Another common and valuable food source for millions of people worldwide is pea (Pisum sativum L.), the essential leguminous crop for both local consumptions as well as exportation. Although the high-yielding cultivars are produced, the average seed yield per unit is still insufficient due to the infection with many diseases (Hamid et al. 2012). Pea root rot and damping-off diseases caused by soil-borne pathogenic fungi, such as F. solani and R. solani, are the most severe seedling diseases that cause substantial losses, either in seed quality or in yield. Hamid et al. (2012) studied the efficiency assessment of T. harzianum, T. viride, Pseudomonas fluorescens, and Gliocladium virens against F. solani. In vitro results indicated that T. harzianum exhibited the highest inhibition percentage in dual culture investigation (78.60%), followed by T. viride (75.72%), G. virens (69.52%), and P. fluorescens (68.37%). In pot experiments, T. harzianum reduced the disease incidence and severity (21.30 and 10.94%), respectively, followed by T. viride (25.30 and 12.02%), P. fluorescens (29.28 and 14.98%), G. virens (38.64 and 17.58%), than the fungicide carbendazim 50 WP (14.64 and 4.98%). No difference occurred between T. harzianum and carbendazim in seed germination percentage (90.00 and 90.00%), and number of days needed for seed germination (7.26 ± 0.07 and 7.34 ± 0.10), respectively, followed by T. viride (86.00% and 7.32 ± 0.13), P. fluorescens (83.00% and 7.37 ± 0.08), G. virens (82.00% and 7.53 ± 0.08), than the control treatment (61.00% and 7.88 ± 0.08).
The efficacy of T. harzianum, T. viride, G. virens, and P. fluorescens on managing of pea root rot disease, caused by F. solani was evaluated by Mudasar et al. (2012). In field trials, T. harzianum reduced disease severity percentages (63.81%), followed by T. viride (60.44%), P. fluorescens (51.19%), G. virens (41.82%) than the fungicide carbendazim 50 WP (82.42%). No difference occurred between T. harzianum and the fungicide in seed germination percentage (80.00 and 80.00%), as well as the number of days needed for seed germination (6.92 ± 0.05 and 7.01 ± 0.08), respectively, followed by T. viride (75.00% and 6.94 ± 0.08), P. fluorescent (73.00% and 6.98 ± 0.07) and G. virens (70.00% and 6.98 ± 0.07), than the control treatment (59.00% and 7.21 ± 0.06).
Evaluation of seed treatment was investigated as well as soil application of T. koningii SMA-7 (Bio-1), RMA-8 (Bio-II), and JMA-11 (Bio-III), and T. harzianum SMA-4 (Bio-IV) by Kapoor et al. (2006). These treatments were mixed with farmyard manure against F. solani. In vitro investigations established that the maximum mycelial growth inhibition of F. solani was recorded (82.16%) with T. harzianum SMA-4 (Bio-IV), followed by T. koningii JMA-11 (Bio-III) at 80.60%, RMA-8 (Bio-II) at 75.19%, whereas SMA-7 (Bio-1) at 70.53%. In addition, they investigated the 4 bioagents of Trichoderma, in the form of soil and seed applications against F. solani under open field conditions. The most effective bioagent, through soil application, was T. koningii SMA-7 (Bio-1), which exhibited the least infection rate (3.46%) of root rot-wilt complex, followed by T. harzianum SMA-4 (Bio-IV) with 3.63%, T. koningii RMA-8 (Bio-II) with 9.49%, and T. koningii JMA-11 (Bio-III) with 23.13% than the control treatment (32.50%). Furthermore, the used bioagents were less effective through seed application than using a soil application. T. koningii RMA-8 (Bio-II) scored the least disease incidence (19.11%) of root rot-wilt complex, followed by T. koningii JMA-11 (Bio-III) with 25.03%, T. harzianum SMA-7 (Bio-1) with 31.62%, T. koningii SMA-4 (Bio-IV) with 33.97% compared to control treatment (32.50%).
