Efficacy of several chemical fungicides and biofungicides for controlling damping-off and root rot diseases in common bean under field conditions.

Efficacy of several chemical fungicides and biofungicides for controlling damping-off and root rot diseases in common bean under field conditions.

R. M. El-Kholy, A. M. El-Samadesy, A. A. Helalia, and M. M. Hassuba ^*

Department of plant protection, Faculty of Agriculture, Cairo, Al-Azher University, Egyp.

*Corresponding author E-mail: hassuba@azhar.edu.eg  (M. Hassuba)

ABSTRACT

Field experiments were performed in a private farm atKhaled Ibn El-WaleedVillage, Badr Center, El-Behera Governorate to evaluate the efficacy of four chemical fungicides and three biofungicides against damping-off and root rot diseases in common bean caused by Fusarium solani, Rhizoctonia solani, Pythium ultimum and Sclerotium rolfsii under field conditions during the two consecutive growing seasons (2018 and 2019). The four fungicides were { Tendro 40% FS (carboxin+thiram), Maxim XL 3.5% FS (fludioxonil+metalaxyl-M), Hattric 6% FS (tebuconazole) and Rizolex-T 50% WP (tolclofos-methyl+thiram) at two rates (1.75 and 3.50 cm³, 0.50 and 1.00 cm³, 0.50 and 1.00 cm³ and 1.50 and 3.00 gm kg^-1 seeds, respectively). Three biofungicides} Rhizo-N [(30 million cell gm^-1) (Bacillus subtilis)], Biocontrol T 34 12% WP (Trichoderma asperellum) and Plant Guard [ (30 million cell ml^-1) (Trichoderma harzianum)] were used at two rates (2.00 and 4.00 gm, 1.00 and 2.00 gm and 1.25 and 2.50 cm³ kg^-1 seeds, respectively)}. The results clearly indicated that, chemical fungicides were more effective than the biofungicides, and all the tested compound particularly Rizolex-T 50% WP, Tendro 40% FS and Maxim XL 3.5% FS were significantly reduced pre- and post-emergence damping-off, rotted roots, increased survival plants and subsequently increase biological, seed and straw yields in comparison with the untreated control. All chemical fungicides particularly Hattric 6% FS reduced nodules number per plant. In contrast, the tested biofungicides increased nodules number per plant. In connection with the tested rates, all the tested compounds gave better results at their high application rates but accompanied with reduced the nodules number in case of chemical fungicides and increased nodules number in case of biofungicides. 

Keywords: Common bean, Damping-off, Root Rot, Chemical fungicides, Biofungicides.

INTRODUCTION

Bean (Phaseolus vulgaris L.) is considered as a very important vegetable crop worldwide including Egypt and consumed as green pods or dry bean seeds (Ragab, Mona et al., 2015). Common bean is one of the most important food legumes for direct human consumption, it comprises 50% of the legumes consumed worldwide (Broughton et al., 2003 and Graham et al., 2003). It plays an important role in human nutrition as a cheap source for protein, carbohydrates, unsaturated fatty acids, vitamins and minerals (Nassar, Rania et al., 2011; Beebe et al., 2013; Yunsheng et al., 2015 and Ganesan and Xu, 2017). The nutritional attributes of common bean make it a potential crop for improving the nutritional security of poor communities (Kator et al., 2016). In addition to this, it is also important in providing fodder for feeding livestock and it contributes to soil fertility improvement through atmospheric nitrogen fixation (Asfaw, 2011; Ambachew et al., 2015 and Abebe and Mekonnen, 2019). In Egypt, common bean is one of the most important leguminous crops cultivated for local consumption and exportation. The total cultivated area of common bean in Egypt in 2018 reached 120729 feddans that yielded 122870 tons (Anonymous, 2018). Also, bean is known by many other names such as common bean (Abeysinghe, 2007; Mahamune and Kakde, 2011; Shehata, 2015 and Hussein et al., 2018), bean (Kataria et al., 2002; Sallam, Nashwa et al., 2008; El-Fiki et al., 2014 and Ragab, Mona et al., 2015), dry bean (Abd-El-Khair et al., 2019 and Jacobs et al., 2019), French bean,Rajma(Hindi), haricot bean, snap bean, navy bean (Mahamune and Kakde, 2011; Yunsheng et al., 2015 and Mahmoud et al., 2018 a), kidney bean (Mahamune and Kakde, 2011 and  Abd El-Hai and Ali, Abeer, 2018) and finally bean which commonly known in Egypt as Phasolia is a member of family Fabaceae (Nassar, Rania et al., 2011 and Yunsheng et al., 2015).

