<?xml version="1.0" encoding="UTF-8"?>
<!DOCTYPE article PUBLIC "-//NLM//DTD JATS (Z39.96) Journal Publishing DTD v1.1 20151215//EN" "http://jats.nlm.nih.gov/publishing/1.1/JATS-journalpublishing1.dtd">
<article xmlns:xlink="http://www.w3.org/1999/xlink" xmlns:mml="http://www.w3.org/1998/Math/MathML" xml:lang="en" article-type="research-article" dtd-version="1.1">
<front>
<journal-meta>
<journal-id journal-id-type="pmc">Phyton</journal-id>
<journal-id journal-id-type="nlm-ta">Phyton</journal-id>
<journal-id journal-id-type="publisher-id">Phyton</journal-id>
<journal-title-group>
<journal-title>Phyton-International Journal of Experimental Botany</journal-title>
</journal-title-group>
<issn pub-type="epub">1851-5657</issn>
<issn pub-type="ppub">0031-9457</issn>
<publisher>
<publisher-name>Tech Science Press</publisher-name>
<publisher-loc>USA</publisher-loc>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="publisher-id">56982</article-id>
<article-id pub-id-type="doi">10.32604/phyton.2024.056982</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Article</subject>
</subj-group>
</article-categories>
<title-group>
<article-title>Aggressiveness Assessment of Two <italic>Fusarium</italic> spp. on Durum Wheat Grain Coleoptiles under Controlled Conditions</article-title><alt-title alt-title-type="left-running-head">Aggressiveness Assessment of Two Fusarium spp. on Durum Wheat Grain Coleoptiles under Controlled Conditions</alt-title><alt-title alt-title-type="right-running-head">Aggressiveness Assessment of Two Fusarium spp. on Durum Wheat Grain Coleoptiles under Controlled Conditions</alt-title>
</title-group>
<contrib-group>
<contrib id="author-1" contrib-type="author" corresp="yes">
<name name-style="western"><surname>Hadjout</surname><given-names>Salah</given-names></name>
<xref ref-type="aff" rid="aff-1">1</xref>
<xref ref-type="aff" rid="aff-2">2</xref><email>hadjout.salah@gmail.com</email>
</contrib>
<contrib id="author-2" contrib-type="author">
<name name-style="western"><surname>Zouidi</surname><given-names>Mohamed</given-names></name>
<xref ref-type="aff" rid="aff-1">1</xref>
</contrib>
<contrib id="author-3" contrib-type="author">
<name name-style="western"><surname>Bougrine</surname><given-names>Houcine</given-names></name>
<xref ref-type="aff" rid="aff-1">1</xref>
</contrib>
<contrib id="author-4" contrib-type="author">
<name name-style="western"><surname>Belkendil</surname><given-names>Abdeldjalil</given-names></name>
<xref ref-type="aff" rid="aff-1">1</xref>
</contrib>
<contrib id="author-5" contrib-type="author">
<name name-style="western"><surname>Zeghmar</surname><given-names>Amer</given-names></name>
<xref ref-type="aff" rid="aff-1">1</xref>
</contrib>
<contrib id="author-6" contrib-type="author">
<name name-style="western"><surname>Ouaret</surname><given-names>Walid</given-names></name>
<xref ref-type="aff" rid="aff-3">3</xref>
</contrib>
<contrib id="author-7" contrib-type="author">
<name name-style="western"><surname>Soufan</surname><given-names>Walid</given-names></name>
<xref ref-type="aff" rid="aff-4">4</xref>
</contrib>
<contrib id="author-8" contrib-type="author">
<name name-style="western"><surname>Belhouadjeb</surname><given-names>Fathi Abdellatif</given-names></name>
<xref ref-type="aff" rid="aff-5">5</xref>
</contrib>
<aff id="aff-1"><label>1</label><institution>Centre de Recherche en Am&#x00E9;nagement du Territoire (CRAT), Campus Zouaghi Slimane, Route de Ain el Bey</institution>, <addr-line>Constantine, 25000</addr-line>, <country>Alg&#x00E9;rie</country></aff>
<aff id="aff-2"><label>2</label><institution>Ecole Nationale Sup&#x00E9;rieure Agronomique (ENSA)</institution>, <addr-line>Alger, 16200</addr-line>, <country>Alg&#x00E9;rie</country></aff>
<aff id="aff-3"><label>3</label><institution>Department of Geographical Sciences, University of Maryland</institution>, <addr-line>College Park, MD 20742</addr-line>, <country>USA</country></aff>
<aff id="aff-4"><label>4</label><institution>Plant Production Department, College of Food and Agriculture Sciences, King Saud University</institution>, <addr-line>Riyadh, 11451</addr-line>, <country>Saudi Arabia</country></aff>
<aff id="aff-5"><label>5</label><institution>Centre de Recherche en Agropastoralisme (CRAPast)</institution>, <addr-line>Djelfa, 17000, Alg&#x00E9;rie</addr-line></aff>
</contrib-group><author-notes><corresp id="cor1"><label>&#x002A;</label>Corresponding Author: Salah Hadjout. Email: <email>hadjout.salah@gmail.com</email></corresp></author-notes>
<pub-date date-type="collection" publication-format="electronic">
<year>2024</year>
</pub-date>
<pub-date date-type="pub" publication-format="electronic">
<day>30</day><month>11</month><year>2024</year>
</pub-date>
<volume>93</volume>
<issue>11</issue>
<fpage>2983</fpage>
<lpage>2992</lpage>
<history>
<date date-type="received"><day>04</day><month>8</month><year>2024</year></date>
<date date-type="accepted"><day>21</day><month>10</month><year>2024</year></date>
</history>
<permissions>
<copyright-statement>&#x00A9; 2024 The Authors.</copyright-statement>
<copyright-year>2024</copyright-year>
<copyright-holder>Published by Tech Science Press.</copyright-holder>
<license xlink:href="https://creativecommons.org/licenses/by/4.0/">
<license-p>This work is licensed under a <ext-link ext-link-type="uri" xlink:type="simple" xlink:href="https://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution 4.0 International License</ext-link>, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.</license-p>
</license>
</permissions>
<self-uri content-type="pdf" xlink:href="TSP_Phyton_56982.pdf"></self-uri>
<abstract>
<p>Fusarium head blight (FHB) is a disease caused by several <italic>Fusarium</italic> species, notably, <italic>F. culmorum</italic> and <italic>F. graminearum</italic>. These pathogens adversely affect the technological and sanitary qualities of cereal grains, particularly durum wheat. Under favorable environmental conditions and in susceptible varieties, these <italic>Fusarium</italic> species can significantly reduce both the quantity and quality of crops. This study evaluated the pathogenicity of the two <italic>Fusarium</italic> species (FC2006 and FG2008) in the growth of durum wheat coleoptiles. The plant material included four commercially grown parental varieties (G9, G10, G11, G12) and eight breeding lines (G1, G2, G3, G4, G5, G6, G7, G8). <italic>In vitro</italic> tests revealed that both <italic>Fusarium</italic> species significantly reduced the coleoptile growth across the studied varieties and lines (<italic>p</italic> &#x2264; 0.001). The control test had an average coleoptile length of 37.87 mm. In contrast, seeds inoculated with FC2006 had an average length of 0.62 mm, and those inoculated with FG2008 had only 0.064 mm. Although there was a slight difference in aggressiveness between the two species, it was not statistically significant (<italic>p</italic> &#x003E; 0.05). Some variability was also noted in the responses of the durum wheat varieties and lines. The G8 genotype showed remarkable behavior in both isolates, with an average length of 1.83 mm for FC2006 and 0.4 mm for FG2008. The other genotypes showed total inhibition of coleoptile growth (0 mm). These findings highlight the importance of conducting further research on the defense mechanisms of durum wheat against <italic>Fusarium</italic> and assessing the local varieties&#x2019; pathogenicity to better explore the interactions between these pathogens and durum wheat genotypes under <italic>in vitro</italic> conditions.</p>
</abstract>
<kwd-group kwd-group-type="author">
<kwd><italic>Fusarium</italic> species</kwd>
<kwd>aggressiveness</kwd>
<kwd>coleoptile growth</kwd>
<kwd>durum wheat</kwd>
