituto al. 1, Akademija, LT-58344 Kėdainiai, Lithuania
*
Author to whom correspondence should be addressed.
Agronomy 2022, 12(11), 2741; https://doi.org/10.3390/agronomy12112741
Submission received: 23 September 2022 / Revised: 31 October 2022 / Accepted: 1 November 2022 / Published: 4 November 2022
(This article belongs to the Special Issue Plant Production and Microorganism Potential in Modern Agro-Ecosystems)
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Abstract

:
Fusarium Head Blight (FHB) is one of the most common worldwide wheat and other small grain diseases. The infection is caused by Fusarium graminearum and other related species, which significantly reduce grain yield and contaminate grains with mycotoxins which are harmful for humans and animals. Fusarium pathogen survives the winter well in plant debris left on the field. Weeds around and within crops are alternative hosts of Fusarium fungi when an economically important host plant is not present. This article focuses on the determination of DNA content of Fusarium species (F. graminearum and F. avenaceum) in artificially inoculated wheat plants with isolates from weeds, as well as its influence on the severity of FHB and spring wheat 1000-grain weight under field conditions. Fungal DNA content in grains was evaluated by quantitative real-time PCR. The results showed that the DNA concentration of F. graminearum was significantly higher in the grain than F. avenaceum. The severity of FHB when wheat heads were inoculated with F. graminearum was significantly higher than with F. avenaceum. All F. graminearum strains statistically significantly reduced the weight of spring wheat grains, while F. avenaceum did not affect the weight of 1000 grain. This investigation has shown that weeds in crop rotations are a potential source of FHB infection. However, the severity of the disease is more affected by the Fusarium species than the host plant. This experiment is, to our knowledge, the first report on the estimation of Fusarium DNA content in artificially inoculated wheat plants with isolates from weeds, as well as its comparison with pathogenicity to wheat and its effect on 1000-grain weight.

1. Introduction

Fusarium Head Blight (FHB) is currently one of the most important diseases, caused primarily by Fusarium graminearum sensu stricto [1], affecting wheat, barley, and other small grain cereal crops [2,3]. The disease causes yield and quality losses and seriously threatens animal and human health due to grains contaminated with mycotoxins [4,5,6]. The most crucial small grain cereals contaminants are trichothecenes, primarily deoxynivalenol (DON), which has been proven to be the most common mycotoxin related to FHB [7,8,9,10]. Thus, managing FHB epidemics in wheat is essential for reducing mycotoxin contamination, minimizing yield losses, and ensuring the safety of both animal and human food. The most common species in Europe are F. graminearum, Fusarium culmorum, Fusarium poae, and Fusarium avenaceum [11,12]. The F. graminearum and F. avenaceum species have also sexually produced ascospores, while other species produce only asexual conidia. Macroconidia are reported to be splash-dispersed at short distances, while sexual spores can be transported for long distances by wind [11].
Sometimes, Fusarium species are present in complex and may interact synergistically, influencing disease development and mycotoxin production. Apart from that, the coincidence of wet and warm environments during wheat flowering and seed filling intensifies the risk of the FHB epidemic [1,13]. However, the impact of weather conditions also depends on the origin of the Fusarium species isolate [14]. In addition, the occurrence of the disease depends on rates of residue decomposition, inoculum production and spreading, crop rotations, temperature, moisture, and carbon dioxide concentration (CO2).
One of the main sources of inoculum is colonized crop debris. The Fusarium pathogen colonizes weeds or other non-cultivated plant species external to crop fields as alternative hosts, usually when the economically significant host plant is not present [15,16,17]. It is worth noticing that sixteen different Fusarium species infect a range of alternative hosts and lead to FHB [18]. The literature usually refers to the fact that isolates of plant pathogens recovered from weeds can be more pathogenic than isolates from cultivated plants [15]. Several previous studies have recovered F. graminearum pathogen from inflorescences of healthy weed plants in Argentina [19], Turkey [20], and Croatia [21], as well as from wild grasses in the USA [22] and Canada [23,24]. F. avenaceum and F. graminearum have repeatedly been reported as non-symptomatic wild grass species colonizers [25,26,27]. Most authors note that the collected weed samples did not show symptoms of FHB, meaning that isolated Fusarium species might exist in weeds as endophytes [15,21].
Over the past decades, F. graminearum has caused significant economic losses to the wheat industry due to an epidemic caused by FHB [18,28]. The identification of F. graminearum, its pathogenicity mechanisms, and its potential inoculum sources has been extensively studied in recent years in order to control the disease. Often, FHB management strategies integrated with chemical fungicides, agronomic practices (e.g., crop rotation), and herbicides fail to reduce the spread of the disease.
The current study aimed to determine the pathogenicity of two Fusarium species (F. graminearum and F. avenaceum) isolated from asymptomatic weeds to spring wheat. More Fusarium species (F. culmorum, F. poae, F. equiseti, F. oxysporum, F. tricinctum, F. redolens, F. sporotrichioides) have been isolated from weeds in previous authors’ research [17]. The most common species are F. graminearum and F. avenaceum, which cause FHB to wheat in Lithuania [29,30]. In addition, both F. graminearum and F. avenaceum have a sexual stage, and ascospores produced at this stage can serve as the main source of spore dispersion when transported long distances by wind [11]. In our study, we used the quantitative real-time PCR (qPCR) method to assess the fungal DNA in grain harvested from wheat. qPCR has enabled the reliability of detection of numerous Fusarium pathogens within plant tissues due to its sensitivity and accuracy. Several studies have used quantitative methods for reporting fungal DNA content to examine F. graminearum [14,31] and F. avenaceum [32] colonization of hosts. However, most studies have focused on the occurrence of Fusarium species in alternative non-cultivated plants or comparing Fusarium DNA content in wheat with toxins accumulation in grain. Therefore, to our knowledge, this study is the first to investigate the DNA content of different strains of F. graminearum and F. avenaceum species isolated from weeds in infected wheat, and to compare it with the severity of FHB and 1000-grain weight.
Finally, it is valuable to understand all possible infection sources, especially weeds’ role in FHB epidemics, which might help to improve the disease’s management. In addition, there is limited information on the pathogenicity and impact of Fusarium species that colonize weeds on FHB disease severity. In order to supplement the knowledge in this field, the present study provides a qualitative and quantitative evaluation of Fusarium fungi isolated from weeds in wheat grains by real-time PCR, and the influence of the evaluated fungal DNA content in grains on the severity of FHB and weight of 1000 spring wheat grain.

