Background

Wheat (Triticum aestivum L.) is one of the major cereals worldwide. In Egypt, wheat is considered a strategic food crop for the population’s diet. However, wheat plants are attacked by various diseases during their vegetative growth. The major diseases of wheat worldwide include the powdery mildew caused by Blumeria graminis f. sp. tritici (DC.) (Golzar et al. 2016; Bradley and Thomas 2019), septoria leaf blotch (SLB) caused by Septoria tritici Desm ((Binalf and Shifa 2018; Mojerlou et al. 2009) and stem rust caused by Puccinia graminis f. sp. tritici Pers (Leonard and Szabo 2005; Reynolds and Borlaug 2006; Singh et al. 2011a; Steffenson et al. 2017). In Egypt, the susceptible wheat cultivars are affected by severe foliar diseases, like powdery mildew, septoria leaf spot and leaf and stem rust. Powdery mildew causes a significant yield loss of 22.5% (Alam et al. 2013; Ashmawy et al. 2014) and up to about 60% (Haggag and Abd-El-Kareem 2009; Haggag 2013) for septoria leaf spot and leaf and stem rust diseases.

For global protection, several investigations have been performed to control wheat foliar diseases such as resistant cultivars, fungicide alternatives, and biocontrol (Provance-Bowley et al. 2010; Turkkan 2014). Using biological control agents to prevent the development of plant diseases caused by fungi is one such alternative. The plant growth-promoting microorganisms are a group of valuable microorganisms in the plant’s rhizosphere, accompanying the root surface. They can enhance plant growth and protect it against several diseases and abiotic stresses (Grover et al. 2011; Glick 2012). Microbial-based agricultural inputs have a long history of enhancing plant production, starting with the inoculation of leguminous roots in the early twentieth century (Desbrosses and Stougaard 2011). Certain bacterial strains of Bacillus, Pseudomonas, Glomus, and others have been broadly used (Borriss 2011; Sivasakthi et al. 2014). Moreover, Singh et al. (2011b) stated that using beneficial microorganisms in crop cultivation is considered a perfect strategy for improving the efficiency of the used resources and increasing the outcome yield. Arbuscular mycorrhizal (AM) fungi are the most widespread root fungal symbionts and were associated with the roots of more than 80% of cultivated crops (Berruti et al. 2016). Kloepper, et al. (2004) reported that plant growth-promoting rhizobacteria (PGPR) could replace chemical fertilizers and pesticides and help in control plant disease. They also demonstrated that PGPR is a component of the integrated management system which decrease the rates of used agrochemicals and cultural control practices and can be used as biocontrol agents Bacillus spp. (B. amyloliguefaciens, B. subtilis, B. pasteurii, B. cereus, B. Pumilus, B. mycoides and B. sphaericus).

Therefore, the current investigation was carried out to evaluate the biocontrol effects of biofertilizers (Pseudomonas fluorescens Migula (NRC2041) and Bacillus subtilis Ehrenberg (NRC313) or AM fungi Glomus mosseae Tul. & C. Tul. (NRC212A) and G. fasciculatum Tul. & C. Tul. (NRC212B). These microorganisms used as soil drench alone or in combination with the antagonists T. harzianum Rifai or P. fluorescens foliar spray against foliar diseases of wheat plants under field conditions.

Methods

The field experiments were performed during two growing seasons 2020/21 and 2021/22 at Kafr-Eldawar region, El-Beheira governorate, Egypt, for evaluating soil drench and foliar spray with some bioagents to reduce foliar diseases of wheat plants under natural field conditions. Three wheat cultivars, Giza 168, Misr 2 and Sids 14, were sown at each growing season. These cultivars are commonly cultivated in Egypt and represent high (Giza 168) moderate (Misr 2) and low resistance (Sis 14) against wheat foliar disease incidence. In the present work, the used wheat cvs. were supplied by Field Crops Research Institute, Agricultural Research Centre, Giza, Egypt (2022) http://www.arc.sci.eg/default.aspx?lang=ar.