<kwd><italic>in vitro</italic> test</kwd>
</kwd-group>
<funding-group>
<award-group id="awg1">
<funding-source>King Saud University, Riyadh, Saudi Arabia</funding-source>
<award-id>RSP2024R390</award-id>
</award-group>
</funding-group>
</article-meta>
</front>
<body>
<sec id="s1">
<label>1</label>
<title>Introduction</title>
<p>Cereal crops are cultivated over an estimated 3.3 million hectares annually, with 1.5 million hectares of durum wheat and 600.000 hectares of soft wheat. The total cereal production in Algeria is approximately 4 million tons, with bread wheat contributing only 1% of the overall harvest [<xref ref-type="bibr" rid="ref-1">1</xref>]. Durum wheat (<italic>Triticum turgidum</italic> var. durum) is the most widely grown cereal crop in the Mediterranean basin, and ranks as the tenth most cultivated species globally [<xref ref-type="bibr" rid="ref-2">2</xref>]. This cereal is a main crop and staple food in certain Mediterranean regions, serving as an essential raw material for finished products such as pasta, couscous, bulgur, and various types of bread, consumed worldwide [<xref ref-type="bibr" rid="ref-3">3</xref>]. In Algeria, wheat has long been the primary dietary staple for consumers [<xref ref-type="bibr" rid="ref-4">4</xref>], and globally, it is the third most harvested crop and the most consumed grain [<xref ref-type="bibr" rid="ref-5">5</xref>].</p>
<p>However, wheat production is affected by severe abiotic factors, including drought, irregular rainfall, frost, extreme temperatures, and increased atmospheric CO<sub>2</sub> levels, all of which can drastically reduce yield and grain quality [<xref ref-type="bibr" rid="ref-6">6</xref>,<xref ref-type="bibr" rid="ref-7">7</xref>]. Additionally, plant diseases caused by pathogenic fungi are prevalent and can lead to significant losses in yield, as well as a decline in grain quality [<xref ref-type="bibr" rid="ref-8">8</xref>,<xref ref-type="bibr" rid="ref-9">9</xref>]. Fusarium head blight (FHB) is one of the most destructive fungal diseases affecting durum wheat, causing yield reductions of up to 61%. FHB is characterized by flower abortion, reduction in grain number and weight, and deterioration of grain quality due to the accumulation of harmful mycotoxins in the grain [<xref ref-type="bibr" rid="ref-10">10</xref>&#x2013;<xref ref-type="bibr" rid="ref-12">12</xref>]. Consequently, FHB is a major threat to cereal production worldwide with significant economic implications [<xref ref-type="bibr" rid="ref-10">10</xref>].</p>
<p>The <italic>Fusarium</italic> genus is recognized as one of the most pathogenic and aggressive fungal groups, comprising multiple species that infect a wide range of cultivated plants and cereals, many of which are essential for both human and animal nutrition, some of them causing FHB [<xref ref-type="bibr" rid="ref-10">10</xref>]. Key targets of <italic>Fusarium</italic> infection include leaves, roots, stems, heads, and crop residues [<xref ref-type="bibr" rid="ref-13">13</xref>,<xref ref-type="bibr" rid="ref-14">14</xref>]. In recent years, several studies have been conducted in Algeria to identify specific <italic>Fusarium</italic> species involved in FHB in wheat [<xref ref-type="bibr" rid="ref-15">15</xref>&#x2013;<xref ref-type="bibr" rid="ref-17">17</xref>]. Using morphological and molecular techniques, these studies have confirmed that <italic>F. culmorum</italic> is the dominant species in durum wheat crops affected by FHB in the region [<xref ref-type="bibr" rid="ref-15">15</xref>,<xref ref-type="bibr" rid="ref-17">17</xref>,<xref ref-type="bibr" rid="ref-18">18</xref>]. Additionally, <italic>F. graminearum</italic> and <italic>F. pseudograminearum</italic>, have been identified, with <italic>F. cerealis</italic> being reported for the first time in Algeria [<xref ref-type="bibr" rid="ref-17">17</xref>]. Globally, <italic>F. graminearum</italic> and <italic>F. culmorum</italic> are the two most prevalent species responsible for root, stem, and ear rots, as well as seedling blight in small-grain cereals, including durum wheat [<xref ref-type="bibr" rid="ref-17">17</xref>,<xref ref-type="bibr" rid="ref-19">19</xref>,<xref ref-type="bibr" rid="ref-20">20</xref>].</p>
<p>The epidemiological cycle of <italic>Fusarium</italic> begins with the survival of the inoculum in the soil or on plant debris, where it persists as a saprophytic mycelium or thick-walled resting spores. When crops are sown in contaminated soils, diseases such as foot rot and seedling blight, can develop. During flowering, fungal infections can spread to wheat heads through conidia dispersed by rain splash or ascospores carried by the wind [<xref ref-type="bibr" rid="ref-21">21</xref>]. <italic>Fusarium</italic>-contaminated seeds further Cereal crops are cultivated over an estimated 3.3 million hectares annually, with 1.5 million hectares of durum wheat and 600.000 hectares of soft wheat. The total cereal production in Algeria is approximately 4 million tons, with bread wheat contributing only 1% of the overall harvest [<xref ref-type="bibr" rid="ref-1">1</xref>]. Durum wheat (<italic>Triticum turgidum</italic> var. durum) is the most widely grown cereal crop in the Mediterranean basin, and ranks as the tenth most cultivated species globally [<xref ref-type="bibr" rid="ref-2">2</xref>]. This cereal is a main crop and staple food in certain Mediterranean regions, serving as an essential raw material for finished products such as pasta, couscous, bulgur, and various types of bread, consumed worldwide [<xref ref-type="bibr" rid="ref-3">3</xref>]. In Algeria, wheat has long been the primary dietary staple for consumers [<xref ref-type="bibr" rid="ref-4">4</xref>], and globally, it is the third most harvested crop and the most consumed grain [<xref ref-type="bibr" rid="ref-5">5</xref>].</p>
<p>However, wheat production is affected by severe abiotic factors, including drought, irregular rainfall, frost, extreme temperatures, and increased atmospheric CO<sub>2</sub> levels, all of which can drastically reduce yield and grain quality [<xref ref-type="bibr" rid="ref-6">6</xref>,<xref ref-type="bibr" rid="ref-7">7</xref>]. Additionally, plant diseases caused by pathogenic fungi are prevalent and can lead to significant losses in yield, as well as a decline in grain quality [<xref ref-type="bibr" rid="ref-8">8</xref>,<xref ref-type="bibr" rid="ref-9">9</xref>]. Fusarium head blight (FHB) is one of the most destructive fungal diseases affecting durum wheat, causing yield reductions of up to 61%. FHB is characterized by flower abortion, reduction in grain number and weight, and deterioration of grain quality due to the accumulation of harmful mycotoxins in the grain [<xref ref-type="bibr" rid="ref-10">10</xref>&#x2013;<xref ref-type="bibr" rid="ref-12">12</xref>]. Consequently, FHB is a major threat to cereal production worldwide with significant economic implications [<xref ref-type="bibr" rid="ref-10">10</xref>].</p>