2. Materials and Methods

2.1. Isolate Collection

Heads of spring wheat cultivar ‘KWS Chamsin’ were inoculated with the most common Fusarium species (F. avenaceum and F. graminearum sensu stricto), isolated from the internal tissues of asymptomatic weeds. Isolates originated from the hosts Viola arvensis, Fallopia convolvulus, Poa annua, Capsella bursa-pastoris, and Tripleurospermum inodorum randomly collected from three different agricultural fields in the central part of Lithuania in the Kedainiai district [33].

2.2. Pathogenicity Test

The pathogenicity of F. graminearum and F. avenaceum isolates, obtained from weeds, to spring wheat was tested in a field experiment conducted at the Institute of Agriculture, Lithuanian Research Centre for Agriculture and Forestry in 2019. In this study, the pathogenicity of Fusarium strains was assessed based on fungal DNA content in grain. We compared the pathogenicity of Fusarium strains isolated from the main (spring wheat ‘KWS Collada,’ Germany) and alternative host plants (weeds) to spring wheat within each Fusarium species. The incidence and severity of FHB caused by Fusarium fungi were assessed 7, 14, and 21 days after inoculation (DAI). All inoculated plants were evaluated. The incidence of FHB is shown as the number of heads affected by the disease, expressed as a percentage. Disease severity (DS), expressed in the percentage of bleached spikelets, was evaluated based on a scale described by Engle et al. [34]. In this study, we used only the mean DS values of the 21st DAI for comparison with the DNA content of Fusarium fungi estimated by the quantitative real-time PCR method.

2.3. Spring Wheat Head Inoculation under Field Condition

The wheat head inoculation procedure was performed as described by Suproniene et al. [33]. The pathogenicity of 12 F. graminearum and 12 F. avenaceum isolates (2 isolates from each host species), obtained from asymptomatic weeds Capsella bursa-pastoris, Fallopia convolvulus, Poa annua, Tripleurospermum inodorum, Viola arvensis, and symptomatic Triticum aestivum (spring type), was tested. The study scheme is presented in Table 1.
Eighty heads from four different places were spray-inoculated on 17 June with each fungal strain, accounting for four replications (20 heads per replication). The pathogenicity test included 25 treatments (12 F. graminearum and 12 F. avenaceum isolates + 1 negative control) × 20 heads × 4 replicates = 2000 heads per experiment. Assessment of F. graminearum and F. avenaceum pathogenicity to spring wheat utilized conidial suspension at a concentration of 1 × 105 CFU ml−1. Inoculated heads and the water-treated control were immediately covered with plastic bags to ensure sufficient humidity conditions; these were removed after three days.

2.4. Determination of 1000 Grains Weight

The weight of the grain was estimated at the complete ripening stage on 29 July. Each bundle of 20 wheat heads (one replication) was cut with secateurs and packed in a paper bag, indicating the date, treatment, and replication number. The grain was threshed using a laboratory single ear thresher (Precision Machine model WHTA010002, Precision Machine Co., Inc., Lincoln, NE, USA), packed in small paper bags, and stored in a dry room for up to two weeks until grain analysis was performed. The total number of grains and the weight of the grains from twenty heads were determined. The weight of 1000 grains was then calculated. Grain samples were packed in frost-resistant plastic containers and stored at −20 °C until milling.

2.5. Grain Homogenization

Grains were roughly milled using a Retsch M 301 (Retsch, Haan, Germany) grinder. 10 g of each grain sample was poured into stainless steel containers, along with two 7-mm-diameter steel balls. The containers were frozen for 5 min in liquid nitrogen. After removing from the nitrogen, the setting was fixed in the mill’s special holders, and shaken for 4 min at 30,000 rpm. Then, the samples were stored in plastic bags at −20 °C until DNA extraction.

2.6. DNA Extraction, Fungal DNA Content Determination

DNA was extracted from 100 mg of grain powder using the commercial ZR Fungal/Bacterial DNA MiniPrep Kit (Zymo Research, Irvine, CA, USA), following the manufacturer’s instructions. DNA concentration and quality were determined using a BioPhotometer® D30 (Eppendorf, Hamburg, Germany) and stored at −20 °C until use.

