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Sustainable Management of the Southern Root-knot Nematode, Meloidogyne incognita (Kofoid and White) Chitwood, by Means of Amendments of Fumaria parviflora.

Byline: Ishrat Naz, Saifullah, Juan Emilio Palomares-Rius, Vivian Blok, Shah Masaud Khan, Sardar Ali and Ayesha Baig

Abstract

Greenhouse and field studies were conducted in the spring and autumn of 2010 to test the efficacy of dry amendments of Fumaria parviflora as a form of eco-friendly management of Meloidogyne incognita in tomato. Various preparations of F. parviflora (in the form of dry root, stem, leaf and whole plant powder) at different dose rates (10, 20 and 30 g per kg of soil) significantly reduced levels of M. incognita in the roots of tomato cv. Rio Grande, and promoted plant growth. The root amendments of F. parviflora at the highest application dose (30 g per kg of soil) were the most effective, significantly reducing the number of galls, the galling index, the egg masses per g of the root, and the adult females per g of the root. Shoot and root lengths, the fresh and the dry shoot weight, and the number of branches and flowers per plant were improved in greenhouse trials that were conducted in the spring and autumn.

Under naturally infested field conditions, the root's amendment of F. parviflora at the highest application dose was the most effective, and reduced the number of galls, the GI, the number of egg masses per g of root, the adult females per g of root, and the reproduction factor (Rf). It also promoted plant, health and increased the number of fruits per plant and the fruit weight per plant in the spring and autumn experiment. Dry amendments of F. parviflora have remarkable nematicidal potential and could be used as an effective and environment- friendly management tool against M. incognita as an alternative to chemical control. Copyright 2015 Friends Science Publishers

Keywords: Fumaria parviflora; Meloidogyne; Tomato; Dry amendments; Eco-friendly management

Introduction

Root-knot nematodes (RKNs) (Meloidogyne spp.) are obligate endoparasitic polyphagous pests of tomato that are found throughout the world (Sasser and Freckmann, 1987). Their worldwide distribution, extensive host ranges, and their involvement with fungi, bacteria and viruses in disease complexes rank them among the top major plant pathogens, mainly in developing countries (Sasser, 1980). Three species of RKNs, namely Meloidogyne incognita, M. javanica and M. arenaria, are the major RKNs in subtropical and tropical countries (Moens et al., 2009). Within these species, the most important, worldwide, is M. incognita (Sasser, 1980). These three species are widely distributed in Pakistan, and particularly in the Khyber Pakhtunkhwa province, where the disease is 100% prevalent in tomato fields (Naz et al., 2012).

Globally, many synthetic nematicides have been effectively used to suppress RKNs in the soil. However, most of them have now been banned because of the health and environmental issues that are associated with their use and production, as well as with the emergence of resistant RKN strains (Conway, 1995). In addition, synthetic nematicides may affect the agro-ecological system, and have a detrimental effect on other beneficial parasites, predators and other soil-dwelling microbes (Faruk et al., 2011). Plant resistance is one of the most effective and economically viable methods of controlling RKN. However, plant resistance is not available in many important crops, and effectiveness is often restricted to a few races of a nematode genus (Whitehead, 1998).

The development of a resistant variety is a long-term and laborious process (Isakeit and Jaster, 2005), with some of them being locally unavailable to the growers in such developing countries as Pakistan (Saifullah, pers. comm.). The resistant tomato-carrying Mi-1 gene has conferred resistance against M. incognita, M. javanica and M. arenaria (Medina-Filho and Stevens, 1980). This resistance breaks down under high (above 28C) soil temperatures (Dropkin, 1969), and leads to the emergence of virulent strains in the field by way of high selection pressure, as a result of the reiterated use of said gene (Verdejo-Lucas et al., 2009), favouring its use within an integrated management context (Sorribas et al., 2005). Therefore, nematologists are currently looking for alternative and novel strategies for the effective management of these pests, or for their integration with other strategies, in order to obtain more congruent and economically viable results.