<p>The <italic>Fusarium</italic> genus is recognized as one of the most pathogenic and aggressive fungal groups, comprising multiple species that infect a wide range of cultivated plants and cereals, many of which are essential for both human and animal nutrition, some of them causing FHB [<xref ref-type="bibr" rid="ref-10">10</xref>]. Key targets of <italic>Fusarium</italic> infection include leaves, roots, stems, heads, and crop residues [<xref ref-type="bibr" rid="ref-13">13</xref>,<xref ref-type="bibr" rid="ref-14">14</xref>]. In recent years, several studies have been conducted in Algeria to identify specific <italic>Fusarium</italic> species involved in FHB in wheat [<xref ref-type="bibr" rid="ref-15">15</xref>&#x2013;<xref ref-type="bibr" rid="ref-17">17</xref>]. Using morphological and molecular techniques, these studies have confirmed that <italic>F. culmorum</italic> is the dominant species in durum wheat crops affected by FHB in the region [<xref ref-type="bibr" rid="ref-15">15</xref>,<xref ref-type="bibr" rid="ref-17">17</xref>,<xref ref-type="bibr" rid="ref-18">18</xref>]. Additionally, <italic>F. graminearum</italic> and <italic>F. pseudograminearum</italic>, have been identified, with <italic>F. cerealis</italic> being reported for the first time in Algeria [<xref ref-type="bibr" rid="ref-17">17</xref>]. Globally, <italic>F. graminearum</italic> and <italic>F. culmorum</italic> are the two most prevalent species responsible for root, stem, and ear rots, as well as seedling blight in small-grain cereals, including durum wheat [<xref ref-type="bibr" rid="ref-17">17</xref>&#x2013;<xref ref-type="bibr" rid="ref-20">20</xref>].</p>
<p>The epidemiological cycle of <italic>Fusarium</italic> begins with the survival of the inoculum in the soil or on plant debris, where it persists as a saprophytic mycelium or thick-walled resting spores. When crops are sown in contaminated soils, diseases such as foot rot and seedling blight can develop. During flowering, fungal infections can spread to wheat heads through conidia dispersed by rain splash or ascospores carried by the wind [<xref ref-type="bibr" rid="ref-21">21</xref>]. The use of <italic>Fusarium</italic>-contaminated seeds and further exacerbates the disease cycle by providing the primary inoculum for the development of FHB and foot rot [<xref ref-type="bibr" rid="ref-22">22</xref>]. The presence of <italic>Fusarium</italic> in seed lots can significantly reduce the germination capacity, resulting in lower emergence rates and seedling blight after germination [<xref ref-type="bibr" rid="ref-23">23</xref>]. Even seeds with healthy, viable embryos may fail to germinate or produce normal seedlings owing to fungal contamination during the germination process [<xref ref-type="bibr" rid="ref-21">21</xref>]. Previous studies have demonstrated that high <italic>Fusarium</italic> aggressiveness is associated with a marked reduction in germination rates, elevated Area Under Disease Progression Curve (AUDPC) values, and a significant decrease in coleoptile length [<xref ref-type="bibr" rid="ref-24">24</xref>].</p>
<p>The present study aimed to evaluate the pathogenicity of <italic>Fusarium culmorum</italic> and <italic>Fusarium graminearum</italic> isolates on durum wheat coleoptile growth while identifying response variations between different varieties and lines. Objectives include measuring the impact of isolates on coleoptile length, comparing the aggressiveness of the two species on the tested genotypes, and analyzing the variability of genotype responses to identify those with increased tolerance or susceptibility. Finally, this research aims to provide useful data for future studies on the management of fusarium head blight under controlled conditions.</p>
</sec>
<sec id="s2">
<label>2</label>
<title>Material and Methods</title>
<sec id="s2_1">
<label>2.1</label>
<title>Plant Material</title>
<p>In this study, we used four parental durum wheat varieties: Ardente, Waha, Simeto, and Vitron (<xref ref-type="table" rid="table-1">Table 1</xref>). Additionally, we included eight breeding lines derived from F15 seeds, which were produced through diallel crosses involving five parental varieties: Ardente, Waha, Simeto, Vitron, and Saadi [<xref ref-type="bibr" rid="ref-25">25</xref>]. The seeds of these lines, used as experimental material, were obtained in June 2011 from plots managed by the Higher National School of Agronomy (ENSA), within the Plant Production Department.</p>
<table-wrap id="table-1"><label>Table 1</label>
<caption>
<title>F15 genealogical lines and parental varieties of durum wheat used in the study</title></caption>
<table><colgroup>
<col/>
<col/>
<col/>
</colgroup>
<thead>
<tr>
<th colspan="2">Lines and varieties</th>
<th>Code</th>
</tr>
</thead>
<tbody>
<tr>
<td rowspan="8"><bold>Lines</bold></td>
<td>Saadi &#x00D7; Waha 431</td>
<td>G1</td>
</tr>
<tr>
<td>Ardente &#x00D7; Waha 423</td>
<td>G2</td>
</tr>
<tr>
<td>Ardente &#x00D7; Waha 221</td>
<td>G3</td>
</tr>
<tr>
<td>Ardente &#x00D7; Simeto 133</td>
<td>G4</td>
</tr>
<tr>
<td>Ardente &#x00D7; Simeto 151</td>
<td>G5</td>
</tr>
<tr>
<td>Ardente &#x00D7; Simeto 164</td>
<td>G6</td>
</tr>
<tr>
<td>Simeto &#x00D7; Vitron 113</td>
<td>G7</td>
</tr>
<tr>
<td>Simeto &#x00D7; Waha 311</td>
<td>G8</td>
</tr>
<tr>
<td rowspan="4"><bold>Varieties</bold></td>
<td>Simeto</td>
<td>G9</td>
</tr>
<tr>
<td>Ardente</td>
<td>G10</td>
</tr>
<tr>
<td>Waha</td>
<td>G11</td>
</tr>
<tr>
<td>Vitron</td>
<td>G12</td>
</tr>
</tbody>
</table>
</table-wrap>
</sec>
<sec id="s2_2">
<label>2.2</label>
<title>Fungal Material</title>
<p>The pathogenic fungal material that was subjected to <italic>in vitro</italic> test consisted of two <italic>Fusarium</italic> isolates, FG2008 and FC2006, belonging to <italic>F. graminearum</italic> and <italic>F. culmorum</italic> species, respectively. These isolates were identified using a combination of morphological observations of mycelia growth on Potato Dextrose Agar (PDA) and microscopic examination of conidia, following the method described by Leslie et al. [<xref ref-type="bibr" rid="ref-26">26</xref>]. Species identification was further confirmed by PCR, using species-specific primers [<xref ref-type="bibr" rid="ref-15">15</xref>,<xref ref-type="bibr" rid="ref-17">17</xref>].</p>
<p>Both isolates were sourced from the mycological collection of the ENSA in El-Harrach, Algiers. The FG2008 isolate was obtained from soft wheat spikelets collected at the ITGC experimental station (Technical Institute of Field Crops) in Algiers, in May 2008. The FC2006 isolate was derived from soft wheat spikelets harvested at the ENSA experimental station in El-Harrach, 2006. Both isolates were obtained from wheat ears displaying typical symptoms of FHB, such as pink to orange discoloration, indicative of significant spore mass formation.</p>
</sec>
<sec id="s2_3">
<label>2.3</label>
<title>In Vitro Pathogenicity Test on Durum Wheat Grains</title>
<p>The pathogenicity of the fungal isolates was evaluated according to a modified version of the protocol established by Mesterhazy [<xref ref-type="bibr" rid="ref-27">27</xref>] using PDA medium. Conidia, represented by mycelium post-conidial germination, were used to prepare the inocula. Conidial concentration and purity were controlled to ensure a consistent amount of inoculum for both species [<xref ref-type="bibr" rid="ref-9">9</xref>]. Mycelial mass was quantified using the method outlined by Brennan et al. [<xref ref-type="bibr" rid="ref-28">28</xref>].</p>
<p>To produce mycelia, 50 mL of Potato Dextrose Broth (PDB) was prepared. For each isolate, four 5-mm mycelial portions were obtained from 7-day-old cultures on PDA medium. These explants were added to PDB and incubated at 20&#x00B0;C on an orbital shaker at 250 rpm for seven days. After incubation, mycelia were harvested by centrifugation at 5000 &#x00D7; G for 10 min, homogenized, and diluted to a concentration of 13.3 mg/mL in a solution containing 0.2% Tween 20.</p>
<p>Petri dishes (85 mm in diameter) containing the PDA medium were prepared. A sterilized filter paper disk with the same diameter was placed on each PDA medium. Homogenized mycelia, diluted in 0.2% Tween 20, were applied evenly at a rate of 8 mL per dish. A second sterile filter paper disk was placed on the top of the inoculum. For each sample, 10 durum wheat grains were disinfected using 2% sodium hypochlorite for 10 min, rinsed thrice with sterile distilled water, and dried between two sterile blotting papers. These pre-disinfected grains were placed in Petri dishes. Plates containing grains inoculated with each <italic>Fusarium</italic> isolate were incubated in the dark at 25&#x00B0;C using a randomized design, with three replicates per isolate. Control plates were subjected to identical conditions, except that sterile distilled water was used instead of mycelial inoculum.</p>
