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BY 4.0 license Open Access Published by De Gruyter Open Access December 5, 2020

Trichoderma asperellum affects Meloidogyne incognita infestation and development in Celosia argentea

  • Alori Elizabeth Temitope EMAIL logo , Aluko Ajibola Patrick , Joseph Abiodun , Adekiya Aruna Olasekan , Aremu Charity Onye , Adebiyi Ojo Timothy Vincent , Adegbite Kehinde Abodunde , Ejue Wutem and Rutazaha JoanPaula Elliseus
From the journal Open Agriculture

Abstract

Due to the rise in cost and detrimental health and environmental consequences that accompany the use of nematicides, there is a need for a more eco-friendly and less expensive alternative to control root-knot nematode (Meloidogyne incognita). Nematode infestation reduces the quality and quantity of Celosia argentea Linn. A pot experiment was conducted in a greenhouse to determine the biocontrol efficacy of Trichoderma asperellum against M. incognita in C. argentea. The treatments consisted M. incognita infected C. argentea inoculated with 0, 2.2 × 107, 4.4 × 107, or 6.6 × 107 cfu/pot of T. asperellum. All doses of T. asperellum reduced the root-knot nematode population and root gall index. Growth and development of C. argentea were improved, indicating that T. asperellum has the potential to be used as a biocontrol agent in C. argentea production. The biocontrol activity of T. asperellum in C. argantea increased as the week went by until the plants attained full maturity. Hence, the control of M. incognita by T. asperellum depends on the developmental stage of the plant root system.

1 Introduction

Celosia argentea Linn. (family Amaranthaceae) is an annual, herbaceous, vegetable whose leaves, tender stems, and young flower spikes are eaten cooked (Daramola et al. 2015). The dried, ripe seed is reported to have medicinal properties because of its β-carotene, vitamin E, folic acid, ascorbic acid, phosphorus, calcium, iron, and protein contents (Tang et al. 2016). The leaves contain amaranthine (betacyanin), oxalic acid, and phytic acid (Tang et al. 2016). The production of C. argentea is challenged by the sedentary endoparasite root-knot nematode (Meloidogyne incognita; Daramola et al. 2015; Fabiyi et al. 2016), which causes 60–80% yield loss of C. argentea (Tang et al. 2016) due in part to stunted growth, rotted, and galled roots (Anwar et al. 2009). Current management of M. incognita in C. argentea production is with synthetic nematicides. Human health risk and environmental consequences accompany the use of synthetic nematicides (Fabiyi et al. 2016; Alori and Babalola 2018). Synthetic nematicides are also very expensive, thereby increasing the cost of C. argentea production. Hence, the need for a more eco-friendly and less expensive alternative that will pose no health risk.

Microbial inoculants are an effective, environmentally safe, alternative method of controlling plant diseases affecting vegetables (Radwan et al. 2012).

Microbial inoculants can improve plant growth and yield and can act as biocontrol agents against many crop pathogens (Zakaria et al. 2013; Alori and Babalola 2018). Whether they are efficacious in the production of C. argentea needs ascertaining. The study therefore evaluated the efficacy of Trichoderma asperellum as a biocontrol agent against M. incognita on C. argentea.

2 Materials and method

2.1 Collection of soil sample and sterilization of soil for pot experiment

Soil samples were randomly collected from a 0 to 15 cm depth at the Landmark Teaching and Research Farm Omuaran, Kwara State, Nigeria, at 80°9′N latitude and 50°61′E longitude. Soil samples were bulked to form a representative sample that was transported to the laboratory for testing. Samples were air-dried for 3 days and passed through a 2 mm sieve in preparation for analysis. Samples were wet sterilized in an autoclave at 121°C for 20 min.

2.2 Sources of C. argentea seeds and T. asperellum

Seeds of C. argentea, var. TLV8, were purchased from the National Horticultural Research Institute, Ibadan, Nigeria, and T. asperellum was obtained from the Microbiology (Nematology) Department, International Institute of Tropical Agriculture, Dar es Salaam, Tanzania.