Bean plants are exposed under greenhouse and field conditions to infection with several foliar and root fungal diseases at all its growth stages and these diseases can attack all plant parts i.e. roots, leaves, stems and pods (Graham and Ranalli,1997 and Mukankusi et al., 2010). Among this disease, damping-off and root rot diseases are serious and persistent problem for bean plants during growing season (Filion et al., 2003; Harveson et al., 2005; Wen et al., 2005 and Ragab, Mona et al., 2015). Damping-off and root rot diseases are caused by several seed and soil-borne pathogenic fungi such as Alternaria alternata, Fusarium solani, F. oxysporum, Pythium spp., Rhizoctonia solani and Sclerotium rolfsii (El- Gamal, Nadia et al., 2003; Abeysinghe, 2007; El-Shami, 2008; Abd-El-Khair et al., 2011; Mahmoud et al., 2013; Pena et al., 2013 and Abd-El-Khair et al., 2019). These pathogens act either individually or in a complex manner (Rusuku et al., 1997) and reduce seed germination, seedling emergence and final plant stand and cause great losses in yield of the affected plants (Mahmoud, 1985; Rizvi and Yang, 1996; EL-Mougy, Nehal, 2001; Vinale et al., 2008; Valentin, 2010 and Yaquelyn et al., 2010). Yield losses in several infested areas approached 50% (Estevez de Jensen et al., 2002).

Various methods were reported to control damping-off and root rot diseases in common bean. These methods including cultivate resistant varieties (Brisa et al., 2007 and Obala et al., 2012), cultural practices (Abeysinghe, 2007; Abawi and Widmer, 2000 and Toledo‑Souza et al., 2012), plant extracts (Kumar and Tripathi, 1991 and Soliman et al., 2013), biological control agents (Sallam, Nashwa et al., 2008; Mahamune and Kakde 2011; El-Fiki et al., 2014; Riad et al., 2015; Hussein et al., 2018 and Korayem et al., 2020) and the most effective method is chemical control (Theer, 2012; Buts and Singh, 2014;  Elshahawy et al., 2016; Kumar et al., 2019 and Korayem et al., 2020 ).

Therefore, the present work was conducted to evaluate the efficiency of four fungicides and three bioagents (BCA_S) for controlling damping-off and root rot diseases of common bean under field conditions and their side effects on nodulation of rhizobium bacteria.

MATERIALS AND METHODS

The field experiments were performed in a private field naturally heavily infested with damping-off and root rot diseases of common bean, atKhaled Ibn El-WaleedVillage, Badr Center, El-Behera Governorate, Egypt, during the two successive growing seasons of 2018 and 2019. Common bean (Phaseolus vulgaris L.) seeds, cv. Giza 6 were obtained from Department of Legume Crop Research, Field Crop Research Institute, Agricultural Research Center (ARC), Ministry of Agriculture and Land Reclamation, Egypt. Rhizobium leguminosarum biovar phaseoli was obtained from Bio-fertilizer Lab, Water and Soil Research Institute, Agricultural Research Center (ARC).

Four fungicides and three biofungicides were used in this study (Table, 1).

The experiments were designed as a randomized complete block design (RCBD) with three replicates for each treatment as well as untreated control. The experimental area of each plot was 21 m² (4.2 × 5m).Each plot comprised of eight rows and 42 holes row^-1. Common bean seeds were treated with the tested fungicides at the recommended and half recommended rates (Table 1) according to the method described byMetwaly et al. (2006). The candidate amount of the tested fungicides was thoroughly mixed with common bean seeds in plastic bags with 3 mL of Arabic gum solution (1%) as sticker and shaked for 10 minutesto insure uniform coverage of seeds with the tested rates. Treated seeds were then allowed to dry at room temperature for 24 hours before sowing. Just before sowing, the seeds were inoculated by Rhizobium leguminosarum biovar phaseoli at the rate 10 gm kg^-1 seed. The inoculum was added and thoroughly mixed with the seeds and during the mixing process 3ml of Arabic gum solution (1 %) was added to ensure their surfaces were uniformly coated and adhere with inoculum. Seeds treated with Rhizobium aloneare used as control.  Treated and untreated seeds were sown at the rate of 2 seeds holes^-1 at 10 cm apart to comprise a total of 672 seeds plot^-1 in Sep. 9, 2018 and Sep.12, 2019 during both growing seasons, respectively. The recommended cultural practices for bean production were adopted throughout growing seasons in this district.