<p>The growth of durum wheat coleoptiles was measured on the fourth day of incubation, and the results were expressed as differences in growth compared to the non-inoculated control.</p>
</sec>
<sec id="s2_4">
<label>2.4</label>
<title>Statistical Analysis</title>
<p>Statistical analysis of the results was performed using Statgraphics software version 15.1.0. Multiple comparisons of means were conducted using the Least Significant Difference (LSD) test at a 5% significance level to determine homogeneous groups.</p>
</sec>
</sec>
<sec id="s3">
<label>3</label>
<title>Results</title>
<p>To assess the impact of the two <italic>Fusarium</italic> isolates, FC2006 from <italic>Fusarium culmorum</italic> and FG2008 from <italic>Fusarium graminearum</italic>, on the growth of coleoptiles in 12 durum wheat genotypes, we developed an <italic>in vitro</italic> evaluation method under controlled laboratory conditions. This experimental approach enabled the precise measurement of the effects of the two isolates on coleoptile growth across different durum wheat varieties and breeding lines. This method provided a clear basis for comparing the differences in coleoptile growth after artificial inoculation with the two <italic>Fusarium</italic> species.</p>
<p>Coleoptile length was measured in millimeters after a 4-day incubation period at 25&#x00B0;C in the dark (<xref ref-type="fig" rid="fig-1">Fig. 1</xref>). To determine the level of aggressiveness of each <italic>Fusarium</italic> isolate on the different genotypes, coleoptile growth was compared with that of the uninoculated controls. The degree of reduction in coleoptile length was used to quantify the severity of the infection caused by the isolates.</p>
<fig id="fig-1">
<label>Figure 1</label>
<caption>
<title>Inhibition of seed germination by both <italic>Fusarium</italic> isolates after 4 days of incubation at 25&#x00B0;C and in darkness, illustrated with some representative images</title></caption>
<graphic mimetype="image" mime-subtype="tif" xlink:href="Phyton-93-56982-f001.tif"/>
</fig>
<p>As presented in <xref ref-type="fig" rid="fig-1">Fig. 1</xref>, coleoptile length was significantly reduced in grains inoculated with either of the <italic>Fusarium</italic> isolates compared to uninoculated controls. This reduction in growth highlights the inhibitory effect of the isolates on durum wheat coleoptiles, consistent with the known pathogenic characteristics of <italic>Fusarium</italic>. The observed inhibition is indicative of diseases, such as grain rot, which are common in infected plants and can lead to substantial economic losses in cereal production.</p>

<p>Statistical analysis of variance revealed that the effects of genotypes, treatments, and the interaction between genotypes and treatments on coleoptile length were highly significant (<italic>p</italic> &#x2264; 0.001). To further compare the mean coleoptile lengths across the three treatments (controls, genotypes inoculated with FC2006, and genotypes inoculated with FG2008), we conducted an LSD test. The test identified three homogeneous groups, with the control group having the longest average coleoptile length of 37.87 mm. By contrast, seeds inoculated with the FC2006 isolate had an average coleoptile length of 0.62 mm, while those inoculated with FG2008 exhibited the shortest average coleoptile length of 0.064 mm (<xref ref-type="fig" rid="fig-2">Fig. 2</xref>).</p>
<fig id="fig-2">
<label>Figure 2</label>
<caption>
<title>Mean coleoptile length of the three treatments after 4 days of incubation at 25&#x00B0;C and in the dark</title></caption>
<graphic mimetype="image" mime-subtype="tif" xlink:href="Phyton-93-56982-f002.tif"/>
</fig>
<p>The interaction between genotypes and treatments, analyzed using the LSD test, distinguished 10 homogeneous groups (<xref ref-type="fig" rid="fig-3">Fig. 3</xref>). The results indicated that the coleoptile growth in all genotypes inoculated with <italic>Fusarium</italic> isolates differed significantly from that of the uninoculated controls (<italic>p</italic> &#x2264; 0.001). In the control group, genotype G4 exhibited the longest coleoptile length at 44.50 mm, whereas G1 recorded the shortest length at 32.17 mm after 4 days of incubation.</p>
<fig id="fig-3">
<label>Figure 3</label>
<caption>
<title>Effect of three treatments on the average coleoptile length after 4 days of incubation at 25&#x00B0;C and in darkness</title></caption>
<graphic mimetype="image" mime-subtype="tif" xlink:href="Phyton-93-56982-f003.tif"/>
</fig>
<p>Among the genotypes inoculated with FC2006, genotype G8 displayed the longest average coleoptile length of 1.83 mm, while genotypes G1, G5, G7, and G11 showed complete inhibition of coleoptile growth, with an average length of 0 mm. Similarly, for the genotypes inoculated with FG2008, genotype G8 again had the highest average coleoptile growth, measuring 0.4 mm, while the other genotypes (G1, G2, G3, G4, G5, G6, G7, G9, G10, and G11) all exhibited total inhibition of coleoptile growth with an average length of 0 mm (<xref ref-type="fig" rid="fig-3">Fig. 3</xref>). Interestingly, these results revealed that several genotypes exhibited complete inhibition of coleoptile growth following inoculation with both FC2006 and FG2008 isolates.</p>
</sec>
<sec id="s4">
<label>4</label>
<title>Discussion</title>
<p>Coleoptiles are conical structures that emerge from seeds and develop into leaves when exposed to light and moisture, making their length a critical indicator for early growth, wheat breeding, and plant development [<xref ref-type="bibr" rid="ref-29">29</xref>,<xref ref-type="bibr" rid="ref-30">30</xref>]. In this study, inoculation of durum wheat grains with <italic>Fusarium</italic> isolates was aimed at evaluating the aggressiveness of the fungi in inhibiting coleoptile growth in different durum wheat varieties andbreeding lines. The observed growth inhibition confirms that both <italic>F. culmorum</italic> and <italic>F. graminearum</italic> fungi have detrimental effects on seed germination and subsequent coleoptile development. Notably, a slight difference in aggressiveness was detected between the two isolates, with <italic>F. graminearum</italic> (FG2008) exhibiting slightly higher aggressiveness than <italic>F. culmorum</italic> (FC2006).</p>
<p>Our findings align with those of previous research, which identified <italic>F. culmorum</italic> and <italic>F. graminearum</italic> as among the most aggressive pathogens affecting the coleoptile growth of wheat and barley [<xref ref-type="bibr" rid="ref-28">28</xref>,<xref ref-type="bibr" rid="ref-31">31</xref>]. Reduced germination rates and shorter coleoptile lengths are commonly used as key indicators of fungal aggressiveness, particularly in <italic>F. graminearum</italic> [<xref ref-type="bibr" rid="ref-24">24</xref>]. Brennan et al. [<xref ref-type="bibr" rid="ref-28">28</xref>] similarly reportedreport that both <italic>F. culmorum</italic> and <italic>F. graminearum</italic> exhibit optimal pathogenicity at temperatures between 20&#x00B0;C and 25&#x00B0;C, reducing coleoptile growth by over 89.3% compared to uninoculated controls. Their study further concluded that <italic>F. graminearum</italic> is a more aggressive species, reducing coleoptile growth by as much as 96% at 25&#x00B0;C, which is consistent with the findings of the present study.</p>