2.3 Extraction of nematode juveniles

Galled roots of C. argentea plants were sourced from the Teaching and Research Farm of Kwara State University, Malete, Kwara State, Nigeria. Galled roots were washed gently with water to remove soil particles. Nematode eggs were extracted from 5 g of chopped galled roots (Hussey and Baker 1973). Density of extracted eggs was assessed by placing 2 mL of nematode suspension into dishes and counting was done at ×40 with a stereomicroscope (Doncaster 1962).

2.4 Pot experiment

Twelve plastic pots, 30 cm diameter, filled with 10 kg of sterilized soil were arranged in a completely randomized design in a screenhouse of the Landmark University Teaching and Research Farm. Four pots containing sterilized soil were inoculated with 0, 2.2 × 107, 4.4 × 107, or 6.6 × 107 cfu/pot of T. asperellum, replicated 3 times to make 12 pots. Two days after inoculation of the fungus, seeds of C. argentea were planted in pots, and the plants were thinned to two per pot after emergence. The plants were inoculated with approximately 1,000 second-stage juveniles (J2) of M. incognita/pot 1 week after emergence, which were added in 3 cm-deep holes around the plant base using the method of Iheukwumere et al. (1995). The experiment was comprised of the following treatments: 1,000 J2 of M. incognita only, 2.2 × 107 cfu/pot of T. asperellum + 1,000 J2 of M. incognita, 4.4 × 107 cfu/pot of T. asperellum + 1,000 J2 of M. incognita, or 6.6 × 107 cfu/pot of T. asperellum + 1,000 J2 of M. incognita, each replicated three times. Average temperature of the screenhouse during the experimental period was 25°C. Plants were supplied with tap water to field capacity at 6 am and 6 pm daily with a watering can.

Evaluations of responses began 3 weeks after planting (WAP). Data were taken weekly on plant height, number of leaves, and stem diameter. Root gall indices and egg counts were recorded after harvest. The scale used for rating roots for galling, or the root gall index, was based on Taylor and Sasser (1978), where 0 = no infestation, 1 = 1–5% of the root galled, 2 = 6–25% of the root galled, 3 = 26–50% of the root galled, 4 = 51–75% of the root galled, and 5 = 76–100% of the root galled.

2.5 Analysis of soil chemical characteristics

Soil chemical properties were determined before and after the experiment, such as soil pH with an electronic soil pH meter (Model 215; Denver Instrument, Colorado, USA), soil particle size analysis by the hydrometer method (Gee and Or 2002), organic matter content was determined using the wet oxidation method (Shamshuddin et al. 1994), and exchangeable bases (K, Mg, Na, and Ca) were determined by ammonium acetate method (Chapman 1965). To determine exchangeable acidity, 5 g of air-dried soil (sieved through 2 mm sieve) was weighed into a 250 mL conical flask. Fifty milliliters of 1 N potassium chloride (KCl) solution was added to the soil sample in the conical flask. The flask was shaken on a reciprocating shaker for 1 h, and the content was filtered through Whatman No. 42 filter paper. Twenty-five milliliters of the filtrate was pipetted into a 100 mL conical flask and 50 mL distilled water was added along with 5 drops of phenolphthalein indicator. The resulting solution was titrated with 0.01 N sodium hydroxide (NaOH) to a permanent pink end point. The volume of the base used was recorded to calculate the total exchangeable acidity (H + Al); the effective cation exchange capacity was determined by the summation of the exchangeable bases (Ca, Mg, Na, and K) and exchangeable acidity expressed in cmol/kg; the total soil nitrogen was determined by Macrokjedahl method (Bremner 1965); and the Bray1 method was used to determine the available phosphorus (Murphy and Riley 1962).

2.6 Data analysis

All data from the experiment were subjected to analysis of variance (ANOVA) using IBM SPSS statistical package (2012). Means were separated using Duncan’s multiple range test (P ≤ 0.05).