Experimental materials

In the current study, the experimental field’s siol was drenched with mixtures of AM fungi and biofertilizers while sowing wheat grains. The AM fungal spores of Glomus mosseae (NRC212A) and G. fasciculatum (NRC212B) were obtained from Agricultural Microbiology Dep., National Research Center, Dokki, Cairo, Egypt. AMF inoculum (Glomus mosseae and G. fasciculatum) was prepared as described by Attia and Eid (2005). Approximately 50 g of prepared mycorrhizal inoculm for each 10 m2 of soil was used.

Biofertilizer (PGPR), Pseudomonas fluorescens (NRC2041) and Bacillus subtilis (NRC313) were grown at 27 °C for 48 h on nutrient broth medium and centrifuged at 3000 × g for 15 min. The pellet was resuspended in sterile distilled water and the final concentration was adjusted to 109 CFU/ml (McGoverin et al. 2020). A volume of 2 L containing fungal spores or bacterial cell suspensions was used for every 100 m2 of grown wheat plants.

The present bioagents were, T. harzianum and P. fluorescens, successfully used in previous studies at Plant Pathology Dept., National Research Centre, Egypt (El-Mougy et al. 2021).

At the sowing date, the soil was inoculated with AMF mixtures and bacterial biofertilizers inocula afterward (Abdel-Kader and El-Mougy 2009). The prepared inocula were mixed in the top 10 cm of soil surface and mixed thoroughly to ensure equal distribution of the added inocula.

A growth suspension of the two bioagents grown on a PDB medium was used as foliar spray for wheat plants. The spore suspension of the fungal strain (1 mL/106) or cell suspension of the bacterial strain (1 mL/108) was inoculated in flasks and incubated at 28–30 °C for seven days at 200 rpm. The resulting fungal spores or bacterial cells suspension were sprayed to wheat. A volume of 2 L containing fungal spores or bacterial cell suspensions were used for every 100 m2 of grown wheat plants.

Fungicide Amistar (25%SC Azoxystrobin- Syngenta Com. India) was applied as a comparison treatment at a 0.5 mL/L rate (Syngenta 2017).

Experimental field design and applied treatments

The experimental field trials were carried out in two successive seasons 2020/21 and 2021/22, and one different location per season. The experimental field in each of the growing season consisted of plots 1 × 10 m containing ten rows. The individual applied treatments were represented by five plots as replicates for each of the three wheat cultivars. Wheat grains cvs. Giza 168, Misr 2 and Sids 14 were sown on December 10th of each cultivation season.

At each growing season, the following treatments were applied:

  1. 1

    The soil was drenched with biofertilizer (500 mL of P. fluorescens and B. subtilis of prepared mixture per 10 m2)

  2. 2

    The soil was drenched with mycorrhizae (50 g of prepared mixture per 10 m2)

  3. 3

    The soil was drenched with mycorrhizae and foliar spray with P. fluorescens suspension (108 CFU/mL)

  4. 4

    The soil was drenched with mycorrhizae and foliar spray with T. harzianum suspension (106 CFU/mL)

  5. 5

    Foliar spray with P. fluorescens suspension (108 CFU/mL)

  6. 6

    Foliar spray with T. harzianum suspension (106 CFU/mL)

  7. 7

    Foliar spray with the fungicide Amistar (0.5 ml/L)

  8. 8

    Untreated control

Wheat plants were sprayed individually with each of the treatments mentioned above, and at the same time, distilled water was used for spraying control treatment. A sprayer tank of 2 L was used for each particular treatment. Spray treatments were performed once two-weeks after the seedling’s emergence. In the second growing season 2021/22, the same previous procedures were followed in another experimental field.

During the two growing seasons, the occurrence of wheat foliar diseases, powdery mildew, SLB and stem rust and determination of their severity percentages was regularly registered after 15 days of foliar spray treatment, along with growth period until yield harvest time (the end of April of each season 2021 and 2022). In addition, the determination of produced grains yield was carried out by randomly choosing ten samples of 1000 wheat kernels of each applied treatment and control. After that, average weights to ton/feddan (4200 m2) were calculated. For both experiments, the disease severity and produced yield were recorded.