<p>Additional studies have reported that <italic>F. culmorum</italic> can reduce coleoptile length by up to 91.32%, whereas <italic>F. graminearum</italic> can cause a 78.32% reduction in growth [<xref ref-type="bibr" rid="ref-31">31</xref>]. Furthermore, <italic>in vitro</italic> seed inoculation test revealed that <italic>F. culmorum</italic> isolates can be highly aggressive, with some strains completely inhibiting coleoptile growth [<xref ref-type="bibr" rid="ref-16">16</xref>]. This extreme sensitivity to the initial infection was especially pronounced in durum wheat genotypes, where <italic>F. culmorum</italic> caused a significant reduction in germination rates. For example, the &#x201C;Hogar&#x201D; durum wheat variety experienced a 52.17% reduction in germination after just three days of inoculation [<xref ref-type="bibr" rid="ref-32">32</xref>].</p>
<p>Therefore, both <italic>F. culmorum</italic> and <italic>F. graminearum</italic> are regarded as highly aggressive pathogens, although their relative degrees of aggressiveness may vary depending on several factors. These include the type of host plant, environmental conditions, interactions with other microorganisms, and the genetic characteristics of the specific fungal isolates.</p>
<p>Other studies reported other <italic>Fusarium</italic> species (<italic>F. equiseti</italic>, <italic>F. chlamydosporum</italic>, <italic>F. poae</italic>, <italic>Microdochium nivale</italic>, <italic>F. verticillioides</italic> and <italic>F. solani</italic>) having negative effect on seed germination and coleoptile length in durum wheat, but with coleoptile length reduction variable depending on the fungal species and isolates [<xref ref-type="bibr" rid="ref-12">12</xref>,<xref ref-type="bibr" rid="ref-28">28</xref>,<xref ref-type="bibr" rid="ref-33">33</xref>,<xref ref-type="bibr" rid="ref-34">34</xref>].</p>
</sec>
<sec id="s5">
<label>5</label>
<title>Conclusion</title>
<p>This study examined the effects of two <italic>Fusarium</italic> isolates, <italic>F. culmorum</italic> (FC2006) and <italic>F. graminearum</italic> (FG2008), on coleoptile growth in different durum wheat genotypes. The results demonstrated that both isolates significantly inhibited coleoptile development across all genotypes tested, with wheat coleoptiles exposed to the fungi exhibiting markedly reduced growth compared to the controls. Moreover, there was a slight but notable difference in aggressiveness between the two isolates, with <italic>F. graminearum</italic> showing a marginally stronger inhibitory effect on coleoptile growth than <italic>F. culmorum</italic>.</p>
<p>These findings offer valuable insights for farmers and breeders in selecting wheat varieties that are more resistant to <italic>Fusarium</italic> infections. It is possible to mitigate the effect of <italic>Fusarium</italic> on crop yields by identifying varieties with increased resistance to these aggressive fungal species, ultimately enhancing the sustainability of wheat production in regions vulnerable to these pathogens.</p>
</sec>
</body>
<back>
<ack>
<p>The authors extend their appreciation to the Researchers Supporting Project number (RSP2024R390), King Saud University, Riyadh, Saudi Arabia, and to la Direction G&#x00E9;n&#x00E9;rale de la Recherche Scientifique et du D&#x00E9;veloppement Technologique (DGRSDT), Algeria.</p>
</ack>
<sec>
<title>Funding Statement</title>
<p>This Research was funded by la Direction G&#x00E9;n&#x00E9;rale de la Recherche Scientifique et du D&#x00E9;veloppement Technologique (DGRSDT), Algeria, and the Researchers Supporting Project number (RSP2024R390), King Saud University, Riyadh, Saudi Arabia.</p>
</sec>
<sec>
<title>Author Contributions</title>
<p>The authors confirm contribution to the paper as follows: study conception and design: Salah Hadjout, Fathi Abdellatif Belhouadjeb, Houcine Bougrine, Abdeldjalil Belkendil; data collection: Salah Hadjout, Mohamed Zouidi, Amer Zeghmar; analysis and interpretation of results: Salah Hadjout, Mohamed Zouidi, Walid Ouaret; draft manuscript preparation: Salah Hadjout, Mohamed Zouidi, Fathi Abdellatif Belhouadjeb, Walid Soufan. All authors reviewed the results and approved the final version of the manuscript.</p>
</sec>
<sec sec-type="data-availability">
<title>Availability of Data and Materials</title>
<p>Not applicable.</p>
</sec>
<sec>
<title>Ethics Approval</title>
<p>Not applicable.</p>
</sec>
<sec sec-type="COI-statement">
<title>Conflicts of Interest</title>
<p>The authors declare that they have no conflicts of interest to report regarding the present study.</p>
</sec>
<ref-list content-type="authoryear">
<title>References</title>
<ref id="ref-1"><label>1.</label><mixed-citation publication-type="other"><person-group person-group-type="author"><string-name><surname>Besaoud</surname> <given-names>O</given-names></string-name>, <string-name><surname>Pellissier</surname> <given-names>JP</given-names></string-name>, <string-name><surname>Rolland</surname> <given-names>JP</given-names></string-name>, <string-name><surname>Khechimi</surname> <given-names>W</given-names></string-name></person-group>. <article-title>Rapport de synth&#x00E8;se sur l&#x2019;agriculture en Alg&#x00E9;rie (Ph.D. Thesis). CIHEAM-IAMM de Montepellier: France</article-title>; <year>2019</year>.</mixed-citation></ref>
<ref id="ref-2"><label>2.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><string-name><surname>Chaouachi</surname> <given-names>L</given-names></string-name>, <string-name><surname>Mar&#x00ED;n-Sanz</surname> <given-names>M</given-names></string-name>, <string-name><surname>Barro</surname> <given-names>F</given-names></string-name>, <string-name><surname>Karmous</surname> <given-names>C</given-names></string-name></person-group>. <article-title>Genetic diversity of durum wheat (<italic>Triticum turgidum</italic> ssp. durum) to mitigate abiotic stress: drought, heat, and their combination</article-title>. <source>PLoS One</source>. <year>2024</year>;<volume>19</volume>:<fpage>e0301018</fpage>. doi:<pub-id pub-id-type="doi">10.1371/journal.pone.0301018</pub-id>; <pub-id pub-id-type="pmid">38574054</pub-id></mixed-citation></ref>
<ref id="ref-3"><label>3.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><string-name><surname>Blanco</surname> <given-names>A</given-names></string-name></person-group>. <article-title>Structure and trends of worldwide research on durum wheat by bibliographic mapping</article-title>. <source>Inter J Plant Biol</source>. <year>2024</year>;<volume>15</volume>(<issue>1</issue>):<fpage>132</fpage>&#x2013;<lpage>60</lpage>. doi:<pub-id pub-id-type="doi">10.3390/ijpb15010012</pub-id>.</mixed-citation></ref>
<ref id="ref-4"><label>4.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><string-name><surname>Bekkis</surname> <given-names>S</given-names></string-name>, <string-name><surname>Benmehaia</surname> <given-names>MA</given-names></string-name>, <string-name><surname>Kaci</surname> <given-names>A</given-names></string-name></person-group>. <article-title>Les enjeux de la d&#x00E9;pendance de la fili&#x00E8;re de bl&#x00E9; en Alg&#x00E9;rie: analyse par asym&#x00E9;tries de r&#x00E9;ponses de l&#x2019;offre dans la cha&#x00EE;ne de valeur</article-title>. <source>N Medit, A Medit J Eco, Agri and Env</source>. <year>2022</year>;<volume>21</volume>(<issue>1</issue>):<fpage>133</fpage>&#x2013;<lpage>47</lpage>. doi:<pub-id pub-id-type="doi">10.30682/nm2201h</pub-id>.</mixed-citation></ref>