The following measurements were recorded during the growing seasons:

Number of pre-emergence damping-off [15 days after sowing (DAS) (Ragab, Mona et al., 2015)].

Number of post-emergence damping-off [45 DAS (Ragab, Mona et al., 2015)].

Number of infected plants by rotted roots [60 DAS (Soliman et al., 2013)].

Number of survival (healthy) plants [60 DAS (Soliman et al., 2013)].

Number of nodules per plant (at the flowering stage, five plants were uprooted from each plot and washed gently with water and the nodules on every plant root system were counted) according to (Elkoca et al., 2010).

In both seasons, the plants were harvested after 100 days from sowing andleftto dry in the field for 15 days, then,the following characters were determined:

Biological yield (weight of all plants Kg plot^-1).

Seed yield (Kg plot^-1).

Straw yield (Kg plot^-1).   

Statistical analysis:

The obtained results were statistically analyzed by analysis of variance (ANOVA) according to Gomez and Gomes (1984), and L.S.D values were obtained at 0.01 and 0.05.

RESULTS AND DISCUSSION

Effect of seed treatments on damping-off, root rot and survival plants.

The data presented in Tables (2 and 3) showed the effect of treatments on pre- and post-emergence damping-off, rotted rots and survival plants. Generally, all treatments, at any rate of application in both seasons 2018 and 2019, significantly (P= 0.05) reduced the number of pre- and post-emergence damping-off, rotted rots and increased survival plants in comparison with the untreated control. The chemical treatments were significantly better than the biological treatments in both seasons. Among the tested fungicides, Rizolex-T 50% WP, Tendro 40% FS and Maxim XL 3.5% FS were the most effective in reducing the number of pre- and post-emergence damping-off, rotted roots and consequently increasing survival (healthy) plants. On the other hand, Plant guardwas the least effective in this respect, while other fungicides showed an intermediate effect, and the results were similar in both seasons. For example, when Rizolex-T 50% WP, Tendro 40% FS and Maxim XL 3.5% FS were applied at recommended rate (3gm, 3.5 cm³ and 1 cm³ kg^-1 seeds, respectively) the number of pre-emergence damping-off recorded 23.67, 24.67 and 32.00 plants plot^-1  in the first season and 19.67, 22.33 and 34.00 plants plot^-1 in the second season, respectively, while the corresponding values with thePlant guardat the highest rate of application (2.5 cm³ kg^-1 seeds) were 110.00 and 104.33 plants plot^-1comparing with those in the control (201.67 and 193.33, plants plot^-1 , respectively). Hattric 6% FS, Rhizo-N and Biocontrol T 34 12% WP at recommended rate (1 cm³, 4gm and 2gm kg^-1 seeds, respectively) gave 50.67, 66.33 and 83.33 plants plot^-1 in the first season and 46.00, 62.67 and79.33 plants plot^-1 in the second season, respectively, indicating that these fungicides have an intermediate effect. For the number of post-emergence damping-off, the same trend was observed in both seasons as that Rizolex-T 50% WP, Tendro 40% FS and Maxim XL 3.5% FS at recommended rate (3gm, 3.5 cm³ and 1 cm³ kg^-1 seeds, respectively), recorded values of 19.33, 22.00 and 27.67 plants plot^-1 in the first season and 14.67, 17.67 and 23.33 plants plot^-1 in the second season, respectively, compared with those in the control (141.67 and 135.67), whilePlant guardgave 97.67 and 93.00 plants plot^-1 in both seasons, respectively. In the case of the number of rotted roots, results indicated that Rizolex-T 50% WP, Tendro 40% FS and Maxim XL 3.5% FS at recommended rate (3gm, 3.5 cm³ and 1 cm³ kg^-1 seeds, respectively) recorded 7.67, 9.33 and 16.00 plants plot^-1 in the first season and 4.33, 5.67 and 13.00 plants plot^-1 in the second season, respectively, in comparison with those in the control which gave 102.00 and 97.00 plants plot^-1 during both seasons, respectively. Concerning the number of survival plants, results showed that Rizolex-T 50% WP, Tendro 40% FS and Maxim XL 3.5% FS were the most effective fungicides. These fungicides at recommended rate (3 gm, 3.5 cm³ and 1 cm³ kg^-1 seeds, respectively) increased the survival plants to 621.33, 616.00 and 596.33 plants plot^-1 in the first season and 633.33, 627.33 and 601.67 plants plot^-1 in the second season comparing to those of control (226.67 and 246.00 plants plot^-1), respectively.