3 Results

3.1 Effects of T. asperellum on the population of nematode on gall index in C. argentea infected with M. incognita

Table 1 shows the population of M. incognita in infected C. argentea inoculated with T. asperellum. M. incognita was found to be the highest in plants treated with 1,000 second-stage juveniles (J2) of M. incognita only and lowest in plants that received 1,000 second-stage juveniles (J2) of M. incognita + 6.6 × 107 cfu/pot of T. asperellum.

Table 1

Effect of treatment on final nematode population and gall index

TreatmentNematode populationRoot gall
InitialFinalindex
1,000 second-stage juveniles (J2) of M. incognita only1,0002,098aa3.3b
2.2 × 107 cfu Trichoderma asperellum/pot + 1,000 second-stage juveniles (J2) of M. incognita1,000 920b3.0ab
4.4 × 107 cfu of T. asperellum/pot + 1,000 second-stage juveniles (J2) of M. incognita1,000 440c2.3a
6.6 × 107 cfu of T. asperellum/pot + 1,000 second-stage juveniles (J2) of M. incognita1,000 230d1.7a
  1. a

    Values in columns followed by the same letter are not significantly different, P ≤ 0.05, Duncan multiple range test.

The C. argentea that received 1,000 second-stage juveniles (J2) of M. incognita only had the highest mean for gall index at 3.3 and this mean was significantly different (P ≤ 0.05) from those plants treated with T. asperellum suspension except for those that received 1,000 second-stage juveniles (J2) of M. incognita + 2.2 × 107 of T. asperellum suspension.

3.2 Effect of T. asperellum on plant height of C. argentea infected with M. incognita

Table 2 reports the impact of T. asperellum on the height of C. argentea infected with M. incognita. It was observed that at 5 and 6 WAP, M. incognita-infected C. argentea inoculated with T. asperellum at the rate of 6.6 × 107 cfu/mL had significantly higher height than the untreated control. However, at 7 and 8 WAP, the application of T. asperellum at the rate of 2.2 × 107, 4.4 × 107, and 6.6 × 107 cfu/mL resulted in significantly higher height of C. argentea when compared to the control that was not treated with T. asperellum.

Table 2

Effect of Trichoderma asperellum on plant height of Celosia argentea infected with Meloidogyne incognita

Trichoderma asperellum application rate (cfu/mL)Plant height (cm)
3WAP4WAP5WAP6WAP7WAP8WAP
08.5a10.8a14.5b16.6b8.8c20.7c
2.2 × 1078.8a12.0a16.3ab19.6ab21.4b22.5b
4.4 × 1078.5a11.8a16.6ab20.1ab23.2ab25.9ab
6.6 × 1079.0a13.7a19.5a23.0a26.3a28.5a

WAP = weeks after planting.

Each value is a mean of three replicates.

Means followed by the same letter along the same column are not significantly different according to Duncan multiple range test (P ≤ 0.05).

3.3 Effect of T. asperellum on number of leaves of C. argentea infected with M. incognita

The effect of T. asperellum on the number of leaves of C. argentea infected with M. incognita is presented in Table 3. At weeks 5 and 6, the application of T. asperellum at 6.6 × 107 cfu/mL significantly increases the number of leaves compared with the uninoculated C. argentea in the presence of M. incognita. However, at weeks 7 and 8, the application of T. asperellum at 2.2 × 107, 4.4 × 107, and 6.6 × 107 increased the number of leaves of C. argentea infected with M. incognita.

Table 3

Effect of Trichoderma asperellum on the number of leaves of Celosia argentea infected with Meloidogyne incognita

Trichoderma asperellum application rate (cfu/mL)Number of leaves
3WAP4WAP5WAP6WAP7WAP8WAP
07.0a9.0a12.0b13.7b15.3c16.7c
2.2 × 1076.7a9.7a13.3a,b16.3a,b18.3b20.3b
4.4 × 1076.7a10.0a14.0a,b17.3a,b19.3a,b22.7a,b
6.6 × 1077.0a12.0a16.0a19.3a21.7a24.0a

WAP = weeks after planting.

Each value is a mean of three replicates.

Means followed by the same letter along the same column are not significantly different according to Duncan multiple range test (P ≤ 0.05).