<ref id="ref-5"><label>5.</label><mixed-citation publication-type="other"><person-group person-group-type="author"><string-name><surname>Nedjah</surname> <given-names>I</given-names></string-name></person-group>. <article-title>Changements physiologiques chez des plantes de bl&#x00E9; dur (<italic>Triticum durum</italic> Desf.) expos&#x00E9;es &#x00E0; une pollution par un m&#x00E9;tal lourd (plomb) (Ph.D. Thesis). Universit&#x00E9; Badji Mokhtar: Algerie</article-title>; <year>2015</year>.</mixed-citation></ref>
<ref id="ref-6"><label>6.</label><mixed-citation publication-type="conf-proc"><person-group person-group-type="author"><string-name><surname>Kalayc&#x0131;</surname> <given-names>M</given-names></string-name>, <string-name><surname>K&#x00FC;&#x00E7;&#x00FC;k&#x00F6;zdemir</surname> <given-names>&#x00DC;</given-names></string-name></person-group>. <article-title>Impact of abiotic stresses on wheat growth and adaptation</article-title>. In: <conf-name>Advances in wheat breeding: Towards climate resilience and nutrient security</conf-name>. <publisher-name>Springer</publisher-name>; <year>2024</year>. p. <fpage>183</fpage>&#x2013;<lpage>313</lpage>. doi:<pub-id pub-id-type="doi">10.1007/978-981-99-9478-6_4</pub-id>.</mixed-citation></ref>
<ref id="ref-7"><label>7.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><string-name><surname>Nyaupane</surname> <given-names>S</given-names></string-name>, <string-name><surname>Poudel</surname> <given-names>MR</given-names></string-name>, <string-name><surname>Panthi</surname> <given-names>B</given-names></string-name>, <string-name><surname>Dhakal</surname> <given-names>A</given-names></string-name>, <string-name><surname>Paudel</surname> <given-names>H</given-names></string-name>, <string-name><surname>Bhandari</surname> <given-names>R</given-names></string-name></person-group>. <article-title>Drought stress effect, tolerance, and management in wheat&#x2013;a review</article-title>. <source>Cog Food Agri</source>. <year>2024</year>;<volume>10</volume>(<issue>1</issue>):<fpage>2296094</fpage>. doi:<pub-id pub-id-type="doi">10.1080/23311932.2023.2296094</pub-id>.</mixed-citation></ref>
<ref id="ref-8"><label>8.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><string-name><surname>Haile</surname> <given-names>JK</given-names></string-name>, <string-name><surname>N&#x2019;Diaye</surname> <given-names>A</given-names></string-name>, <string-name><surname>Walkowiak</surname> <given-names>S</given-names></string-name>, <string-name><surname>Nilsen</surname> <given-names>KT</given-names></string-name>, <string-name><surname>Clarke</surname> <given-names>JM</given-names></string-name>, <string-name><surname>Kutcher</surname> <given-names>HR</given-names></string-name>, <etal>et al</etal></person-group>. <article-title>Fusarium head blight in durum wheat: recent status, breeding directions, and future research prospects</article-title>. <source>Phytopath</source>. <year>2019</year>;<volume>109</volume>(<issue>10</issue>):<fpage>1664</fpage>&#x2013;<lpage>75</lpage>. doi:<pub-id pub-id-type="doi">10.1094/PHYTO-03-19-0095-RVW</pub-id>; <pub-id pub-id-type="pmid">31369363</pub-id></mixed-citation></ref>
<ref id="ref-9"><label>9.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><string-name><surname>Hadjout</surname> <given-names>S</given-names></string-name>, <string-name><surname>Zouidi</surname> <given-names>M</given-names></string-name></person-group>. <article-title>Morphological and cultural characterization of two <italic>Fusarium</italic> isolates causing wheat fusarium head blight in Algeria</article-title>. <source>Not Scien Biol</source>. <year>2022</year>;<volume>14</volume>:<fpage>11318</fpage>. doi:<pub-id pub-id-type="doi">10.55779/nsb14411318</pub-id>.</mixed-citation></ref>
<ref id="ref-10"><label>10.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><string-name><surname>Shikur Gebremariam</surname> <given-names>E</given-names></string-name>, <string-name><surname>Sharma-Poudyal</surname> <given-names>D</given-names></string-name>, <string-name><surname>Paulitz</surname> <given-names>TC</given-names></string-name>, <string-name><surname>Erginbas-Orakci</surname> <given-names>G</given-names></string-name>, <string-name><surname>Karakaya</surname> <given-names>AZ&#x0130;Z</given-names></string-name>, <string-name><surname>Dababat</surname> <given-names>AA</given-names></string-name></person-group>. <article-title>Identity and pathogenicity of <italic>Fusarium</italic> species associated with crown rot on wheat (<italic>Triticum</italic> spp.) in Turkey</article-title>. <source>Eur J Plant Patho</source>. <year>2018</year>;<volume>150</volume>(<issue>2</issue>):<fpage>387</fpage>&#x2013;<lpage>99</lpage>. doi:<pub-id pub-id-type="doi">10.1007/s10658-017-1285-7</pub-id>.</mixed-citation></ref>
<ref id="ref-11"><label>11.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><string-name><surname>Beccari</surname> <given-names>G</given-names></string-name>, <string-name><surname>Senatore</surname> <given-names>MT</given-names></string-name>, <string-name><surname>Tini</surname> <given-names>F</given-names></string-name>, <string-name><surname>Sulyok</surname> <given-names>M</given-names></string-name>, <string-name><surname>Covarelli</surname> <given-names>L</given-names></string-name></person-group>. <article-title>Fungal community, Fusarium head blight complex and secondary metabolites associated with malting barley grains harvested in Umbria, central Italy</article-title>. <source>Inter J Food Microb</source>. <year>2018</year>;<volume>273</volume>:<fpage>33</fpage>&#x2013;<lpage>42</lpage>. doi:<pub-id pub-id-type="doi">10.1016/j.ijfoodmicro.2018.03.005</pub-id>; <pub-id pub-id-type="pmid">29574332</pub-id></mixed-citation></ref>
<ref id="ref-12"><label>12.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><string-name><surname>Bencheikh</surname> <given-names>A</given-names></string-name>, <string-name><surname>Rouag</surname> <given-names>N</given-names></string-name>, <string-name><surname>Mamache</surname> <given-names>W</given-names></string-name>, <string-name><surname>Belabed</surname> <given-names>I</given-names></string-name></person-group>. <article-title>First report of <italic>Fusarium equiseti</italic> causing crown rot and damping-off on durum wheat in Algeria</article-title>. <source>Arch Phytopath Plant Protect</source>. <year>2020</year>;<volume>53</volume>:<fpage>915</fpage>&#x2013;<lpage>31</lpage>. doi:<pub-id pub-id-type="doi">10.1080/03235408.2020.1804303</pub-id>.</mixed-citation></ref>
<ref id="ref-13"><label>13.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><string-name><surname>Karlsson</surname> <given-names>I</given-names></string-name>, <string-name><surname>Persson</surname> <given-names>P</given-names></string-name>, <string-name><surname>Friberg</surname> <given-names>H</given-names></string-name></person-group>. <article-title>Fusarium head blight from a microbiome perspective</article-title>. <source>Front Microb</source>. <year>2021</year>;<volume>12</volume>:<fpage>628373</fpage>. doi:<pub-id pub-id-type="doi">10.3389/fmicb.2021.628373</pub-id>; <pub-id pub-id-type="pmid">33732223</pub-id></mixed-citation></ref>
<ref id="ref-14"><label>14.</label><mixed-citation publication-type="book"><person-group person-group-type="author"><string-name><surname>Askun</surname> <given-names>T</given-names></string-name></person-group>. <chapter-title>Introductory chapter: <italic>Fusarium</italic>: pathogenicity, infections, diseases, mycotoxins, and management</chapter-title>. In: <source><italic>Fusarium</italic>&#x2013;plant diseases, pathogen diversity, genetic diversity, resistance and molecular markers</source>. <publisher-loc>UK</publisher-loc>: <publisher-name>IntechOpen</publisher-name>; <year>2018</year>. doi:<pub-id pub-id-type="doi">10.5772/intechopen.76507</pub-id>.</mixed-citation></ref>