2.7. Molecular Identification and RT-PCR

The amplification was performed using a thermocycler 7900HT Sequence Detection system (Applied Biosystems, Waltham, MA, USA), using the translation elongation factor 1α primers: FgramB379 and FgramB411; Fave574 and Fave627; wheat plant Hor1 and Hor2 (Table 2). Each PCR assay was performed in a 12.5 μL mixture comprising 6.3 μL of Power SYBR ® Green PCR Master Mix (ThermoFisher Scientific, Vilnius, Lithuania) 0.3 μL of each primer, 0.5 μg/μL of bovine serum albumin (bovine serum albumin—BSA, Thermo Fisher Scientific, Vilnius, Lithuania), 2.7 μL of ddH2O, and 2.5 μL of DNA template. Genomic DNA from grain samples was diluted 1:10. PCR was performed using the following cycling parameters: for 2 min at 50 °C (denaturation), for 10 min at 95 °C (annealing), and extension for 15 s at 95 °C and for 1 min at 62 °C, followed by 40 cycles. Sequencing of tef1α (=eEF1 α a, translation elongation factor 1- α) gene amplicons was carried out for four F. graminearum strains—WB-544r, WB-144r, FP-541s, FP-153l, which matches with codes 544r, 144r, 541s, 153l, as described by Suproniene et al. [33]. All F. graminearum strains belong to F. graminearum sensu stricto, as well as the other 36 F. graminearum strains obtained from weeds in the previous study. The rest of the F. graminearum and F. avenaceum used in the current study was identified by species-specific PCR, as described by Suproniene et al. [17,33].

2.8. Fusarium spp. DNA Content Quantification

The F. graminearum and F. avenaceum DNA content in spring wheat grain were analyzed using quantitative real-time PCR, following the method described by Nicolaisen et al. [35]. Standard curves for the two Fusarium species and wheat were made of a sixfold dilution series (dilution ratio 1:10) using fungal and wheat DNA with known DNA concentration, determined using NanoDrop 1000 (Thermo Scientific, Wilmington, DE, USA) from pure cultures. The content of F. graminearum and F. avenaceum DNA was calculated using the standard curve from the cycle threshold (Ct) values. Amplification results of each sample from each species-specific assay were evaluated by studying the dissociation curve and the Ct value. The wheat plant assay was further used to provide a normalized measurement for DNA content in each sample, which was expressed as picograms of Fusarium DNA per microgram of plant DNA, according to Nicolaisen et al. [35].

2.9. Statistical Analysis

Fusarium DNA content, FHB severity, and 1000-grain weight were statistically evaluated, and calculations were performed in Microsoft Office Excel 2007. Arithmetic averages (Xv), mean square deviations (S), correlation coefficients (r), standard error of the mean (SEM), and reliability (p) were calculated. Research data were processed by the method of univariate analysis of variance, using the statistical program ANOVA and Tukey’s Means Separation Test (p = 0.05). The correlation coefficients between mean Fusarium DNA content, FHB severity, and weight of 1000 grains were explored by Pearson correlation tests. The Microsoft Office Excel 2007 program was used to present the data graphically.

3. Results

3.1. F. graminearum and F. avenaceum DNA Content Identification in Grains

After determining the concentration of DNA of the main FHB pathogens (F. graminearum sensu stricto and F. avenaceum) in grain by qPCR, the results showed that the highest concentration of F. avenaceum DNA (52.1 pg/µg) was found in grain inoculated with F. avenaceum which was isolated from the wild buckwheat strain WB-1180l, which was statistically significantly different from the control. Comparatively less (26.6 and 23.6 pg/µg) DNA of this fungus was found in grains inoculated with F. avenaceum strains SFM-1118c and FP-1109s, which were isolated from the scentless false mayweed and field pansy, respectively. When spring wheat species were inoculated with strains of F. avenaceum from meadow grass (MG-1126s), shepherd’s purse (SP-1149c and SP-1101fl), and scentless false mayweed (SFM-1143s), the DNA content did not differ, showing similar results (19–20 pg/µg). The lowest concentration of F. avenaceum DNA content (6.2 pg/µg) was found in grain inoculated with the SW-TG5 strain, whose host plant was spring wheat. In addition, a similar concentration (7.3 pg/µg) was found in grain inoculated with the meadow grass MG-1128f strain. Minimal quantities of F. avenaceum DNA (0.002–0.42 pg/µg) were found in grains inoculated with different strains of the F. graminearum species (Figure 1).
In contrast, F. graminearum DNA content in spring wheat grain was found in significantly higher quantities than F. avenaceum. The highest concentration of the F. graminearum pathogen (2068.34 and 1277.347 pg/µg) was found in spring wheat grains inoculated with the F. graminearum SW-6K4V1 and SW-6K5V1 strains, isolated from the main host plants (spring wheat), which were the most statistically significantly different from the control (Figure 2). In addition, a high concentration of F. graminearum DNA (1126 pg/µg) was found in spring wheat inoculated with the WB-544r strain which was isolated from wild buckwheat. The DNA content of the other F. graminearum strains, FP-541s and FP-153l, which were isolated from field pansy, and strain SFM-1265f, from the scentless false mayweed, was found in grain in similar quantities (770–840 pg/plant DNA µg), which differed significantly from the control, but did not differ between these treatments.
The lowest F. graminearum DNA content (194.8 pg/µg) was found in wheat inoculated with the MG-90c strain, which was isolated from meadow grass. In addition, minimal quantities of F. graminearum (0.253–17.233 pg/µg) were found in treatments where wheat heads were inoculated with different F. avenaceum strains. These treatments indicate natural F. graminearum infection from the environment.