The data of diseases appearance on all grown wheat cultivars were recorded and meteorological data for temperature, humidity and rainfall throughout the experimental periods (November 2020–May 2021 and November 2021–May 2022) for the two growing seasons [Cited from: Meteorological Authority, General Administration of Information Center, Statistics Department, Annual statistical guide in Arabic https://www.meteoblue.com/ar/weather/historyclimate/weatherarchive/358448].

Diseases assessment

The disease severity was assessed using a scale of five grades according to the leaf area that showed disease symptoms. These grades start from no symptoms and ascending up to more than 75% as follows: no symptoms (grade 1), up to 25% (grade 2), up to 50% (grade 3), up to 75% (grade 4) and more than 75% (grade 5). Yu et al. (2001) used the measuring scale for the powdery mildew disease. Meanwhile, SLB and stem rust disease severity were measured according to the scale described by Gomes et al. (2016).

Disease severity (%) was calculated by using the following equation:

$${\text{Disease severity }}\left( \% \right) = \frac{{{\text{Total}}\;{\text{of}}\;{\text{all}}\;{\text{diseased}}\;{\text{plants}}\;{\text{in}}\;{\text{each}}\;{\text{grade}}}}{{{\text{Whole number of examined plants }} \quad \times {\text{ Maximum disease grade}}}} \times 100$$

Statistical analysis

The recorded results were analyzed using IBM SPSS software version 14.0. Meanwhile, Duncan’s multiple range test at p < 0.05 was used to determine variance analysis and the mean value comparison.

Results

The efficiency of applied bioagents as soil drenching and foliar spray against the wheat foliar disease severity of powdery mildew, SLB and stem rust was assessed for two successive growing seasons (2020/21 and 2021/22) under field conditions. Wheat plants sprayed with the fungicide Amistar at a dose of 0.5 mL/L were used as comparison treatment.

The data presented in Table 1 showed that the recorded powdery mildew severity was higher in the second season than in the first growing season. All applied treatments reduced disease severity compared with the control. It was observed that the grown wheat cultivars differed in their response to powdery mildew disease severity, being low records found for Giza 168 followed by Misr 2 and Sida 14, respectively. Furthermore, the fungicide treatment showed higher efficacy in reducing the severity of powdery mildew. In contrast, the recorded percentages at the two cultivation seasons were 7.4%, 9.6% for Giza 168, 8.8%, 12.4% for Misr 2 and 10.4%, 17.6% for Sids 14, respectively. The combined soil drench treatment with mycorrhizae followed by foliar spray with P. fluorescens or T. harzianum showed more efficacy for reducing disease severity than for each alone. Also, data in Table 1 revealed the powdery mildew disease reduction percentages for each treatment and cultivation season. A high reduction in disease severity was observed at soil drench treatments with mycorrhizae followed by foliar spray with either P. fluorescens 63.5%–64.8%; 56.9%–61.9%; 60.3%43.6% or T. harzianum 51.2% − 58.8%; 49.8%–57.1%; and 40.3%–49.2% for Giza 168, Misr 2 and Sids 14, respectively, throughout the two growing seasons compared with other applied treatments. Moreover, soil drenched with biofertilizers treatment showed the lowest efficacy for reducing the severity of powdery mildew 26.2%–33.1%; 29.8%–33.6%; 27.5%–30.1% for the same cultivars at the two seasons, although it differed significantly from than untreated control.

Table 1 Wheat powdery mildew disease severity in response to soil drenching and foliar spray with bioagents under natural field conditions during two successive growing seasons 20/21 and 21/22
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Data in Table 2 showed the impact of soil drenching with PGPR or mycorrhizae alone or followed by foliar spray with either P. fluorescens or T. harzianum on the severity of SLB disease. A significant difference was observed in disease severity between all treatments and control. The presented data in Table 2 showed that Sids 14 expressed the highest susceptibility to SLB disease severity followed by Misr 2 and Giza 168 cvs. Furthermore, it was observed that all cultivars showed high disease severity in the second cultivation season than those cultivated in the first season at all applied treatments and control.