Presently, researchers have diverted their attention to managing plant-parasitic nematodes through the use of plant-derived safe phytochemicals (PACopyrightrez et al., 2003; Naz et al., 2013a), organic amendments and biopesticides (Faruk et al., 2011). The use of phytochemical compounds and natural plant extracts has substantially reduced the number of M. incognita disease galls, and the extent of reproduction occurring on, tomato plants (Naz et al., 2013a, b). More specifically, the decomposition of organic residues from some green manure oily plant residues, such as cottonseed meal, or from meal from certain types of mustard, have been reported as releasing toxic ammonia, organic acids and other compounds as a by-product that can kill nematodes (Oka, 2010; McSorley, 2011; Thoden et al., 2011).

Amendments from a number of plants, including the castor oil plant (Ricinus communis), velvet bean (Mucuna spp.), marigold (Tagetes spp.), and sunn hemp (Crotalaria juncea), neem cake, Rakshak gold (a neem-based product) and cruciferous plants have been used successfully against RKNs (Randhawa et al., 2002; Wang et al., 2002; Hooks et al., 2010). Plants, in their entirely or in parts, can be used as soil amendments, either fresh or in dry form, as has been demonstrated in one study on chickpea, in which soil amendments with flowers, leaves, roots, and seeds of Chrysanthemum coronarium, and with flowers from Chrysanthemum segetum, Calendula maritime, Calendula officinalis, and Calendula suffruticosa, showed differential effects on M. artiellia eggs and juveniles (PACopyrightrez et al., 2003).

Previously, in vitro and in planta nematicidal activity of Fumaria parviflora Lam (Fumariaceae) extracts was evaluated against the southern RKN, M. incognita, and different classes of bioactive nematicidal compounds, namely tannins, saponins, steroids, flavonoids, glycosides, alkaloids, and phenols were detected in the plant roots and stem (Naz et al., 2013a). Powdered aerial parts of F. parviflora have been shown to possess antibacterial activity (Vahabi et al., 2011), whereas almost no information has yet been made available on the nematicidal activity of F. parviflora used as organic amendments. In the present paper, nematicidal activities of F. parviflora was reported on M. incognita populations using tomato plants, and the beneficial increase of plant growth parameters under artificially inoculated greenhouse and naturally infested field conditions.

Materials and Methods

Collection of Fumaria parviflora and the Preparation of Dry Amendments

Mature F. parviflora plants were collected in the months of March-April 2010 from the wheat fields of the Agriculture Research Farm, Malkandher, the University of Agriculture, Peshawar. The plants were authenticated, and the voucher specimen no. ISH-1732 was deposited in the herbarium of the Department of Botany, the University of Peshawar (Naz et al., 2013a). Plants were washed in running tap water and separated into stem, leaves and roots, whereas some plants were left intact. All the plant parts, including those that were intact, were dried in an oven at 45C for one week, and later gently ground to a particle size of 1 mm (Naz et al., 2013a). The powdered plant material was stored at room temperature (25C) in paper bags prior to use.

In planta Experiment using Dry Powder Application of Fumaria parviflora and Tomato cv. Rio Grande during the Spring and Autumn of 2010 The experiments were carried out in a greenhouse of the Plant Pathology Department, the University of Agriculture, Peshawar (30 5C temperature, 70.0% relative humidity, and a 16 h photoperiod of fluorescent light). A tomato nursery (cv. Rio Grande) was raised in steam-sterilised sandy loam soil. About two-week-old tomato seedlings (one plant/pot) were transplanted into clay pots (15 cm mouth wide or 75 mm diameter) containing 1000 cm3 (sand: clay loam, 2:1, v/v) that had been steam-heated at 100C for 6 h (Naz et al., 2013a) to kill potential plant pathogens. For experimental treatments, the potting mixture was amended with powdered and homogenised plant material (in the form of stem, root, leaf, and whole plant powder) of Fumaria parviflora at 10, 20 and 30 g per kg of soil. Unamended soil and only inoculated soil served as controls.