Generally, the recommended rates of treatments significantly (P= 0.05) decreased the number of pre- and post-emergence damping-off, rotted roots and subsequently increased the number of survival plants in comparison with half rate. However, certain exceptions were recorded. For example, no significant differences were observed between the effects of half recommended and the recommended rates (1.75 and 3.5 cm³ kg^-1 seeds) of Tendro 40% FS against pre-emergence damping-off, which recorded 25.33 and 22.33 plants plot^-1 in the second season (Table, 3) and Rizolex-T 50% WP at the same rates of application (1.5 and 3 gm kg^-1 seeds) in case of pre- and post-emergence damping-off, rotted roots and survival plants during both seasons (Tables 2 and 3).

The high efficacy of Rizolex-T 50% WP, Tendro 40% FS and Maxim XL 3.5% FS in reducing pre-emergence, post emergence damping-off and root rot diseases may be due to the high activity of these fungicides on fungal pathogens of the seed and root rot diseases including genera of Fusarium, Sclerotium, Pythium and Rhizoctonia. Efficiency of tested fungicides for controlling damping-off and root rot diseases in the present study are consistent with those described by several authors.Kataria et al. (2002)found that treatment of bean seeds with tebuconazole and tolclofos-methyl resulted in maximum protection to bean seedlings against pre- and post-emergence damping-off and yielded healthy seedling stands up to > 90 %. Theer (2012) recorded that pre- and post-emergence damping-off caused by Rhizoctonia solani and Fusarium oxysporum significantly decreased by using seed dressing fungicides (Rhizolex-T, Topsin-M and Basten).Mahmoud et al. (2018 b)found that Rizolex-T and Moncut were the most effective fungicides in reducing the percentages of pre- and post-emergence damping-off caused by F. solani and R. solani in faba bean.

On the other hand, several mechanisms were suggested to explain the role of biocontrol agent as antagonistic organisms in suppression phytopathogenic fungi and controlling diseases. Their action could be occurred through mycoparasitism (Haran et al., 1996; Viterbo et al., 2002 and Pierre et al., 2016) competition for nutrients and space (Inbar et al., 1994), production of antibiotics, stimulate plants for producing chemical defenses compounds, induced systemic resistance in plants (Ghisalberti and Rowland, 1993; Howell et al., 2000 and Morsy et al., 2005) and produced extracellular enzymes such as proteases, chitinases, glucanases,b-1-3-glucanase, protease and lipase (Chet and Inbar,1994; Harman, 2006 and Fernando et al., 2007 ). The obtained results are in agreement with those obtained by several researchers. El-Fiki et al. (2014) reported that treatment of bean seeds with Trichoderma harzianum, T. viride, Bacillus subtilis and Pseudomonas fluorescens at the different rates of 2, 4 and 8 gm kg^-1 seeds reduced the incidence of pre- and post-emergence damping off and increased crop parameters under greenhouse conditions in comparison to the control. Sowing coated bean seeds with Bacillus megaterium, B. subtilis, Pseudomonas fluorescens, Serratia marcescens, Trichoderma album, T. harzianum, T.   lignorum and T. viride significantly reduced the incidence of pre- and post-emergence damping- off with significant increase in the fresh and dry weight of roots and shoots compared with control treatment (Ahmed, 2016). Also, Abd-El-Khair et al. (2019) found that T. harzianum, T. viride, and T. virens significantly reduced the incidence of damping-off, root rot, wilt diseases and increased the percentage of survival bean plants under greenhouse and field conditions.