Table 2 Wheat septoria leaf blotch disease severity in response to soil drenching and foliar spray with bioagents under natural field conditions during two successive growing seasons 20/21 and 21/22
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Also, the recorded lowest disease severity was obtained for [Mycorrhizae and P. fluorescens] and [Mycorrhizae and T. harzianum] treatments. The recorded disease severity was 10.5%, 8.6%, 10.2% and 13.6%, 12.3%, 15.2%, for Giza 168, Misr 23, Sids 14 at the two cultivation seasons, respectively. Following foliar spray with both bioagents showed moderate effects in reducing disease severity was observed. Pseudomonas fluorescens spray treatment recorded decrease in disease severity, with respect to control, estimated as 45.8%–52.6%; 57.8%–64.3%; 63.3%–57.3% at two cultivation seasons for Giza 168, Misr 23, Sids 14 wheat cultivars, respectively. Meanwhile, at T. harzianum treatment, disease severity was reduced by 43.0%–56.3%; 43.0%–58.1%; 49.5%–53.2% at the two cultivation seasons for wheat grown cultivars, in relevant respective order. Also, data in Table 2 demonstrate that the applied fungicide Amistar revealed the lowest disease severity estimated between 8.5% and 12.6% and between 10.5% and 18.3% for wheat cultivars at the first and second growing seasons, respectively. The fungicide Amistar could reduce SLB disease severity by 60.6%, 72.3% and 65.2% for Giza 168, Misr 23, Sids 14 cvs. Moreover, they achieved 70.4%, 62.4% and 62.1% for the same wheat cultivars during the two seasons.

Concerning the severity percentage of stem rust disease, the presented data in Table 3 showed that the utilized treatments resulted in a reduction in the severity of stem rust disease compared with untreated control. Percentages of stem rust disease severity in wheat cultivars were higher at the second growing season than those sown in the first one. Also, Giza 168 cv. revealed the least disease severity followed by Misr 2 and Sids 14 cvs. in ascending order. Highly effective treatments for stem rust severity which were observed at [Mycorrhizae and T. harzianum] followed by [Mycorrhizae and P. fluorescens] treatments. They recorded 5.6%, 5.6%, 7.6% and 7.3%,7.2%, 9.0% and 6.3%, 6.3%, 8.2% and 8.3%, 7.6%, 8.6% disease severity for Giza 168, Misr 2, Sids 14 cvs. at the first and second growing seasons, in the respective order. In the untreated control, stem rust severity was 15.3%, 20.6%, 24.5% and 18.5%, 23.6%, 27.0%, in the same order for wheat cultivars and cultivation seasons.

Table 3 Wheat stem rust disease severity in response to soil drenching and foliar spray with bioagents under natural field conditions during two successive growing seasons 20/21 and 21/22
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Furthermore, data in Table 3 revealed moderate reduction in disease severity calculated of 50.9%, 61.1%, 60.0% and 58.9%, 59.3%, 61.8% for P. fluorescens, while 56.2%, 64.5%, 62.4% and 63.2%, 62.7%, 58.1% for T. harzianum treatments for Giza 168, Misr 2, Sids 14 cvs. at the first and second growing seasons, respectively. Low reduction in stem rust severity was observed with biofertilizer treatment, whereas 31.3%, 43.6%, 46.9% and 31.3%, 44.9%, 48.1% at the two growing seasons and wheat cultivars Giza 168, Misr 2, Sids 14 were recorded, respectively. Also, reductions in disease severity were 41.1%, 53.8%, 56.7% and 43.2%, 55.0%, 59.2% in mycorrhizae treatment. The fungicide Amistar showed the highest reduction in disease severity at the first growing season for Giza 168, Misr 2, Sids 14 cvs. by 77.1%, 73.3% and 74.2%. Meanwhile, 74.0%, 67.7% and 68.1% disease severity reductions were recorded in the second season for the same cultivars.