<ref id="ref-15"><label>15.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><string-name><surname>Touati-Hattab</surname> <given-names>S</given-names></string-name>, <string-name><surname>Barreau</surname> <given-names>C</given-names></string-name>, <string-name><surname>Verdal-Bonnin</surname> <given-names>MN</given-names></string-name>, <string-name><surname>Chereau</surname> <given-names>S</given-names></string-name>, <string-name><surname>Richard-Forget</surname> <given-names>F</given-names></string-name>, <string-name><surname>Hadjout</surname> <given-names>S</given-names></string-name>, <etal>et al</etal></person-group>. <article-title>Pathogenicity and trichothecenes production of <italic>Fusarium culmorum</italic> strains causing head blight on wheat and evaluation of resistance of the varieties cultivated in Algeria</article-title>. <source>Eur J Plant Pathol</source>. <year>2016</year>;<volume>145</volume>:<fpage>797</fpage>&#x2013;<lpage>814</lpage>. doi:<pub-id pub-id-type="doi">10.1007/s10658-016-0869</pub-id>.</mixed-citation></ref>
<ref id="ref-16"><label>16.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><string-name><surname>Abdallah-Nekache</surname> <given-names>N</given-names></string-name>, <string-name><surname>Laraba</surname> <given-names>I</given-names></string-name>, <string-name><surname>Ducos</surname> <given-names>C</given-names></string-name>, <string-name><surname>Barreau</surname> <given-names>C</given-names></string-name>, <string-name><surname>Bouznad</surname> <given-names>Z</given-names></string-name>, <string-name><surname>Boureghda</surname> <given-names>H</given-names></string-name></person-group>. <article-title>Occurrence of fusarium head blight and fusarium crown rot in Algerian wheat: identification of associated species and assessment of aggressiveness</article-title>. <source>Euro J Plant Pathol</source>. <year>2019</year>;<volume>154</volume>(<issue>3</issue>):<fpage>499</fpage>&#x2013;<lpage>512</lpage>. doi:<pub-id pub-id-type="doi">10.1007/s10658-019-01673-7</pub-id>.</mixed-citation></ref>
<ref id="ref-17"><label>17.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><string-name><surname>Hadjout</surname> <given-names>S</given-names></string-name>, <string-name><surname>Ch&#x00E9;reau</surname> <given-names>S</given-names></string-name>, <string-name><surname>Mekliche</surname> <given-names>L</given-names></string-name>, <string-name><surname>Marchegay</surname> <given-names>G</given-names></string-name>, <string-name><surname>Ducos</surname> <given-names>C</given-names></string-name>, <string-name><surname>Boureghda</surname> <given-names>H</given-names></string-name>, <etal>et al.</etal></person-group> <article-title>Molecular identification of some <italic>Fusarium</italic> isolates and their chemotypes involved in fusarium head blight on durum wheat in Algeria</article-title>. <source>Arch Phytopatho Plant Prot</source>. <year>2022b</year>;<volume>55</volume>(<issue>4</issue>):<fpage>499</fpage>&#x2013;<lpage>513</lpage>. doi:<pub-id pub-id-type="doi">10.1080/03235408.2022.2034363</pub-id>.</mixed-citation></ref>
<ref id="ref-18"><label>18.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><string-name><surname>Laraba</surname> <given-names>I</given-names></string-name>, <string-name><surname>Boureghda</surname> <given-names>H</given-names></string-name>, <string-name><surname>Abdallah</surname> <given-names>N</given-names></string-name>, <string-name><surname>Bouaicha</surname> <given-names>O</given-names></string-name>, <string-name><surname>Obanor</surname> <given-names>F</given-names></string-name>, <string-name><surname>Moretti</surname> <given-names>A</given-names></string-name>, <etal>et al</etal></person-group>. <article-title>Population genetic structure and mycotoxin potential of the wheat crown rot and head blight pathogen <italic>Fusarium culmorum</italic> in Algeria</article-title>. <source>Fun Gen Biol</source>. <year>2017</year>;<volume>103</volume>:<fpage>34</fpage>&#x2013;<lpage>41</lpage>. doi:<pub-id pub-id-type="doi">10.1016/j.fgb.2017.04.001</pub-id>; <pub-id pub-id-type="pmid">28392426</pub-id></mixed-citation></ref>
<ref id="ref-19"><label>19.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><string-name><surname>Nicol</surname> <given-names>JM</given-names></string-name>, <string-name><surname>Elek&#x00E7;io&#x011F;lu</surname> <given-names>IH</given-names></string-name>, <string-name><surname>Bolat</surname> <given-names>N</given-names></string-name>, <string-name><surname>Rivoal</surname> <given-names>R</given-names></string-name></person-group>. <article-title>The global importance of the cereal cyst nematode (<italic>Heterodera</italic> spp.) on wheat and international approaches to its control</article-title>. <source>Com Agri Appl Biol Sci</source>. <year>2007</year>;<volume>72</volume>:<fpage>677</fpage>&#x2013;<lpage>86</lpage>.</mixed-citation></ref>
<ref id="ref-20"><label>20.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><string-name><surname>Tunali</surname> <given-names>B</given-names></string-name>, <string-name><surname>Obanor</surname> <given-names>F</given-names></string-name>, <string-name><surname>Erginba&#x015F;</surname> <given-names>G</given-names></string-name>, <string-name><surname>Westecott</surname> <given-names>RA</given-names></string-name>, <string-name><surname>Nicol</surname> <given-names>J</given-names></string-name>, <string-name><surname>Chakraborty</surname> <given-names>S</given-names></string-name></person-group>. <article-title>Fitness of three <italic>Fusarium</italic> pathogens of wheat</article-title>. <source>FEMS Microb Ecol</source>. <year>2012</year>;<volume>81</volume>:<fpage>596</fpage>&#x2013;<lpage>609</lpage>. doi:<pub-id pub-id-type="doi">10.1111/j.1574-6941.2012.01388.x</pub-id>; <pub-id pub-id-type="pmid">22500915</pub-id></mixed-citation></ref>
<ref id="ref-21"><label>21.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><string-name><surname>Tekle</surname> <given-names>S</given-names></string-name>, <string-name><surname>Skinnes</surname> <given-names>H</given-names></string-name>, <string-name><surname>Bj&#x00F8;rnstad</surname> <given-names>&#x00C5;</given-names></string-name></person-group>. <article-title>The germination problem of oat seed lots affected by Fusarium head blight</article-title>. <source>Eur J Plant Patho</source>. <year>2013</year>;<volume>135</volume>:<fpage>147</fpage>&#x2013;<lpage>158</lpage>. doi:<pub-id pub-id-type="doi">10.1007/s10658-012-0074-6</pub-id>.</mixed-citation></ref>
<ref id="ref-22"><label>22.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><string-name><surname>Parry</surname> <given-names>DW</given-names></string-name>, <string-name><surname>Jenkinson</surname> <given-names>P</given-names></string-name>, <string-name><surname>McLeod</surname> <given-names>L</given-names></string-name></person-group>. <article-title>Fusarium ear blight (scab) in small grain cereals&#x2014;a review</article-title>. <source>Plant Patho</source>. <year>1995</year>;<volume>44</volume>:<fpage>207</fpage>&#x2013;<lpage>38</lpage>. doi:<pub-id pub-id-type="doi">10.1111/j.1365-3059.1995.tb02773.x</pub-id>.</mixed-citation></ref>
<ref id="ref-23"><label>23.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><string-name><surname>Jones</surname> <given-names>RK</given-names></string-name></person-group>. <article-title>Seedling blight development and control in spring wheat damaged by <italic>Fusarium graminearum</italic> group 2</article-title>. <source>Plant Dis</source>. <year>1999</year>;<volume>83</volume>(<issue>11</issue>):<fpage>1013</fpage>&#x2013;<lpage>8</lpage>. doi:<pub-id pub-id-type="doi">10.1094/PDIS.1999.83.11.1013</pub-id>; <pub-id pub-id-type="pmid">30841269</pub-id></mixed-citation></ref>