3.2. Pathogenicity of Fusarium Strains from Alternative (Weed) and Main Host (Wheat) to Spring Wheat

The visual pathogenicity test was used to examine the effect of F. graminearum and F. avenaceum isolates from different host plants (weeds and wheat) on the severity of FHB of spring wheat.
The disease severity was higher in wheat inoculated with F. graminearum strains than with F. avenaceum (Figure 3). Each isolate caused different disease severities at 21 DAI, ranging from 53.6% to 84.1% in spring wheat inoculated with F. graminearum and 1.1% to 27.2% in wheat inoculated with F. avenaceum (Figure 4).
The highest severity of FHB was found in wheat inoculated with the F. graminearum FP-153l strain (84%) isolated from field pansy, which was statistically significantly the most aggressive compared to the water control. A similar disease severity (83%) was observed when wheat was inoculated with the SW-6K4V1 strain isolated from spring wheat. The lowest severity (53%) of the disease caused by F. graminearum was found in wheat inoculated with the F. graminearum WB-144r strain isolated from wild buckwheat, which was less aggressive than the strains isolated from field pansy. Based on the results of FHB disease severity and fungal DNA content, we confirmed that isolates of F. graminearum were significantly more aggressive than those of F. avenaceum in spring wheat.

3.3. Effect of Fusarium Strains Isolated from Alternative (Weeds) and Main (Wheat) Host Plants on Grain Weight

The grain weight was statistically significantly different in all F. graminearum treatments compared to the control. The infection of the F. graminearum strain SW-6K4V1 on inoculated heads reduced the average of 1000-grain weight almost twice, compared with water treatment (Figure 5).
The results reveal that the isolate from the alternative host plant field pansy (FP-153l) reduced grain weight, similarly to the isolate from the main host plant, spring wheat, which was the SW-6K5V1 strain. Likewise, the Fusarium graminearum isolate FP-153l from field pansy reduced the grain weight more significantly than the FP-541s strain. On the other hand, the weight of grain inoculated with F. graminearum strains from scentless false mayweed statistically differed from spring wheat F. graminearum strains. In both cases, significant statistical differences were observed, confirming variable degrees of grain weight reduction in the wheat plants artificially inoculated with F. graminearum strains.
After testing the 1000-grain weight of spring wheat inoculated with F. avenaceum strains, the results did not show a decrease in grain weight in most cases. Figure 5 illustrates that there were no significant differences between the F. avenaceum strains of scentless false mayweed (SFM-1118c), field pansy (FP-1109s), shepherd’s purse (SP-1101fl), meadow grass (MG-1126s), and control. Interestingly, the F. avenaceum isolates from wheat (SW-G1 and SW-TG5) partially significantly increased grain weight compared to the control. Wheat inoculated with strains obtained from scentless false mayweed (SFM-1143s) and meadow grass (MG-1128f) showed slight 1000-grain weight reduction, and only the strain from wild buckwheat (WB-1178fl) showed a significant effect. These results indicate that the F. avenaceum species does not significantly affect grain weight, unlike F. graminearum.

3.4. Correlation Determination between the DNA Content of Fusarium Strains, Fusarium Head Blight Intensity, and Spring Wheat 1000-Grain Weight

Pearson correlation tests were used in order to determine the relationships between the Fusarium DNA content, FHB severity, and weight of 1000 grains. The relationship between the F. avenaceum DNA content in grain and the severity of FHB was negatively correlated (−0.682) (Table 3). This correlation may have been a false negative, due to the random collection of wheat heads and grain size in these test variants and controls. The results show that F. avenaceum did not significantly affect the grain weight, and the increased weight compared to the control was simply a coincidence. However, this was attributed to a very low concentration of F. avenaceum DNA, which did not affect the pathogenicity. In our view, it could be caused by the artificial infection of the F. graminearum species. In contrast, a strong significant linear relationship (0.791) was found between F. graminearum DNA content in spring wheat grain and disease severity. It indicates that F. graminearum is a potent pathogen for wheat.
The correlation between Fusarium species DNA content and 1000 spring wheat grain weight was used to determine the influence of fungal DNA content on 1000-grain weight. As expected, results showed that the correlation between F. graminearum and 1000-grain weight was strongly negative (−0.808). Contrary to expectations, the relationship between F. avenaceum DNA content and 1000-grain weight were positively correlated (0.686). It is likely that a small concentration of F. avenaceum DNA and artificial F. graminearum infection from the environment may have led to a positive relationship.
In order to compare the relationships between visual pathogenicity and fungal DNA content with 1000-grain weight, we determined the correlation between FHB severity and 1000-grain weight. The results showed a statistically reliable, significantly (p < 0.001) negative, and very strong (−0.910) correlation. While F. graminearum DNA content had a slightly weaker negative correlation with grain weight (−0.808) than disease severity with grain weight (−0.910), this indicates that in this situation, the visual evaluation method was more accurate in assessing the negative effects of Fusarium fungi on spring wheat.
The results of Fusarium DNA content and pathogenicity (FHB severity) on spring wheat with F. graminearum and F. avenaceum isolates from weeds are summarized in Table 4.