Concerning wheat foliar diseases, in control treatment, the first occurrence of powdery mildew for sown cultivars (Giza 168, Misr 2, Sids 14) was detected on February of both seasons 2020/21 and 2021/22. Illustrated data in Fig. 1 at this period showed, records of air temperature, air humidity and rainfall were 9.1–22.2 °C, 64.9%, 24.8 mm, and 7.2–19.7 °C, 57.9%, 26.7 mm, respectively. Moreover, on March 2020 and 2021, the SLB disease was detected in control treatment, at records air temperature, air humidity and rainfall as 9.9–23.4 °C, 63.2%, 9.6 mm for the first growing season and 8.0–21.7 °C, 46.3%, 11.5 mm for the second season. Meanwhile, stem rust disease observation was detected in control treatment on April of 2021 and 2022 when air temperature, air humidity and rainfall were recorded as 11.6–29.7 °C, 53.9%, 1.9 mm and 13.5–32.3 °C, 46.5%, 3.8 mm, respectively.

Fig. 1
figure 1

Meteorological data for temperature, humidity and rainfall from November 2020 until May 2021 and November 2021 until May 2022 (https://www.meteoblue.com/ar/weather/historyclimate/weatherarchive/358448)

Full size image

Wheat grains production, presented data in Table 4, showed that the highest yield was observed for Giza 168 followed by Misr 2 and Sids 14, respectively. Also, in all conditions, the wheat grains produced were higher in the second growing season than in the first. Data in Table 4 showed variation in produced grain yield among applied treatments. The fungicide Amistar produced the highest yield 3.0, 3.1, 2.8 and 3.1, 3.3, 3.0 ton/feddan for Giza 168, Misr 2 and Sids 14 at the first and second growing seasons, respectively. Moreover, data in Table 4 revealed that with [mycorrhizae and P. fluorescens] treatment a range between 2.8 and 3.0 ton/feddan and a yield increase of 47.3%–66.6% over untreated control was obtained. Similarly, with the treatment of [mycorrhizae and T. harzianum] the produced grain yield ranged between 2.8 and 3.0 ton/feddan with an increase in yield by 27.2%–70.5% over control. Likewise, in individual P. fluorescens and T. harzianum treatments, the produced yield recorded a range of 2.6–3.0 ton/feddan with an increase of 36.3%–55.5% and between 2.6 – 2.9 ton/feddan with an increase of 33.3%–52.9%, respectively, over control treatment. Also, it was observed that the obtained yield was recorded between 2.4 and 2.8 ton/feddan with an increase of 33.3%–41.1% and a range of 2.3–2.9 ton/feddan with yield increase over control by 22.7%–42.1%, for mycorrhizae and biofertilizer treatments, respectively.

Table 4 Efficacy of soil drenching and foliar spray with bioagents on average grain yield of wheat under natural field conditions during two successive growing seasons 20/21 and 21/22
Full size table

Discussion

In the present study, foliar spray with the Amistar fungicide showed superior effects on reducing the severity of wheat diseases. Amistar (azoxystrobin) decreased the disease intensity throughout the three growing seasons in Pyrethrum fields (Pethybridge and Hay 2005). Its application reduced the common rust severity of maize hybrids (Wright et al. 2014). Similarly, Mahmoud et al. (2016) recorded that during two successive growing seasons, Amistar showed the highest efficacy for decreasing the severity of downy mildew and purple blotch diseases and increasing the onion bulb yield compared to chemical inducers salicylic acid and indol butyric acid. Also, in a study by Boualem et al. (2017), the application of fungicides (Artea and Amistar Xtra) significantly reduced the severity of powdery mildew, yellow rust, and brown rust diseases and increased the yield of wheat plants.

Microbial Biological Control Agents (MBCAs) involve the application of antagonistic microorganisms to crops to control harmful phytopathogenic microorganisms via different mechanisms of action. The MBCAs affect the target pathogen either directly via hyperparasitism, antibiosis (Ghorbanpour et al. 2018) or indirectly by reacting with the substances responsible for plants resistance (Pieterse et al. 2014; Conrath et al. 2015). Spadaro and Droby (2016) reported another mechanism of MBCAs known to compete for nutritive resources or change the growth circumstances for the target pathogens. Previously, Raaijmakers and Mazzola (2012) showed that interactions are a highly regulated network of metabolic proceedings, often merging various modes of action.