<ref id="ref-24"><label>24.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><string-name><surname>Purahong</surname> <given-names>W</given-names></string-name>, <string-name><surname>Alkadri</surname> <given-names>D</given-names></string-name>, <string-name><surname>Nipoti</surname> <given-names>P</given-names></string-name>, <string-name><surname>Pisi</surname> <given-names>A</given-names></string-name>, <string-name><surname>Lemmens</surname> <given-names>M</given-names></string-name>, <string-name><surname>Prodi</surname> <given-names>A</given-names></string-name></person-group>. <article-title>Validation of a modified Petri-dish test to quantify aggressiveness of <italic>Fusarium graminearum</italic> in durum wheat</article-title>. <source>Eur J Plant Patho</source>. <year>2012</year>;<volume>132</volume>:<fpage>381</fpage>&#x2013;<lpage>91</lpage>. doi:<pub-id pub-id-type="doi">10.1007/s10658-011-9883-2</pub-id>.</mixed-citation></ref>
<ref id="ref-25"><label>25.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><string-name><surname>Mekliche</surname> <given-names>A</given-names></string-name>, <string-name><surname>Dahlia</surname> <given-names>F</given-names></string-name>, <string-name><surname>Hanifi-Mekliche</surname> <given-names>L</given-names></string-name></person-group>. <article-title>Agromorphological diversity and stability of durum wheat lines (<italic>Triticum durum</italic> Desf.) in Algeria</article-title>. <source>Acta Agro Hung</source>. <year>2013</year>;<volume>61</volume>:<fpage>149</fpage>&#x2013;<lpage>59</lpage>. doi:<pub-id pub-id-type="doi">10.1556/AAgr.61.2013.2.6</pub-id>.</mixed-citation></ref>
<ref id="ref-26"><label>26.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><string-name><surname>Leslie</surname> <given-names>JF</given-names></string-name>, <string-name><surname>Summerell</surname> <given-names>BA</given-names></string-name></person-group>. <article-title>Morphological and molecular identification of fusarium head blight isolates from wheat in the north of Iran</article-title>. <source>Aust J Crop Sci</source>. <year>2006</year>;<volume>6</volume>:<fpage>1356</fpage>&#x2013;<lpage>61</lpage>.</mixed-citation></ref>
<ref id="ref-27"><label>27.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><string-name><surname>Mesterhazy</surname> <given-names>A</given-names></string-name></person-group>. <article-title>Breeding wheat for resistance to <italic>Fusarium graminearum</italic> and <italic>Fusarium culmorum</italic></article-title>. <source>Zeit f&#x00FC;r Pflanzen</source>. <year>1983</year>;<volume>91</volume>:<fpage>295</fpage>&#x2013;<lpage>311</lpage>.</mixed-citation></ref>
<ref id="ref-28"><label>28.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><string-name><surname>Brennan</surname> <given-names>JM</given-names></string-name>, <string-name><surname>Fagan</surname> <given-names>B</given-names></string-name>, <string-name><surname>Van Maanen</surname> <given-names>A</given-names></string-name>, <string-name><surname>Cooke</surname> <given-names>BM</given-names></string-name>, <string-name><surname>Doohan</surname> <given-names>FM</given-names></string-name></person-group>. <article-title>Studies on <italic>in vitro</italic> growth and pathogenicity of European <italic>Fusarium</italic> fungi</article-title>. <source>Eur J Plant Patho</source>. <year>2003</year>;<volume>109</volume>:<fpage>577</fpage>&#x2013;<lpage>87</lpage>. doi:<pub-id pub-id-type="doi">10.1023/A:1024712415326</pub-id>.</mixed-citation></ref>
<ref id="ref-29"><label>29.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><string-name><surname>Pucciariello</surname> <given-names>C</given-names></string-name></person-group>. <article-title>Molecular mechanisms supporting rice germination and coleoptile elongation under low oxygen</article-title>. <source>Plants</source>. <year>2020</year>;<volume>9</volume>:<fpage>1037</fpage>. doi:<pub-id pub-id-type="doi">10.3390/plants9081037</pub-id>; <pub-id pub-id-type="pmid">32824201</pub-id></mixed-citation></ref>
<ref id="ref-30"><label>30.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><string-name><surname>Wei</surname> <given-names>N</given-names></string-name>, <string-name><surname>Zhang</surname> <given-names>S</given-names></string-name>, <string-name><surname>Liu</surname> <given-names>Y</given-names></string-name>, <string-name><surname>Wang</surname> <given-names>J</given-names></string-name>, <string-name><surname>Wu</surname> <given-names>B</given-names></string-name>, <string-name><surname>Zhao</surname> <given-names>J</given-names></string-name>, <etal>et al.</etal></person-group> <article-title>Genome-wide association study of coleoptile length with Shanxi wheat</article-title>. <source>Front Plant Sci</source>. <year>2022</year>;<volume>13</volume>:<fpage>188</fpage>. doi:<pub-id pub-id-type="doi">10.3389/fpls.2022.1016551</pub-id>; <pub-id pub-id-type="pmid">36212294</pub-id></mixed-citation></ref>
<ref id="ref-31"><label>31.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><string-name><surname>Hudec</surname> <given-names>K</given-names></string-name></person-group>. <article-title>Pathogenicity of fungi associated with wheat and barley seedling emergence and fungicide efficacy of seed treatment</article-title>. <source>Biologia</source>. <year>2007</year>;<volume>62</volume>(<issue>3</issue>):<fpage>287</fpage>&#x2013;<lpage>91</lpage>. doi:<pub-id pub-id-type="doi">10.2478/s11756-007-0050-3</pub-id>.</mixed-citation></ref>
<ref id="ref-32"><label>32.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><string-name><surname>Bouanaka</surname> <given-names>H</given-names></string-name>, <string-name><surname>Bellil</surname> <given-names>I</given-names></string-name>, <string-name><surname>Khelifi</surname> <given-names>D</given-names></string-name></person-group>. <article-title>Multiple methods for varietal resistance assessment of durum wheat cultivars against <italic>Fusarium culmorum</italic> the causal agent of fusarium head blight and crown rot in Algeria</article-title>. <source>Physio Mol Plant Patha</source>. <year>2021</year>;<volume>115</volume>(<issue>6</issue>):<fpage>101683</fpage>. doi:<pub-id pub-id-type="doi">10.1016/j.pmpp.2021.101683</pub-id>.</mixed-citation></ref>
<ref id="ref-33"><label>33.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><string-name><surname>Bencheikh</surname> <given-names>A</given-names></string-name>, <string-name><surname>Rouag</surname> <given-names>N</given-names></string-name>, <string-name><surname>Boutalbi</surname> <given-names>W</given-names></string-name>, <string-name><surname>Belabed</surname> <given-names>I</given-names></string-name></person-group>. <article-title>First report of <italic>Fusarium chlamydosporum</italic> causing crown rot and dumping off on durum wheat in Algeria</article-title>. <source>J Nov Res Plant Protect</source>. <year>2018</year>;<volume>9</volume>:<fpage>309</fpage>&#x2013;<lpage>24</lpage>.</mixed-citation></ref>
<ref id="ref-34"><label>34.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><string-name><surname>Sakr</surname> <given-names>N</given-names></string-name></person-group>. <article-title><italic>Intra</italic>- and <italic>inter</italic>-species variability of the aggressiveness in four fusarium head blight species on durum wheat plants detected in an <italic>in vitro</italic> Petri-dish assay</article-title>. <source>Arch Phytopat Plant Protect</source>. <year>2018</year>;<volume>51</volume>:<fpage>814</fpage>&#x2013;<lpage>23</lpage>. doi:<pub-id pub-id-type="doi">10.1080/03235408.2018.1495390</pub-id>.</mixed-citation></ref>
</ref-list>
</back>
</article>