3.5. Weather Conditions

The meteorological conditions during spring wheat inoculation with Fusarium strains and grain threshing were described using data from the Dotnuva Hydrometeorological station, Kedainiai district, Lithuania (Figure 6). Climatic conditions mainly influenced plant pathogenic fungi. A wet and warm environment during wheat flowering and seed filling increased the risk of FHB disease.
Spring wheat heads were inoculated on 17 June, when warm weather prevailed. The inoculation date was characterized by the fixed temperature at 22.5 °C and humidity at 85%, which was 25% higher than average for the rest of the month. After three days, it rained; the precipitation of the day was 5.2 mm. However, the average precipitation for the entire month was low. The average air temperature in June was 20.1 °C, with a humidity of 60.5%. The warmest day was on 26 June, when the temperature rose to 31.6 °C. The coldest night occurred on 29 June, when the air temperature dropped to 8.5 °C. In July, until the head collection day (29 July), the average air temperature was fixed at 17.4 °C, close to the long-term average, and the average air humidity was 70%. This month’s highest temperature reached 29.8 °C, while the lowest temperature fell to 8.4 °C. Rainfall in July was unevenly distributed, with a monthly total of 66 mm (86% of the long-term average). Heavy rains were recorded on 16 July and 22 July, on which 19.6 mm and 22 mm of rain fell. On 29 July, head harvesting day, it was hot, without rain.

4. Discussion

Weeds growing in cereal and other crop fields show the ability to act as alternative host plants for pathogens of the Fusarium species. As mentioned by Postic et al. [15], weeds often become a source of pathogens when there is no significant host plant around. According to the study conducted by Suproniene et al. [33], the main FHB causing Fusarium species—F. graminearum in weed tissues in Lithuania was isolated from a total of 41 different weed species out of 57 tested. Another common Fusarium species, F. avenaceum, colonizes many plants and can cause FHB disease in wheat. In our study, two species of Fusarium, isolated from five weed species tissues (Fallopia convolvulus, Poa annua, Capsella bursa-pastoris, Viola arvensis, and Tripleurospermum inodorum), and spring wheat were selected for comparison. None of the analyzed weed species presented symptoms of Fusarium infection on host plants, in agreement with previous reports [19,36]. All collected portions of the weed were surface sterilized to remove superficial organisms, assuming Fusarium spp. is growing from colonized host tissues [23,37]. Twelve F. graminearum and 12 F. avenaceum strains were tested for pathogenicity on spring wheat. The results revealed that all F. graminearum isolates were determined to be pathogenic, and visual FHB disease severity varied between 53 and 84%. In comparison, F. avenaceum strains did not cause significant FHB severity. It is essential to mention that no previous study has compared the DNA content of Fusarium strains isolated from different host plants (weeds and wheat) with the severity of the disease and the weight of 1000 grains.
The role of alternative host plants in pathogen evolution and FHB disease in wheat is still not widely understood. Several authors have recovered F. graminearum and other species [19,24,25,38], including F. avenaceum, from the tissues of many weeds under natural conditions [15,23]. Inch and Gilbert [23] observed that only F. graminearum species was isolated from wild grasses (Agropyron repens, Agropyron trachycaulum, Agrostis stolonifera, Bromus inermis, Calamagrostis canadensis, and Echinocloa crusgalli) in June, while in mid-August, seven species of Fusarium were isolated; among them was the aforementioned F. avenaceum species (found only in B. inermis). This fact explains the influence of climatic conditions on the predominance of different fungi [39]. The author also noted that no Fusarium species was detected in 16 grass species, including Poa annua. Meanwhile, in our investigation, strains of F. graminearum isolated from this weed species caused relatively high FHB severity. It is worth noticing that all tested weed species were previously cited as hosts of F. graminearum in Argentina [19], Lithuania [33,40], England [38], and Croatia [15].
Determination of F. avenaceum and F. graminearum DNA content in grains showed that the highest concentration of F. avenaceum DNA was found in wheats inoculated with the F. avenaceum WB-1180l strain, which was isolated from wild buckwheat. The wheat inoculated with the strain SW-TG5, whose host plant was spring wheat, contained the least DNA of this species. In comparison, F. graminearum DNA was found in significantly higher concentrations in grain than F. avenaceum. Likewise, the highest concentration of F. graminearum DNA was found when wheat was inoculated with the F. graminearum SW-6K4V1 strain isolated from spring wheat tissues, while the lowest DNA concentration was measured in wheats inoculated with the MG-90c strain from meadow grass. In addition, the concentration of F. graminearum DNA in wheat infected with the SW-6K5V1 and WB-544r strains from spring wheat and wild buckwheat was not statistically significantly different. Detection of high F. graminearum DNA concentration in wheat may indicate that this species more easily colonizes cultivated plants and weeds than F. avenaceum does. This is partly due to the lack of structural barriers to Fusarium pathogen gene flow, which is uninhibited between wheat and weed plants [41]. Our results also reveal that the lower DNA content of F. graminearum in wheat induced more severe FHB disease, similar to the findings of Hay and others [14].
Temperature and humidity during wheat flowering and seed filling are major factors affecting the development of Fusarium species. According to Parikka et al. [42], temperatures close to 25 °C with high humidity favour F. graminearum infections in grain, while for F. avenaceum, the optimum is 20 °C and moist conditions in late summer. In our situation, the average air temperature in June was slightly higher (20.1 °C) than in July (17.4 °C). These weather conditions are more optimal for F. avenaceum species development in wheat, according to the authors mentioned above. However, higher DNA content and FHB severity caused by F. graminearum showed the opposite results. Our results agree with the findings of Hay and others [14] that F. graminearum DNA accumulation in wheat depends on temperature. For instance, cool growing conditions (20 °C/18 °C day/night) resulted in the highest concentrations of DNA in inoculated wheat, while at warm temperatures (25 °C/23 °C), despite reduced DNA content, the fungal pathogen was more aggressive, with greater disease severity. In addition, the high humidity after inoculation may cause a greater development of this Fusarium species.
Based on the results of FHB disease severity and fungal DNA content, we confirmed that isolates of F. graminearum were significantly more aggressive than those of F. avenaceum in spring wheat. The F. graminearum is a very important pathogen in Lithuania [33], and is one of the main agents causing FHB disease in Europe [43,44]. The pathogenicity test confirmed that all F. graminearum isolates from host plants were able to develop head blight symptoms with different disease severity. The highest disease severity (84%) was found in wheat heads inoculated with the F. graminearum FP-153l strain, which was isolated from field pansy; similar disease severity was observed with the SW-6K4V1 strain, isolated from spring wheat. Meanwhile, the highest disease severity caused by F. avenaceum (27%) was found in wheat inoculated with the WB-1178fl strain, isolated from wild buckwheat. Postic’s [15] hypothesis that the pathogenicity of Fusarium strains from weed tissues can be more pathogenic to wheat plants was confirmed in our case. The pathogenicity of the strains isolated from this weed significantly differed from the other isolates. Other F. avenaceum isolates did not have a strong significant effect on disease intensity. The obtained data show that weeds spread in cereal crop rotations are a potential source of wheat head blight and disease severity, depending more on the Fusarium species and the specific strain than the host plant of the pathogen.
The study on the influence of Fusarium strains on grain weight showed that all tested F. graminearum strains statistically reliably reduced spring wheat grain weight, compared to the control variant. The most significant influence was found for strain SW-6K4V1, isolated from spring wheat, in which inoculated wheat grains weighed two times less than in the control variant. This is consistent with the findings of Twamley et al. [45], where F. graminearum infection in inoculated wheat heads reduced grain weight per head by 65%. However, the 1000-grain weight of spring wheat inoculated with F. avenaceum strains did not show a decrease in grain weight. This indicates that F. avenaceum, in our case, did not significantly affect 1000-grain weight in contrast to F. graminearum, and the host plant affects the pathogenicity of these species less significantly.
Based on the results of the correlations, we found that the DNA content of F. graminearum positively correlated with FHB disease severity, which was evaluated visually, and negatively correlated with 1000-grain weight. These findings are similar to previous results from Goral [30]. He determined the positive correlation between F. graminearum DNA content and the FHB index. Palazzini‘s [46] study also showed that DNA content increases exponentially with the severity of the wheat head disease. They observed maximum disease severity in wheat heads by 35%, corresponding to an average of 5675 pg DNA. This is similar to our results, which show a strong positive correlation between disease severity of the heads and F. graminearum DNA content in grains. In our experiments, F. graminearum infection reduced spring wheat’s 1000-grain weight from 22% to 46% compared with the control. These results confirmed F. graminearum’s pathogenicity to wheat and its influence on grain weight. Despite this fact, the determination of F. avenaceum’s DNA concentration did not reflect the effect of the pathogen on grain weight, and the relationship with FHB severity was insignificant. These findings are in contradiction with previous results by Xue et al. [47], Vogelgsang et al. [48], and Mesterha’zy et al. [49], who reported F. avenaceum as a pathogenic fungus on wheat, causing FHB disease, decreasing yields, and contaminating grain with trichothecene mycotoxins. Abdellatif et al. [50] noted that the variation in virulence within F. avenaceum isolates ranged from high to avirulent in wheat, and it depends on the climate characteristics of each agricultural region. In our case, F. avenaceum DNA content positively correlated with grain weight and FHB severity. Perhaps this was due to unfavorable climatic conditions for the development of this pathogen, which led to low DNA content and weak spread of the disease, and therefore did not affect grain weight. In addition, F. graminearum DNA content had a slightly weaker negative correlation with grain weight than disease severity with grain weight; this shows that the visual head blight disease evaluation method was more accurate.