In the current study, biofertilizer (PGPB), mycorrhizae and bioagents were evaluated throughout two successive growing seasons for their activity to reduce wheat foliar diseases. Interestingly, the severity of wheat foliar diseases like powdery mildew, SLB and stem rust was higher in the second cultivation season than in the first. This comparison showed no effect of air temperature, humidity, or rainfall on the appearance of foliar diseases. However, it may affect the diseases severity, as shown by the data in Table 1. in addition to the genetic differences in self-resistance of grown wheat cultivars whereas the Wheat cultivar Giza 168 showed more resistance to foliar diseases followed by Misr 2 and Sids 14, in decreasing order. In this regard, El-Shamy et al. (2016) stated that among the Egyptian wheat cultivars, Giza-167, Giza-168, Giza-171 Misr-2, Sids-13, Gemmiza-11 and Gemmiza-12 expressed different types of disease infections with high disease resistance. Therefore, resistant cultivars incorporated in the breeding program or commercial wheat cultivation fields could be recommended. The current study recorded the meteorological data concerning temperature, humidity and rainfall throughout the two experimental growing seasons. It was observed that, powdery mildew, SLB and stem rust on wheat cultivars, Giza 168, Misr 2, Sids 14 started in February, March and April of each growing season, respectively. These results were similar to those recorded previously by El-Mougy et al. (2021) wherein these diseases started to occur during these periods in wheat cultivars, Giza 171, Misr 2 and Gemmiza 12. They stated that during the growing season of 2019/20, the temperature, humidity and rainfall during similar months were 15 °C–23 °C, 45% and 27.9 mm, 16 °C–24 °C, 58% and 12.7 mm, 21 °C –28 °C, 62% and 5.0 mm, respectively.

The fungicide Amistar demonstrated the highest reduction in the severity of all recorded foliar diseases. Meanwhile, the applied approaches of soil drenching and foliar spray reduced foliar diseases and their development.

Soil drenched with biofertilizer (PGPB) or mycorrhizae followed by foliar spray with the bioagent (P. fluorescens and T. harzianum) treatments revealed high effectiveness in reducing the disease’s severity of powdery mildew, SLB and stem rust. These treatments were followed by plant foliar spray with P. fluorescens and T. harzianum.

In this concern, bacterial genera, i.e., Bacillus and Pseudomonas spp., have been identified as PGPR, which are predominant in soil and plant rhizosphere (Podile and Kishore 2006). PGPR synthesizes compounds such as hormones or facilitates the uptake of certain environmental nutrients as a direct promotion or indirectly produces antagonistic substances or induces resistance to prevent phytopathogenic organisms (Patten and Glick 2002). Pieterse et al. (2009) stated that these PGPB could act as an inducer for systemic resistance (ISR), similar to the phenomenon known as systemic acquired resistance (SAR), which occurs when the target plants activate their defense mechanisms in reaction to pathogens infection. This ISR is effective for controlling diseases caused by different pathogens. The ISR involves hormones such as jasmonate and ethylene signaling within the plants that stimulate the host plant’s defense responses to a wide range of pathogens (Verhagen et al. 2004). In addition, Beneduzi et al. (2012) reported that rhizobacteria induces resistance through the salicylic acid-dependent SAR pathway, or requires jasmonic acid and ethylene perception from the plant for ISR. Rhizobacteria belonging to the genera Pseudomonas and Bacillus are well known for their antagonistic effects and ability to trigger ISR. PGPB-elicited ISR was first observed when the susceptibility was reduced to wilt caused by Fusarium sp. (van Peer 1991) and on the cucumber to foliar disease caused by Colletotrichum orbiculare (Wei et al. 1991). Also, de Souza et al. (2015) reported that bacteria could promote plant growth, protect plants against diseases and abiotic stresses, and reduce the severity of many fungal diseases called plant growth-promoting bacteria (PGPB). Kumar et al. (2017) reported that foliar spray with P. fluorescens reduced the incidence of rice blast disease and increased crop yield. Also, Ganeshan and Kumar (2005) recorded that strains of Pseudomonas fluorescens are successful tools as biocontrol agents. These strains can effectively control various diseases in cereals, horticultural crops, oil seeds and others caused by microorganisms such as fungi, bacteria and nematodes.