Each treatment was replicated ten times, and the pots were arranged on benches in a screen house in a completely randomised design (CRD) with factorial arrangement. The nematodes were obtained from pure culture on cv. Rio Grande tomato and eggs were extracted from the roots with 0.5% NaOCl (Naz et al., 2013b). A total of 4000 10 eggs of M. incognita (contained in a 100 mL of H2O) were applied at the root zone of a tomato seedling using a sterilised pipette three days after transplanting (Naz et al., 2013b) in the amended soil. Plants were watered daily with 50 mL tap water, and fertilised with slow-release fertilisers (14-14-14, N-P-K) (Sasser, 1990) at 5 g per kg of soil at the beginning of the experiment. The experiment was evaluated 60 days after inoculation. The shoot of each plant was cut off at the soil level, and the roots were washed with tap water.

Egg masses from the roots were extracted after exposure to 1% NaOCl for 5 min (Hussey and Barker, 1973). The severity of nematode galling of the root system was then assessed (Taylor and Sasser, 1978). The experiments were conducted twice during the spring and autumn of 2010, and data were recorded on number of galls per root system, galling index (GI), number of egg masses per g of the roots, number of adult females per g of root, shoot and root lengths (in cm), the fresh root weight (in g), fresh and the dry shoot weight (in g), number of flowers per plant, and number of branches per plant.

Field Experiments using Dry Powder Application of Fumaria parviflora in the Spring and Autumn of 2010 Growing Seasons

Field experiments were carried out during the spring and autumn of 2010 growing season in M. incognita naturally infested fields of Dargai, Khyber Pakhtunkhwa, Pakistan. Pre- and post treatment Meloidogyne spp., densities were calculated by taking 20 soil cores with the help of cylindrical sampling tube (10 cm diameter and 25 cm deep) from each plot and Baremann pan method (Southey, 1986). Initial and final densities were used to calculate the reproduction factor (Rf). Both experiments were performed in the same field of Dargai, using a susceptible tomato cv. Rio Grande. A nursery was raised in steam-sterilised soil (100C for 6 h) in clay pots, and four-weeks-old tomato seedlings were transplanted into the naturally infested fields of Dargai. Five days after transplantation, dry powder of F. parviflora (consisting of stem, root, leaf, and whole plant powder) (at 10, 20 and 30 g per plant) were applied close to the tomato rhizosphere.

The control plants were not treated with any of the plant amendments (0 g per plant). The experiments were laid out in a randomised complete block design (RCBD) with factorial arrangement. A total of ten replications were taken with plant-to-plant and row-to-row distance of 30 and 60 cm, respectively, whereas each replication consisted of two sub-rows, with 12 plants in each row. Normal agronomic practices used in the area (e.g irrigation, fertilisation, and earthing up near the root zone and hand weeding) were continued during the course of the experiments. Data were recorded on four randomly selected plants (two from each sub-row), and pooled as a means. The plants were carefully uprooted, separately labelled, and brought to the laboratory.

The shoots were cut off at the soil line, the roots were washed gently with running tap water, and the data obtained were recorded on the following parameters: the number of galls per plant root system, GI, number of egg masses per g of root, number of adult females per g of root, reproduction factor (Rf = Pf/Pi; the final/initial nematode numbers); shoot and root lengths (in cm), fresh and dry shoot weight (in g), fresh root weight, number of flowers per plant, the number of branches per plant, number of fruits per plant, and fruit weight per plant (in kg), after three months. The roots were scored for GI, using a rating scale of 0-5 on the galling scale (where 0 = no gall on the roots; 1 = 1-2; 2 = 3-10; 3 = 11-30; 4 = 31-100; 5 = more than 100 galls per root) (Taylor and Sasser, 1978). Galled roots (1 g each) were stained for 15-20 min in an aqueous solution of phloxine B (15 mg per L). Egg masses were counted with the help of a stereomicroscope.

Other agronomic parameters assessed were shoot and root lengths, number of flowers and branches per plant, and number and weight of fruit obtained (kg per plant). Chemical and physical properties of the field, namely the pH (7.3-7.9), the organic matter contents (9.9-11.0 g/kg of soil), the electrical conductivity (EC) (0.18-0.21 dSm-1), the soil texture (29.9% sand, 23.0% clay, and 47.1% silt in 1 kg soil, at a depth of 30 cm), were all assessed in the Soil and Pesticide Chemistry Department (Agricultural Research Institute (ARI), Tarnab, Peshawar).