Side effect of seed treatments on nodulation number of rhizobium bacteria in common bean.

Data illustrated in Table (4) clearly indicated that, all the tested chemical fungicides, particularly Hattric 6% FS significantly (P=0.05) reduced the number of nodules per plant compared with the untreated control, except for Maxim XL 3.5% FS (at both rate of application) in the first season and at half recommended rate in the second season. Also, insignificant reduction in nodules number plant^-1 in both seasons was found when Rizolex-T 50% WP was used at half recommended rate. On the contrary, biofungicides significantly (P= 0.05) increased the number of nodules per plant compared with the untreated control, with the exception ofPlant guardwhich exhibited insignificant effect at half recommended rate in the first season and at both rates in the second season. These results were similar in the two consecutive growing seasons 2018 and 2019. For example, Hattric 6% FS at recommended rate (1cm³ kg^-1 seeds) reduced the number of nodules per plant to 2.80 and 4.00 during both seasons respectively, while Rhizo-N at recommended rate (4gm kg^-1 seeds) increased the number of nodules per plant to 28.03 and 30.40 during both seasons, comparing with those of the control (20.73 and 22.93), respectively.

Results indicated that, recommended rate of chemical fungicides significantly (P= 0.05) reduced the number of nodules per plant compared with the half recommended rate, with the exception of Maxim XL 3.5% FS at half recommended and recommended rates, that was insignificant during the two tested seasons. For example, significant differences were observed between the effects of the half recommended and recommended rates (1.75 and 3.5 cm³ kg^-1 seeds) of Tendro 40% FS on number of nodules per plant, which recorded 15.83 and 13.80 in the first season and 18.70 and 15.73 in the second season, respectively. In contrast, all biofungicides at recommended rate significantly (P= 0.05) increased the number of nodules per plant, except forPlant guardat half recommended and recommended rates resulted insignificant differences in the second season.

The harmful effect of chemical fungicides on rhizobium bacteria may be due to these fungicides disrupt the signaling between plants and rhizobia by blocking the communication between plant derived phytochemicals and Rhizobium Nod D receptors that plays an important role in initiating nodulation leading to a successful N₂ fixation (Fox et al., 2007). Also, fungicides reducing the inoculation viability, death of rhizobium cells, altering the root exudate composition and consequently acts on the molecular signals to the bacteria and alters the bacterial morphology and physiology (Andrés et al., 1998 and Dunfield et al., 2000). On the other hand, the nodulation on the roots of bean plants treated with biocontrol agents were increased may be due to stimulate the growth of Rhizobium phaseoli (Smith, 1996 and Baraka et al., 1998). Biocontrol agents such as Trichoderma spp. and Bacillus spp. increased number of nodules (Ragab, Mona et al., 2015; Baraka et al., 1998 and El-Dabaa et al., 2019).

The negative effects of fungicides on nodulation were observed by (Ahmed, 1997) who cited that Rizolex T at rates 3 kg seeds^-1 reduced the number of nodules in groundnut. Zilli et al. (2009) found that carbendazim + thiram and carboxin + thiram reduced soybean nodulation. Kintschev et al., (2014) reported that carbendazim + thiram (Product A), carbendazim + thiram (Product B), carboxin + thiram, fludioxonil + metalaxyl-M and fludioxonil + metalaxyl-M + thiabendazole led to a reduction in the nodulation of bean plants, especially for nodular mass.

Effect of seed treatments on some agronomic traits of common bean.