5. Conclusions

This study showed that (i) all F. graminearum isolates (regardless of host plant) were determined as pathogenic, while F. avenaceum isolates did not have a strong significant effect on disease severity and 1000-grain weight; (ii) the positive significant correlation between F. graminearum DNA content in grain and FHB severity confirmed the aggressiveness of this species; (iii) F. graminearum infection reduced spring wheat grain weight from 22% to 46%. These findings may be useful for understanding the non-cultivated plants, such as the role of weeds in FHB epidemiology, and for the developing tillage practices to note special attention to weeds growing in crops in order to reduce the amount of inoculum. It is essential to mention that this study was conducted over only one year, and weather conditions during wheat anthesis could affect results. Understanding the influence of meteorological conditions on the severity of FHB will require further research.

Author Contributions

Conceptualization, S.S. and G.K.; methodology, S.S., G.K., N.M., E.Z. and S.J.; validation, N.M., S.S. and G.K.; formal analysis, N.M.; investigation, S.S., G.K., N.M., E.Z. and S.J.; data curation, N.M.; writing—original draft preparation, N.M.; writing—review and editing, S.S., G.K., S.J., E.Z. and A.S.; visualization, N.M. and S.J.; supervision, S.S. and G.K. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Data Availability Statement

Not applicable.

Acknowledgments

This study was supported by the long-term research program ‘Harmful Organisms in Agro and Forest Ecosystems’ implemented by Lithuanian Research Centre for Agriculture and Forestry.

Conflicts of Interest

The authors declare no conflict of interest.