Statistics

Data of greenhouse and field trials were subjected to analysis of variance (ANOVA) using Statistix (NH Analytical Software, Roseville, MN, USA) (Campbell and Madden, 1990). Treatment means of the different parameters were compared using Fisher's protected least significant difference (LSD) test at P = 0.05 (Gomez and Gomez, 1984).

Results

Effect of Dry Amendments of Fumaria parviflora on Meloidogyne incognita on Tomato and Plant Growth Parameters in the Greenhouse Conditions Results of the greenhouse trials for both growing seasons indicated that tomato plants, amended with different dry powder of F. parviflora at different application doses, significantly (P less than 0.05) reduced the nematode parameters, and promoted the plant growth parameters. In the spring 2010 trial, the root powder at all application doses (10, 20 and 30 g per kg) effectively suppressed M. incognita on tomato plants (Table 1). The number of galls per plant (23.00), the GI (1.13), the egg masses per g of the root (17.75), and the number of adult females per g of root (8.00) were drastically reduced (P less than 0.05), with the root amendments at 30 g per kg application dose, in comparison to the control.

The stem powder, at all application doses, ranked second and reduced the number of nematode galls per plant, the GI, the number of egg masses per g of root, and the number of females per g of root by 61.20, 59.18, 61.63 and 72.41% respectively, over the untreated control (0.0 g per kg), at the highest dose of 30 g per kg. Plant growth parameters, namely the shoot length, the root length, the fresh shoot weight, the dry shoot weight, and the number of branches and the number of flowers per plant were significantly (P less than 0.05) increased by 50.70, 69.49, 146.40, 102.00, 109.67 and 53.44% over the untreated control at 30 g per kg root dose application (Table 1). Plant growth parameters improved significantly with the application of dry amendments other than the roots (Table 1).

In the 2010 autumn trial, all the treated groups showed significant reduction (P less than 0.05) in the nematode parameters, compared to the untreated control (Table 2). The number of nematode galls per plant (32.0), the GI (1.50), number of egg masses per g of the root (26.00), and the number of females per g of the root (8.70) were markedly reduced (P less than 0.05), with the roots amendments applied at 30 g per kg dose rate (Table 2). A maximum increase in the disease severity and in the GI was observed in the control treatments at 0.0 g per kg dose rate. An increase in the dose rate of all amendments significantly reduced M. incognita on tomato plants at all application doses, compared to the respective control dose (0.0 g per kg) (Table 2). Results of the 2010 autumn trials on the plant growth parameters were similar to those observed in the 2010 spring trial.

All the plant growth parameters, for example, the shoot and root lengths, the fresh and the dry shoot weight, the number of branches and flowers per plant showed differential results with an increase in the dose rate of the amended material, used as root, stem, leaf, or whole plant powder. Amongst the plant powder material applied, the dry root and stem powder showed very different results at the highest dose rate of 30 g per kg, and enhanced all the plant growth parameters studied under the 2010 autumn greenhouse conditions (Table 2).

Effect of Dry Amendments of Fumaria parviflora on Meloidogyne incognita on Tomato Plants and Plant Growth Parameters under Naturally Infested Field Conditions of Dargai Data recorded under natural field conditions of Dargai in the spring of 2010 showed the nematicidal potential of all amendments (Table 3). All forms of F. parviflora preparations at the three different dose rates reduced (Pless than 0.05) the number of galls, the GI, the number of egg masses per g of the root, the number of females per g of the root, and the Rf markedly, compared to the control treatments (Table 3). The fresh root weight was the highest in the control treatments.

The highest dose of 30 g per plant resulted in outstanding reduction (P less than 0.05) in gall numbers, in the GI, and in other nematode parameters, whereas the maximum increase in such plant growth parameters as the shoot and root lengths, the fresh and the dry shoot weight, the number of branches and flowers per plant, the number of fruits per plant and the fruit weight per plant was recorded (Table 3).