The data in Tables (5 and 6) indicated the effect of chemical and biological seed treatments on biological yield, seed yield and straw yield during the two tested seasons (2018 and 2019). These results showed that all treatments, at any rate of applications, were significantly (P= 0.05) increased biological yield, seed yield and straw yield in comparison with the untreated control during both seasons. As stated previously with other evaluation parameters, Rizolex-T 50% WP, Tendro 40% FS and Maxim XL 3.5% FS were the most effective fungicides in this respect whereas Plant guardwas the lowest effective one. For example, the application of Rizolex-T 50% WP, Tendro 40% FS and Maxim XL 3.5% FS at recommended rate (3gm, 3.5 cm³ and 1 cm³ kg^-1seeds, respectively) resulted in biological yield values 11.15, 10.97 and 10.43 kg plot^-1in the first season and 11.75, 11.55 and 10.87 kg plot-¹ in the second season, respectively, whereas the corresponding biological yield values of Plant guardwere6.15 and 6.53 kg plot^-1. On the other hand, the corresponding seed yield values of the same fungicides at the same application rate were 5.70, 5.62 and 5.43 kg plot-¹ in the first season and 6.05, 6.00 and 5.62 kg plot^-1 in the second season, respectively, while those of Plant guard were 3.35 and 3.48 kg plot^-1.

Regarding the examined rates of fungicides, and as expected, recommended rate significantly (P = 0.05) increment biological yield, seed yield and straw yield compared with half rate. For example, Hattric 6% FS at 0. 5 and 1 cm³ kg^-1 seeds significantly increased biological yield values from 8.42 to 9.40 kg plot^-1 in the first season and from 8.70 to 9.70 kg plot^-1 in the second season, respectively, while seed yield values were 4.42 and 4.95 kg plot^-1 in the first season and 4.50 and 5 kg plot^-1 in the second season, respectively. In addition, the same fungicide at the same rates of application significantly increased straw yield values from 4.00 to 4.45 kg plot^-1 in the first season and from 4.20 to 4.70 kg plot^-1 in the second season, respectively. Generally, chemical fungicides gave biological yield, seed yield and straw yield better than the bioagents and this may be resulted from the efficacy of these compounds in controlling damping-off and root rot diseases than bioagent compounds. Also, these results suggested that, most fungicides were more effective than bioagents (BCAs). These results are in agreement with those obtained by several authors. Shehata (2015) found that treatment common bean seeds with Rhizolex-T reduced percentage of pre- and post-emergence damping-off, increased the percentage of healthy survival plants and significantly increased number of pods/plant and seed yield compared with untreated control. Under field conditions highest reduction in the diseases incidences and increases in the percentages of bean yield (number and weight of pods plant^-1 and dry weight of 100 seeds) were induced by T. harzianum, followed by T. viride when used as seed treatment (El-Fiki et al., 2014). Also, Abd-El-Khair et al. (2019) reported that T. harzianum, T. viride and T. virens increased yield components of the survival dry bean plants.

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Table 1: The tested chemical fungicides and biofungicides.

Table 4: Effect of treatments on numbers of nodules per plant of common bean under field conditions during seasons 2018 and 2019.

 ^*Nodules number plant^-1 resulted from 5 plants collected randomly from each replicate at the flowering stage.

Table 2: Effect of treatments on pre- and post- emergence damping-off, rotted roots and survival plants of common bean under field conditions during season (2018).

^*Mean number of pre-emergence damping-off 15 days after sowing (DAS).

^**Mean number of post-emergence damping-off 45 DAS.

^***Mean number of infected plants by rotted roots 60 DAS.                        

^****Mean number of survival (healthy) plants 60 DAS.

Table 3: Effect of treatments on pre- and post- emergence damping-off, rotted roots and survival plants of common bean under field conditions during season

              (2019).

^*Mean number of pre-emergence damping-off 15 days after sowing (DAS).

^**Mean number of post-emergence damping-off 45 DAS.

^***Mean number of infected plants by rotted roots 60 DAS.                        

^****Mean number of survival (healthy) plants 60 DAS.

Table 5: Effect of treatments on biological yield, seed yield and straw yield of common bean under field conditions during season (2018).

Biological yield = weight of all plants in each plot (kg polt^-1)

Seed yield = weight of seeds in each plot (kg polt^-1)

Straw yield = weight of straw in each plot (kg polt^-1)

YOC % = yield over control (treatment – control / treatment ×100)

Table 6: Effect of treatments on biological yield, seed yield and straw yield of common bean under field conditions during season (2019).

Biological yield = weight of all plants in each plot (kg polt^-1)

Seed yield = weight of seeds in each plot (kg polt^-1)

Straw yield = weight of straw in each plot (kg polt^-1)

YOC % = yield over control (treatment – control / treatment