Another important point, the efficiency of seed priming (polyethylene glycol-PEG-8000 in ration 30.2 g/100 ml), seed dressing (fungicide Rizolex-T 50% WP at a recommended dose of 3 g/kg seeds), and seed coating [seeds were immersed in 1% carboxymethylcellulose (CMC) for 30 min, then coated with an individual suspension (107 CFU/ml) of Bacillus subtilis, Pseudomonas fluorescence and 3 × 104 conidia/ml of T. harzianum]. Then, seed bio-priming (spore suspension of T. harzianum, as well as bacterial suspension of B. subtilis, P. fluorescence supplemented with 1% CMC solution, against pea root rot disease induced by R. solani, F. solani, F. oxysporum, Sclerotium rolfsii, and Pythium spp. Furthermore, plant growth and crop yield, under greenhouse and open field conditions, were examined during the 2 growing seasons 2005/06 and 2006/07 by El-Mohamedy and Abd El-Baky (2008). Interestingly, the results of greenhouse experiment indicated that the incidence of disease, at pre-emergence (15 days after sowing) and root rot (45 days after sowing), was suppressed by all types of seed treatments. Seed bio-priming with T. harzianum reduced the pre-emergence damping-off 15 days after sowing by F. solani (58.8%), R. solani (50%), and S. rolfsii (50%), followed by seed coating treatment, F. solani (29.4%), R. solani (30%), and S. rolfsii (28.5%), than the control treatment with a reduction 0% of all pathogens. The same trend was observed when applying the bio-priming seed treatment, which resulted in a reduction of F. solani, R. solani, and S. rolfsii, after 45 days from sowing, followed by seed coating treatment. Moreover, the results obtained from the field experiment showed that the disease incidence, in the pre-emergence (15 days after sowing) and root rot (45 and 60 days after sowing), was eliminated by types of seed treatments used over 2 seasons 2005/06 and 2006/07. In the first season 2005/06, seed bio-priming with T. harzianum resulted in a decrease in disease incidence, in the pre-emergence damping-off 15 days after sowing) with all pathogens (72.8%), root rot after 45 days (72.2%), and root rot after 60 days (67.6%), followed by seed coating treatment with 48.4, 46.3, and 43.2%, respectively, than the control treatment with 0% reduction in all stages. The same trend was observed during the following season 2006/07 when the bio-priming seed treatment resulted in the highest efficacy, followed by seed coating treatment. Moreover, during both seasons, bio-priming followed by seed coating with T. harzianum treatments stimulated plant height, the average number of leaves/plant, the average number of branches/plant and dry weight of shoots/plant, as well as yield improvement, i.e., the average number of pods/plants, average pod weight/plant and total yield of pea plants than the control treatment.
El-abd et al. (2013) studied the effect of biological seed treatments, such as priming with 1% carboxymethylcellulose, seed coating with (3×106 conidia/ml) of T. harzianum, and bio-priming 1% CMC mixed with (3×106 conidia/ml) of T. harzianum, against pea root rot and damping-off diseases, growth and yield of plants under different concentrations of phosphorus fertilization (0, 25, 50, and 75 kg P2O5/feddan) (feddan = 4200 m2). The results of pre-emergence damping-off percentages indicated that the usage of bio-priming 1% CMC mixed with (3 × 106 conidia/ml) of T. harzianum, reduced the disease incidence to 4%, followed by seed coating and priming treatments with no differences with phosphorus amount (50 or 75 kg P2O5). A similar trend was obtained by root rot incidence. Disease reduction was achieved when seed bio-priming 1% CMC mixed with (3 × 106 conidia/ml) of T. harzianum treatment with (75 kg/fed P2O5). This treatment reduced post-emergence pea root rot to 4.25% after 40 days, and to 3% after 60 days. The second effective treatment was seed coating, followed by seed priming. These results indicate that the general increase in vegetative growth and yield, such as plant height, number of leaves/plant, fresh weight of leaves, pod yield, and green seed TSS with both increased levels of phosphorus fertilization and bio-priming 1% CMC, mixed with 3 × 106 conidia/ml of T. harzianum treatment was a direct result of the T. harzianum ability to management root rot disease and increase root mass.
Evaluation of different leaf extracts, chemicals, and 2 Trichoderma species (T. harzianum and T. viride), against the root rot of pea in a field trial, was investigated by Singh et al. (2014). T. harzianum and T. viride treatments were highly effective in reducing the root rot disease incidence with 18.94 and 19.52%, respectively, followed by drek (neem) Melia azadirachta seed extract (21.00%) and drek (neem) leaf extract (25.37%). All treatments were compared to fungicides carbendazim and (metalaxyl and mancozeb) as well as the control treatment which scored root rot disease incidence (9.55, 8.56, and 38.96%), respectively. T. harzianum and T. viride improved plant height, the number of branches/plants, pod weight, the number of pods/plant, pod length, the number of grains/pod, and yield/ha. However, drek (neem) seed and leaf extracts were found to enhance growth and yield parameters, compared to the fungicides carbendazim and (metalaxyl and mancozeb) and control treatment.