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Agronomy 12 02741 g001 550
Figure 1. The DNA content of the pathogen F. avenaceum (F. avenaceum DNA pg/plant DNA µg) (±SEM) in spring wheat grains inoculated with different strains of F. avenaceum and F. graminearum from alternative host weeds and the main host wheat (values with different letters (a–f) indicate statistically significant differences (p < 0.05) between study treatments, C—water inoculated control).
Figure 1. The DNA content of the pathogen F. avenaceum (F. avenaceum DNA pg/plant DNA µg) (±SEM) in spring wheat grains inoculated with different strains of F. avenaceum and F. graminearum from alternative host weeds and the main host wheat (values with different letters (a–f) indicate statistically significant differences (p < 0.05) between study treatments, C—water inoculated control).
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Figure 2. The DNA content of the pathogen F. graminearum (F. graminearum DNA pg/plant DNA µg) (±SEM) in spring wheat grains inoculated with different strains of F. avenaceum and F. graminearum from alternative host weeds and the main host wheat (values with different letters (a–f) indicate statistically significant differences (p < 0.05) between study variants, C—water inoculated control).
Figure 2. The DNA content of the pathogen F. graminearum (F. graminearum DNA pg/plant DNA µg) (±SEM) in spring wheat grains inoculated with different strains of F. avenaceum and F. graminearum from alternative host weeds and the main host wheat (values with different letters (a–f) indicate statistically significant differences (p < 0.05) between study variants, C—water inoculated control).
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Figure 3. Spring wheat heads with signs of Fusarium head blight infection caused by F. avenaceum (on the right) and F. graminearum (on the left).
Figure 3. Spring wheat heads with signs of Fusarium head blight infection caused by F. avenaceum (on the right) and F. graminearum (on the left).
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Figure 4. Fusarium head blight severity (FHB) in spring wheat heads inoculated with Fusarium isolates from weed and wheat (the percentage of FHB severity (±SEM) was calculated from the average of the four replications (20 heads per replication) inoculated wheat heads at 21 DPI. (Different letters (a–i) above the bars indicate statistically significant differences (p < 0.05) between study treatments. C—water inoculated control).
Figure 4. Fusarium head blight severity (FHB) in spring wheat heads inoculated with Fusarium isolates from weed and wheat (the percentage of FHB severity (±SEM) was calculated from the average of the four replications (20 heads per replication) inoculated wheat heads at 21 DPI. (Different letters (a–i) above the bars indicate statistically significant differences (p < 0.05) between study treatments. C—water inoculated control).
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Figure 5. Average 1000-grain weight of spring wheat inoculated with different Fusarium strains isolated from alternative (weeds) and main (wheat) host plants (1000-grain weight was calculated based on the weight and number of grains per 20 heads). (Different letters above bars indicate significant (p ≤ 0.05) differences (a–k) within the control treatment and Fusarium strain inoculated treatments, and error bars indicate ±SEM. C—water inoculated control).
Figure 5. Average 1000-grain weight of spring wheat inoculated with different Fusarium strains isolated from alternative (weeds) and main (wheat) host plants (1000-grain weight was calculated based on the weight and number of grains per 20 heads). (Different letters above bars indicate significant (p ≤ 0.05) differences (a–k) within the control treatment and Fusarium strain inoculated treatments, and error bars indicate ±SEM. C—water inoculated control).
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Figure 6. Meteorological observations after wheat inoculation day.
Figure 6. Meteorological observations after wheat inoculation day.
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Table
Table 1. The study scheme.
Table 1. The study scheme.
Treatment No.Host PlantF. avenaceum
Strain Code		F. graminearum
Strain Code
1Spring wheat
(Triticum aestivum)		SW-G1SW-6K5V1
2SW-TG5SW-6K4V1
3Wild buckwheat
(Fallopia convolvulus)		WB-1180lWB-544r
4WB-1178flWB-144r
5Meadow grass
(Poa annua)		MG-1128fMG-161r
6MG-1126sMG-90c
7Shepherd’s purse
(Capsella bursa-pastoris)		SP-1149cSP-1400l
8SP-1101flSP-1151f
9Field pansy
(Viola arvensis)		FP-1110fFP-541s
10FP-1109sFP-153l
11Scentless false mayweed
(Tripleurospermum inodorum)		SFM-1143sSFM-1265f
12SFM-1118cSFM-1120c
13ControlSterile distilled water