Results of the 2010 autumn field experiment showed significant (P less than 0.05) efficacy of the dry amendments of F. parviflora (using the root, stem, leaf and whole plant powder) applied at 10, 20 and 30 g per plant dose rate (Table 4). At the 30 g per plant dose rate, the number of galls induced by M. incognita reduced drastically (P less than 0.05) in all those treatments, where dry amendments were applied. Plants amended with the root powder of F. parvilora had a strong effect on the nematode invasion, and displayed maximum nematicidal activity. The number of galls per plant (31.0), the GI (1.25), the number of egg masses per g of root (45.25), and the number of females per g of root (40.25) were the lowest for the root amendments, whereas the dry stem powder ranked second at the highest dose rate (Table 4). The leaf and stem powder, at all application rates, markedly reduced the amount of nematode growth and reproduction that occurred in the tomato plant roots.

The Rf was reduced to a minimum of 0.13 and 0.5 in the plants amended with the root and stem powder, as compared to the untreated controls, which gave Rf values of 1.9 and 2.0, respectively. Plants in the control treatments showed heavily galled roots and the highest fresh root weight. The shoot and root lengths (48.50 and 21.50 cm), the fresh and the dry shoot weight (55.00 and 27.00 g), and the number of branches and flowers per plant-1 (20.00 and 65.00) were the maximum in the treatments, where F. parviflora root preparations were applied at the highest dose rate. Compared to the control plants, the maximum number of fruits per plant and increase in fruit weight was recorded in treatments using any form of the F. parviflora preparations. The root powder showed an increase of 157.30 and 83.96% in the number of fruits per plant and in fruit weight, respectively, over the control plants (Table 4).

Discussion

The use of plants as nematicidal or nematostatic products has been regarded as effective, economical and eco-friendly by numerous researchers (Chitwood, 2002). A study that was conducted under greenhouse and naturally-infested field conditions in the spring and autumn of 2010 revealed the promising effect of F. parviflora against M. incognita on tomato plants. A variety of preparations (using the root, stem, leaf and whole plant powder) and doses (10, 20 and 30 g per kg) of F. parviflora effectively suppressed M. incognita on tomato plants, and promoted the plant growth parameters. The in planta study clearly demonstrated that the number of nematode galls on tomato roots, the GI, and the number of egg masses, and the number of adult females, per g of root were significantly reduced by means of the application of various preparations of F. parviflora. Nevertheless, the root doses gave very effective results, both in the greenhouse and in the field trials.

Under natural field conditions, the dry root powder application of F. parviflora exhibited maximum reduction in the number of galls per plant (39.25 and 31.00), and in terms of the GI (1.87 and 1.13), in comparison to the corresponding controls. The stem powder ranked second in nematicidal effect at all doses. This study demonstrated that the variation in the reduction of the number of galls per plant, the GI, and the other parameters of parasitism was positively influenced by the different application doses used.

Table 1: Effect of dry powder of Fumaria parviflora on nematicidal properties of Meloidogyne incognita on tomato and plant growth parameters under green-house conditions (spring, 2010)a

Plant parts and Galls###GIb###Egg masses Adult females Shoot###Root length Fresh shoot Dry shoot Number of###Number of

###-1

doses (g kg-1)###plant-1###g-1 of root g of root###length (cm) (cm)###weight (g) weight (g) branches plant-1 flowers plant-1

Roots

0###80 a###4.70 a###65.75 ab###41.25 c###26.25 j###5.72 f###19.33 gh###8.48 fg###7.75 e###29.00 ef

10###46.75 c 1.87 e###28.00 gh###19.00 fgh###48.75 b###13.38 b###24.88 ef###8.33 fg###9.25 cde###33.00 cde

20###36.75 de 1.63 ef 24.50 hi###17.75 gh###52.50 a###12.88 b###38.88 bc###14.55 b###12.00 bc###37.50 bc

30###23.0 f###1.13 f###17.75 i###8.00 i###53.25 a###18.75 a###47.63 a###17.13 a###16.25 a###44.50 a