3.4 Interactive effects of T. asperellum and WAP on growth parameters of C. argentea infected with M. incognita

Table 4 reports the impact of the interactive effects of T. asperellum and WAP on the growth parameters of C. argentea infected with M. incognita. The treatment (inoculants, WAP) effects on measured plant growth parameters were significant (P ≤ 0.05). It was observed that inoculation of M. incognita-infected C. argentea with T. asperellum significantly increased the plant height and the number of leaves.

Table 4

Interactive effect of Trichoderma asperellum and WAP on growth parameters of Celosia argentea infected with Meloidogyne incognita measured over time

Plant heightNumber of leaves
Weeks after planting
38.70e6.85f
412.08d10.18e
516.73c13.83d
619.83b16.65c
719.93b18.65b
824.41a20.93a
Microbial inoculants
1,000 second-stage juveniles (J2) of M. incognita only13.33d12.28d
2.2 × 107 cfu/pot of T. asperellum + 1,000 second-stage juveniles (J2) of M. incognita16.77c14.10c
4.4 × 107 cfu/pot of T. asperellum + 1,000 second-stage juveniles (J2) of M. incognita17.68b15.00b
6.6 × 107 cfu/pot of T. asperellum + 1,000 second-stage juveniles (J2) of M. incognita20.00a16.67a
ANOVA response
Week0.000.00
Inoculants0.000.00
Week × inoculants0.000.00

Values in columns followed by the same letter are not significantly different according to Duncan multiple range test (P ≤ 0.05).

Likewise, the interactive effect (inoculant × weeks) on measured growth parameters was significant. This implies that the interaction between T. asperellum with the C. argantea seedling root increases as the week goes by.

3.5 Effects of T. asperellum on chemical composition of the soil used

The result in Table 5 shows that the application of microbial inoculants caused a significant change in the mineral composition of the soil after harvesting. The pH of the soil where plants were treated with M. incognita only increased by 13%, while the soil where plants were treated with M. incognita + 2.2 × 107 cfu/pot of T. asperellum, M. incognita + 4.4 × 107 cfu/pot of T. asperellum, and M. incognita + 6.6 × 107 cfu/pot of T. asperellum caused up to 7% reduction in pH. There was an increase in all the mineral contents of the soil of plants treated with M. incognita + 2.2 × 107 cfu/pot of T. asperellum, M. incognita + 4.4 × 107 cfu/pot of T. asperellum, and M. incognita + 6.6 × 107 cfu/pot of T. asperellum when compared with the composition at the start of the experiment (Table 5).

4 Discussion

4.1 Effects of T. asperellum on the population of nematode on gall index in C. argentea infected with M. incognita

The higher the rate of application of T. asperellum, the lower the population of M. incognita in infected C. argentea. This may be due to the ability of the fungi conidial to get attached to the eggs and cause immobilization of the second-stage juvenile of the nematode (Mascarin et al. 2012). Second, Trichoderma strains are reported to colonize root systems in many plants, thereby coordinating the defense mechanisms of host plant (Hermosa et al. 2012).

The result on galling index reflects a similar trend with regard to the number of nematodes because nematodes determine the presence of root galls in the root system of C. argentea plants, meaning the number of nematodes is directly proportional to galling index. Since T. asperellum caused immobilization of the second-stage juvenile of the nematode, galling cannot occur. Mechanisms of Trichoderma spp. to control plant pathogen include parasitism and antagonism. Trichoderma spp. induce systemic resistance in plants (Harman 2006).

4.2 Effect of T. asperellum on growth parameters of C. argentea infected with M. incognita

Significant increase in plant height and the number of leaves observed by reason of inoculation of M. incognita-infected C. argentea could be attributed to the reduction in nematode population and galling index as shown in Table 1. T. harzianum (T22) was reported to increase the growth of maize (Akladious and Abbas 2012). Also, according to Bíró-Stingli and Tóth (2011), northern root-knot nematode-infected green pepper treated with T. asperellum experiences up to 18% increase in height compared to the untreated control. T. harzianum caused an increase in the growth of M. javanica-infected tomato (Javeed and Al-Hazm 2015).