The recorded reduction of wheat foliar diseases in our current investigation is similar to those reported by other workers (García-Gutiérrez et al. 2013; Tanaka et al. 2017) who stated that they used biocontrol agents which showed similar activity to reduce foliar diseases. Previously, studies showed the capability of Bacillus spp. and Trichoderma sp. to control plant diseases, particularly powdery mildew (Sawant et al. 2017). El-Sharkaway et al. (2014) reported that the bacterium Bacillus sp. successfully controlled powdery mildew in a cucurbit and achieved the highest reduction in disease severity. This reduction was attributed to B. subtilis as PGPR which a broad spectrum application for managing many plant diseases (Liu et al. 2014). Hafez et al (2018) demonstrated a significant reduction in powdery mildew disease symptoms and severity was recorded for squash plants treated with several bioagents suspension of Bacillus subtilis, B. chitinosporus, B. pumilus, B. megaterium, B. polymexa, T. harzianum, and T. viridi. Furthermore, Abd El-Ghany et al. (2009) demonstrate that the bioagents, T. harzianum and Saccharomyces cerevisiae gave moderate control against leaf rust disease severity of willow plants. Also, Trichoderma harzianum T39 induced resistance to downy mildew in Grapevine (Roatti et al. 2013). El-Sharkawy et al (2015) reported that leaf rust disease severity was significantly decreased in two wheat susceptible genotypes Morocco and Sids-1 when sprayed with T. harzianum and Streptomyces viridosporus. In addition, several investigators indicated the efficacy of bioagents in reducing foliar disease severity in various crops such as Bacillus subtilis, P. fluorescens and Streptomyces sp. against Fusarium head blight in wheat (Nourozian et al. 2006), Streptomyces sindeneusis against rice blast (Zarandi et al. 2009), T. harzianum, S. plicatus and P. fluorescence downy mildew in grape (El-Naggar et al. 2012) and T. harzianum, Bacillus subtilis and Ampelomyces qusisqualis against a chocolate spot in broad bean (El-Banoby et al. 2013). A significant reduction in some foliar diseases, i.e., powdery mildew, leaf blotches, and leaf rust was observed in wheat plants sprayed with Pseudomonas putida, methyl jasmonate and chitosan. At the same time, total phenols, peroxidase, chitinase and total soluble proteins also increased by Haggag et al. (2014) significantly.

In the present investigation, it was found that soil drenched with mycorrhizae alone and/or by foliar spray with either P. fluorescence or T. harzianum recorded a significant reduction in all foliar diseases of wheat under field trials throughout two successive growing seasons. Also, they are known as natural biofertilizers, they exchange the host plant with water, nutrients, and pathogen protection, in return for photosynthetic products. In this regard, Pozo and Azcon-Aguilar (2007) stated that the mycorrhizal system is among the most debatable mechanisms of induced plant resistance. During the formation of mycorrhizae nodulation, plant defense responses occur, potentially through cross-signals pathways between salicylic acid and jasmonate. This modulation may stimulate the plant’s reaction to expected enemies by priming the tissues for more efficient activation of defense mechanisms. Also, the application of AM fungi individually or in combination with T. harzianum HL1 and T. viride HL5 was found significantly reduce stem rust disease measures of wheat plants under greenhouse conditions (El-Sharkawy et al. 2018). In a field study by Kabdwal et al. (2019), they concluded that soil drench in combination with bioagents, T. harzianum, P. fluorescens, Jas mycorrhiza (AMF) in addition to three foliar sprays of the fungicide Mancozeb showed effectivity in decreasing tomato diseases such as late, early blight, stem rot and wilt and increasing the yield in the same time.

Conclusion

The results obtained in the current study demonstrated that soil drenched with biofertilizer (PGPB) or mycorrhizal fungi followed by foliar spray with bioagents, T. harzianum or P. fluorescens, could help decrease wheat foliar disease severity of powdery mildew, SLB and stem rust. These approaches are safe and cost effective for reducing foliar wheat diseases, considering them a suitable chemical fungicide alternative.