SW = spring wheat, WB = wild buckwheat, MG = meadow grass, SP = shepherd’s purse, FP = field pansy, SFM = scentless false mayweed. c, f, fl, l, r, s—isolate obtained from crown (c), fruit (f), flower (fl), leaf (l), root (r), stem (s).
Table
Table 2. Sequences and names of species-specific primers.
Table 2. Sequences and names of species-specific primers.
TargetPrimer NameSequence (5′–3′)Literature Source
F. graminearumFgramB379 fwdCCATTCCCTGGGCGCT[35]
FgramB411 revCCTATTGACAGGTGGTTAGTGACTGG
F. avenaceumFave574 fwdTATGTTGTCACTGTCTCACACCACC
Fave627 revAGAGGGATGTTAGCATGATGAAG
Plant EF1αHor1fwdTCTCTGGGTTTGAGGGTGAC
Hor2revGGCCCTTGTACCAGTCAAGGT
Table
Table 3. Correlations between FHB severity (FHBs), 1000-grain weight and different (F. avenaceum and F. graminearum) fungal DNA content in wheat grains.
Table 3. Correlations between FHB severity (FHBs), 1000-grain weight and different (F. avenaceum and F. graminearum) fungal DNA content in wheat grains.
Variables (n = 25)FHBs (%)1000-Grain Weight (g)
F. avenaceum DNA content (pg/ng)−0.682 **0.686 **
F. graminearum DNA content (pg/ng)0.791 **−0.808 **
FHBs (%) −0.910 **
** values are significant at the 0.01 level.
Table
Table 4. The relative concentration of DNA of the fungus F. avenaceum and F. graminearum (pg Fusarium spp. DNA/µg plant DNA) in spring wheat grains inoculated with F. avenaceum and F. graminearum strains, fusarium head blight severity (FHBs), and 1000 grains weight of spring wheat. Values with letters (a–i) indicate statistically significant differences (p < 0.05) between study variants.
Table 4. The relative concentration of DNA of the fungus F. avenaceum and F. graminearum (pg Fusarium spp. DNA/µg plant DNA) in spring wheat grains inoculated with F. avenaceum and F. graminearum strains, fusarium head blight severity (FHBs), and 1000 grains weight of spring wheat. Values with letters (a–i) indicate statistically significant differences (p < 0.05) between study variants.
Host PlantNo.StrainDNA Content of F. avenaceumDNA Content of F. graminearumFHBs (%)1000-Grain Weight (g)
F. graminearumSpring wheat
(Triticum aestivum)		1SW-6K5V10.007 a1277,374 e64.8 def17.3 ab
2SW-6K4V10.010 a2068.344 f83.4 hi15.9 a
Wild buckwheat
(Fallopia convolvulus)		3WB-544r0.022 a1126.426 e66.0 defg18.6 abcd
4WB-144r0.004 a743.660 bcde53.6 d21.4 de
Meadow grass
(Poa annua)		5MG-161r0.002 a406.922 abcd76.3 fghi17.6 abcd
6MG-90c0.004 a194.898 ab69.0 efg20.0 bcde
Shepherd’s purse
(Capsella bursa-pastoris)		7SP-1400l0.010 a909.203 de78.5 ghi20.0 bcde
8SP-1151f0.049 a410.992 abcd57.9 de20.6 cde
Field pansy
(Viola arvensis)		9FP-541s0.015 a770.917 cde67.0 efg21.4 de
10FP-153l0.002 a839.418 cde84.1 hi17.8 abc
Scentless false mayweed
(Tripleurospermum inodorum)		11SFM-1265f0.050 a815.719 cde72.1 fghi23.0 ef
12SFM-1120c0.423 a348.702 abc71.3 fghi22.8 ef
F. avenaceumSpring wheat
(Triticum aestivum)		13SW-G1-II11.846 bcd0.566 a7.5 ab34.0 k
14SW-TG5-IV6.201 ab0.414 a10.8 ab30.2 i
Wild buckwheat
(Fallopia convolvulus)		15WB-1180l52.153 f5.860 a14.3 b31.2 ijk
16WB-1178fl12.374 bcd0.253 a27.2 c25.0 fg
Meadow grass
(Poa annua)		17MG-1128f7.311 abc0.291 a3.5 ab26.6 gh
18MG-1126s19.860 de2.995 a4.9 ab28.4 hi
Shepherd’s purse
(Capsella bursa-pastoris)		19SP-1149c19.029 de0.334 a1.2 a31.3 ijk
20SP-1101fl20.374 de2.092 a1.7 a28.5 hi
Field pansy
(Viola arvensis)		21FP-1110f17.313 cde17.233 a1.8 a30.2 i
22FP-1109s23.574 e1.682 a2.4 ab29.3 hi
Scentless false mayweed
(Tripleurospermum inodorum)		23SFM-1143s19.536 de6.724 a1.4 a26.1 fgh
24SFM-1118c26.618 e0.381 a1.1 a28.4 hi
ControlH2O25-0.014 a0.593 a0.4 a29.4 hi
SW = spring wheat, WB = wild buckwheat, MG = meadow grass, SP = shepherd’s purse, FP = field pansy, SFM = scentless false mayweed. c, f, fl, l, r, s—isolate obtained from crown (c), fruit (f), flower (fl), leaf (l), root (r), stem (s).
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Matelionienė, N.; Supronienė, S.; Shamshitov, A.; Zavtrikovienė, E.; Janavičienė, S.; Kadžienė, G. Weeds in Cereal Crop Rotations May Host Fusarium Species That Cause Fusarium Head Blight and Grain Weight Losses in Wheat. Agronomy 2022, 12, 2741. https://doi.org/10.3390/agronomy12112741

AMA Style

Matelionienė N, Supronienė S, Shamshitov A, Zavtrikovienė E, Janavičienė S, Kadžienė G. Weeds in Cereal Crop Rotations May Host Fusarium Species That Cause Fusarium Head Blight and Grain Weight Losses in Wheat. Agronomy. 2022; 12(11):2741. https://doi.org/10.3390/agronomy12112741

Chicago/Turabian Style

Matelionienė, Neringa, Skaidrė Supronienė, Arman Shamshitov, Evelina Zavtrikovienė, Sigita Janavičienė, and Gražina Kadžienė. 2022. "Weeds in Cereal Crop Rotations May Host Fusarium Species That Cause Fusarium Head Blight and Grain Weight Losses in Wheat" Agronomy 12, no. 11: 2741. https://doi.org/10.3390/agronomy12112741

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