4.3 Interactive effects of T. asperellum and WAP on growth parameters of C. argentea infected with M. incognita

Increased plant height and number of leaves could be attributed to the reduction in nematode population and galling index (Table 1). The improved growth recorded in this research could also be attributed to increased nutrient status of the soil because of the application of T. asperellum as seen in Table 5. Alori and Babalola (2018) reported that microbial inoculants effectively control plant pathogens by either direct or indirect mechanism. They improved plant growth by the production of plant growth hormones. However, T. asperellum spp. increased plant growth due to increased nutrient uptake (Harman 2006).

The interaction between T. asperellum and WAP depends on the developmental stage of the plant root system, which improves with the age of the plant. Idowu et al. (2016) reported a similar effect.

4.4 Effects of T. asperellum on the chemical composition of the soil used

A reduction in pH recorded in pots treated with T. asperellum probably accounts for the reduction in nematode population and root gall index.

Also, increase in all the mineral contents of the soil when compared with the composition at the start of the experiment as recorded in Table 5 agrees with the findings of many researchers; Marathe et al. (2011) reported that microbial inoculant application resulted in improved soil fertility status and plant nutrient uptake. A significant increase in organic carbon content of the soil was noted by reason of inoculation of groundnut with microbial inoculants such as T. viride, T. harzianum, and Bacillus megaterium (Prasad et al. 2017). This could be due to the ability of these organisms to accelerate decomposition of organic matter and the mineralization of both micro- and macronutrients in the soil (Xu and Li 2017; Table 5).

Table 5

Effects of Trichoderma asperellum on chemical composition of the soil used

Soil chemical property1,000 second-stage juveniles (J2) of M. incognita only2.2 × 107 cfu/pot of T. asperellum + 1,000 second-stage juveniles (J2) of M. incognita4.4 × 107 cfu/pot of T. asperellum + 1,000 second-stage juveniles (J2) of M. incognita6.6 × 107 cfu/pot of T. asperellum + 1,000 second-stage juveniles (J2) of M. incognitaInitial chemical property of soilValue
pH (H2O) 1:26.56a5.43d5.48c5.71bpH (H2O) 1:25.84 ± 0.1
Total N (%)2.20b2.69ab2.65ab2.85aTotal N (%)0.30 ± 0.1
Avail. P (g/kg)16.99c14.88d27.56b29.67aAvail. P (g/kg)12.50 ± 0.5
Organic matter (%)1.52c2.00a1.74b1.95aOrganic matter (%)1.8 ± 0.01
Na+ (cmol/kg)0.74d0.78c0.88a0.80bNa+ (cmol/kg)0.05 ± 0.01
K+ (cmol/kg)0.47c0.45c0.55b0.61aK+ (cmol/kg)0.07 ± 0
Ca2+ (cmol/kg)3.28c3.16d3.97b4.11aCa2+ (cmol/kg)0.4 ± 0.1
Mg+ (cmol/kg)0.95d1.01c1.23b1.42a
Al+ H (cmol/kg)0.05a0.07a0.07a0.06a
ECEC (cmol/kg)5.48c5.47c6.70b7.00a

ECEC = effective cation exchange capacity.

Values in rows followed by the same letter are not significantly different according to Duncan multiple range test (P ≤ 0.05).

5 Conclusion

Trichoderma asperellum improved the growth and development of C. argentea infected with M. incognita, indicating that T. asperellum has the potential to be used as a biocontrol agent in C. argentea production. The biocontrol activity of T. asperellum in C. argantea increased as the week went by until the plants attained full maturity. Hence, the control of M. incognita by T. asperellum depends on the developmental stage of the plant root system.

  1. Conflict of interest: The authors declare no conflicts of interest.

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Received: 2020-03-27
Revised: 2020-05-19
Accepted: 2020-06-04
Published Online: 2020-12-05

© 2020 Alori Elizabeth Temitope et al., published by De Gruyter

This work is licensed under the Creative Commons Attribution 4.0 International License.

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