Stem

0###74.75 a 4.90 a###61.25 b###58.00 a###28.75 i###5.80 f###19.38 gh###7.70 g###10.00 cde###25.50 f

10###44.50 cd 2.85 d###36.00 def 25.50 def###37.75 ef###10.25 cd###20.50 gh###9.10 f###9.25 cde###33.00 cde

20###38.25 d 3.00 cd 30.50 fgh 26.25 de###41.50 c###11.50 bc###27.25 e###12.13 cd###11.50 bcd###38.00 b

30###29.00 ef 2.00 e###23.50 hi###16.00 h###38.75 de###12.38 b###32.00 d###12.50 c###13.25 b###39.00 b

Leaves

0###79.25 a 4.82 a###69.00 a###56.50 ab###26.50 j###5.72 f###19.20 gh###7.50 g###8.75 de###26.75 f

10###62.50 b 3.85 b###44.00 c###31.25 d###35.50 h###7.75 ef###20.05 gh###9.30 f###9.00 de###28.50 ef

20###61.25 b 3.53 bc 41.25 cd###22.75 efgh###38.50 de###9.23 de###24.50 ef###10.50 e###9.500 cde###32.00 de

30###56.50 b 3.03 cd 36.00 def 22.75 efgh###39.00 d###11.70 bc###22.13 fg###11.25 de###8.75 de###36.50 bcd

Whole plant

0###81.00 a 4.82 a###69.50 a###50.50 b###28.50 i###5.80 f###18.42 h###8.25 fg###7.25 e###25.00 f

10###60.25 b 3.47 bc 40.75 cd###27.00 de###35.75 gh###7.15 ef###35.50 c###12.50 c###7.75 e###29.25 ef

20###58.25 b 3.25 cd 38.75 cde 23.25 efg###36.75 fg###10.13 cd###37.75 c###14.63 b###9.75 cde###35.25 bcd

30###39.0 cd 3.03 cd 32.25 efg 17.00 gh###35.50 h###11.52 bc###41.20 b###17.75 a###10.00 cde###35.50 bcd

LSD values###3.92###0.28###3.76###3.4###0.62###1.04###1.69###0.57###1.39###2.36

Table 2: Effect of dry powder of Fumaria parviflora on nematicidal properties of Meloidogyne incognita on tomato and plant growth parameters under green-house conditions (autumn, 2010)a

Plant parts and Galls plant-1 GIb###Egg masses Adult females Shoot length Root length Fresh shoot Dry shoot Number of###Number of

###-1###-1

doses (g kg-1)###g-1 of root g of root###(cm)###(cm)###weight (g) weight (g) branches plant###flowers plant-1

Roots

0###99.25 a###4.87 a###98.00 a###70.75 ab###30.25 efgh###7.82 fgh###18.13 gh###7.47 gh###8.75 de###23.00 ef

10###63.5 de###3.00 ef###50.50 fg###20.75 gh###38.25 bc###9.52 de###23.40 ef###7.62 g###10.25 cde###26.25 def

20###50.75 f###2.50 f###45.00 g###16.75 h###41.50 b###15.63 b###34.75 c###14.95 c###14.25 b###37.75 b

30###31 g###1.50 g###26.00 h###8.750 i###52.50 a###20.00 a###55.70 a###19.13 a###17.25 a###48.75 a

Stem

0###100.3 a###5.00 a###94.00 a###67.50 b###28.75 gh###8.00 fg###24.27 def 5.30 i###11.00 cd###21.75 f

10###78.75 b###3.62 bcd 62.00 de###34.25 e###29.25 efgh###9.22 def###20.75 efg 8.62 fg###10.25 cde###28.50 cde

20###63.75 cde 3.25 de 56.25 ef###26.50 f###31.25 defgh 12.00 c###21.63 efg 9.25 ef###12.25 bc###32.25 bc

30###48.75 f###2.50 f###44.00 g###19.75 h###34.00 cde###12.07 c###25.72 de###12.13 d###14.00 b###36.75 b

Leaves

0###103.8 a###4.92 a###97.50 a###75.50 a###29.00 fgh###6.40 h###23.95 def 5.77 i###9.75 de###21.75 f