Combination of Trichoderma species with beneficial bacteria such as P. fluorescens, Rhizobium sp., and B. subtilis under open field and greenhouse conditions was studied. Negi et al. (2014) evaluated the effects of pea seed treatment with T. harzianum and T. virens, individually or in combination with P. fluorescens, against R. solani and F. solani under field conditions. They found that T. harzianum reduced root rot disease severity in combination with P. fluorescens. The combination between T. harzianum and P. fluorescens as seed bio-priming recorded the least disease severity (20%), followed by T. harzianum + P. fluorescens + T. virens (30%), P. fluorescens (31.1%) than the untreated control treatment (49.4%). In addition, the combination of T. harzianum with P. fluorescens had a remarkable increase in planta, for instance, germination percentage, shoot, root and seedling lengths, vigor index, number of pods/plant, pod weight, number of grains/pod, and total yield/ha were recorded. These investigations revealed that the combination of T. harzianum with P. fluorescens was the most effective treatment in reducing disease severity percentages and increasing plant growth parameters, as well as yield components compared to T. virens or T. harzianum treatment alone.
Trichoderma harzianum, Rhizobium sp., and B. subtilis were used as biological agents to manage pea root rot complex and improve plant growth parameters according to the study done by Muhanna et al. (2018). The results revealed that the root rot complex was caused by R. solani, F. oxysporum, Thielaviopsis basicola, and S. sclerotiorum. Field experiments indicated that all treatments decreased disease severity percentages. With T. harzianum at 50 and 100 ml (concentration 3 × 107 conidia/ml), disease severity was decreased (15.1 and 13.8%) and (17.8 and 15.6%), respectively, than the control treatment (22.2 and 20.5%). Rhizobium sp., at (50 and 100 ml), reduced the disease severity (16.9 and 13.1%) and (17.8 and 14.2%), respectively, followed by treatments with B. subtilis (15.4 and 13.3%) and (16.9 and 14.7%), than the control treatment. Obtained results showed that all the biocontrol agents increased the growth parameters when applied at 100 ml.
Rhizobium leguminosarum combined with Trichoderma lignorum, T. longibrachiatum, and T. koningii were used as biological agents against pea root rot complex and improved plant growth parameters according to the study of Ketta et al. (2021). Greenhouse experiments indicated that combination of R. leguminosarum with T. longibrachiatum reduced the post-emergence damping-off (6.67%) and root rot (9.58%) caused by R. solani. Survived plants, nitrogen fixation, and yield parameters were also increased. Treatment of R. leguminosarum combined with T. koningii against F. solani reduced the post-emergence damping-off (6.67%) and root rot (13.06%).
The outcomes of using beneficial microbes such as Trichoderma fungi for management of root rot in the bean and pea have benefits for the plant health and production. For instance, they suppress pathogens, promoting plant growth, improving the availability of nutrient uptake, such as iron, nitrogen, and phosphorus, and enhancing host capacity under stressful conditions in the rhizosphere. Besides, the different mode of action of Trichoderma that includes competition for nutrients and space in the colonization sites, antibiosis and stimulation of plant immunity, and defense mechanisms. Secondary metabolites (SMs) produced by Trichoderma species are considered to be one of the most effective bioactive molecules in the biological control strategies. Microorganisms and plants, mainly produce these natural compounds from different pathways derived from acetyl coenzyme A, or amino acids, which have many biological activities related to the survival functions of the organism, such as competitive as an antifungal activity and auxin production as a symbiotic relationship. Beneficial microorganisms such as Trichoderma species can produce bioactive molecules that can participate in the interactive process, between plants and their invaded pathogens, with consequences for crop production. Biocontrol agents belonging to Trichoderma genus are well-known producers of SMs, i.e., mycotoxins, antibiotics, and pigments, which are suppressive compounds to soil-borne pathogens or microbial competitors.
Beside the abovementioned recommendations for improvement of Trichoderma efficiency, soil application treatments are more effective than using a seed application. In case of seed application treatment, bio-priming was an effective treatment compared to seed priming and seed coating. The combination of Trichoderma species with beneficial bacteria such as P. fluorescens, Rhizobium sp., and B. subtilis is recommended.