10###75.50 b###4.07 b###82.50 b###51.75 c###28.50 gh###8.00 fg###19.38 fg###6.10 hi###8.25 e###23.00 ef

20###71.50 bc###3.50 cde 74.75 bc###42.75 d###33.75 cdef###12.13 c###22.10 efg 8.75 fg###10.50 cde###28.50 cde

30###61.50 e###3.25 de 66.50 cd###33.00 e###26.75 h###12.32 c###23.55 ef###10.43 e###9.75 de###29.50 cd

Whole plant

0###106.8 a###5.00 a###93.25 a###74.00 a###27.25 gh###7.00 gh###13.20 h###8.02 fg###8.25 e###23.50 ef

10###71.00 bcd 3.62 bcd 73.25 c###52.25 c###31.75 defg###8.40 efg###17.38 gh###10.63 de 8.75 de###27.25 cdef

20###71.25 bcd 4.00 bc 64.25 de###41.50 d###30.00 efgh###10.13 d###28.83 d###15.50 c###10.75 cd###25.50 def

30###66.75 cde 2.62 f###49.00 fg###26.00 fg###35.50 cd###12.75 c###42.20 b###17.50 b###10.75 cd###35.75 b

LSD values###3.92###0.52###4.5###2.8###2.41###0.74###2.55###0.76###1.2###2.77

The data for nematicidal activity of Fumariaceae agreed with the results of our previous studies, where the n-hexane and methanol root extracts of the plant significantly reduced the number of nematode galls, the GI, the number of egg masses, and the number of adult females in the root tissues at 3000 ppm concentration (Naz et al., 2013a). Fumaria parviflora quantity levels of amendments applied were lower than were the levels of other plants used in the biocontrol, as in the case of the dry powder of Acoruscalamus rhizome (Devi et al., 2011), Datura stramonium (Pariha et al., 2012), in the suppression of Meloidogyne spp. Similar studies were conducted by other researchers,

Table 3: Effect of dry powder of Fumaria parviflora on nematicidal properties of Meloidogyne incognita on tomato and plant growth parameters under natural field conditions of Dargai (spring, 2010)a

Plant parts###Galls###GIb###Egg###Adult###Shoot###Root###Fresh###Dry shoot fresh root###Number of Number Fruits###Fruit###Rfc

and doses (g###plant-1###masses###females###length###length###shoot###weight (g) weight###branches of flowers plant-1###weight

plant-1)###g-1 of###-1

###g of root (cm)###(cm)###weight###plant-1###plant-1###(Kg

###root###(g)###plant-1)

Roots

0###86.00 b###4.92 a###83.25 ab###59.00 b###30.00 i###11.25 f###34.25 d###16.00 f###28.50 a###10.25 gh###34.75 h###21.00 h###2.90 e###2.0 a

10###61.25 de###2.75 cdef###43.50 fg###28.50 f###48.00 b###19.50 bc###47.75 b###23.50 cd###17.75 de###18.75 bcd###61.25 bc###39.75 d###3.57 bcd###0.80 bcd

20###53.75 fg###2.37 efg###43.50 fg###19.25 g###50.50 b###24.50 a###51.00 ab###27.75 ab###18.50 de###19.75 b###65.50 ab###46.00 bc###3.95 b###0.733 cd

30###39.25 h###1.87 fg###31.00 h###18.50 g###55.00 a###26.75 a###53.00 a###29.25 a###20.75 bc###22.50 a###69.50 a###55.25 a###4.75 a###0.53 e

Stem

0###89.25 ab###4.95 a###90.00 a###63.75 ab###29.50 i###10.25 f###27.00 e###14.75 f###29.25 a###10.00 h###30.00 i###21.75 h###2.87 e###2.1 a

10###63.25 de###3.12 bcde###52.25 de###44.00 cde###41.25 ef###14.75 e###42.25 c###20.25 de###16.50 ef###17.50 de###46.50 ef###34.00 f###3.30 cde###0.93 b

20###53.75 fg###2.62 def###49.75 ef###39.50 e###44.00 cd###17.25 cde###48.00 b###24.50 bc###18.75 cd###17.75 cde###50.50 e###39.00 de###3.70 bc###0.80 bcd

30###48.25 g###1.50 g###38.75 g###27.50 f###48.50 b###21.00 b###47.75 b###25.50 abc###19.25 bcd###19.25 bcd###56.75 d###46.00 bc###4.75 a###0.63 de

Leaves

0###87.00 b###4.92 a###81.75 b###66.25 a###29.50 i###10.50 f###27.00 e###14.75 f###29.00 a###12.00 g###31.25 hi###21.00 h###2.90 e###2.0 a

10###70.75 c###3.75 b###69.50 c###50.00 c###33.75 h###15.25 de###39.25 c###17.75 ef###15.50 f###14.25 f###40.25 g###29.00 g###2.97 e###0.93 b

20###71.25 c###3.62 bc###57.50 d###43.50 cde###36.25 gh###17.25 cde###47.75 b###24.25 bcd###17.25 def###16.50 e###42.00 g###36.50 ef###3.65 bcd###0.83 bc

30###64.75 cd###3.12 bcde###49.75 ef###37.50 e###41.75 de###19.75 bc###49.25 ab###24.00 bcd###18.50 de###19.25 bcd###44.25 fg###43.25 c###3.90 b###0.73 cd

Whole plant

0###96.50 a###4.95 a###85.50 ab###66.00 a###30.00 i###11.00 f###28.00 e###14.00 f###29.50 a###11.50 gh###30.50 hi###21.75 h###2.92 e###2.0 a

10###67.50 cd###3.00 bcde###57.50 d###48.75 cd###38.75 fg###17.25 cde###40.50 c###21.75 cde###17.25 def###16.25 e###48.50 ef###37.75 de###3.20 de###0.86 bc

20###56.50 ef###3.50 bcd###52.50 de###47.00 cd###42.00 cde###17.50 cd###48.75 ab###24.25 bcd###19.25 bcd###18.75 bcd###56.25 d###46.25 bc###3.70 bc###0.80 bcd

30###53.00 fg###2.25 efg###37.50 gh###43.00 de###44.50 c###21.50 b###51.50 ab###25.75 abc###21.00 b###19.50 bc###57.75 cd###48.75 b###4.00 b###0.73 cd

LSD values (P###3.63###0.44###3.49###3.47###1.35###1.31###2.13###2.1###1.07###0.99###2.2###1.56###0.24###0.17

Table 4: Effect of dry powder of Fumaria parviflora on nematicidal properties of Meloidogyne incognita on tomato and plant growth parameters under natural field conditions of Dargai (autumn, 2010)a

Plant parts###Galls###GIb###Egg###Adult###Shoot###Root###Fresh shoot Dry shoot fresh root###Number of Number Fruits###Fruit weight Rfc

and doses###plant-1###masses g-1 females length###length###weight (g) weight (g) weight###branches of flowers plant-1###(Kg plant-1)

(g plant-1)###of root###g-1 of root (cm)###(cm)###plant-1###plant-1

Roots

0###99.25 a###4.95 a###109.3 a###95.50 a###31.25 hi###14.75 cd###22.00 i###9.25 i###28.50 a###10.00 g###34.75 gh###22.25 i###2.62 gh###1.9 a

10###63.50 de###2.50 d###62.75 de###58.50 de###40.75 cde###15.25 cd###31.25 de###16.75 cd###18.00 cdef###15.00 bcde###48.00 cde###41.75 cd###3.47 cd###0.63 cd

20###50.75 f###2.07 de###58.75 ef###45.75 fg###46.00 ab###17.50 bc###36.75 c###19.00 bc###19.50 cde###17.50 ab###51.75 bcd###46.50 b###3.92 b###0.43 e

30###31.00 g###1.25 f###45.25 g###40.25 g###48.50 a###21.50 a###55.00 a###27.00 a###21.63 bc###20.00 a###65.00 a###57.25 a###4.82 a###0.13 f

Stem

0###100.3 a###4.92 a###109.5 a###94.00 a###27.50 i###14.75 cd###23.00

hi###10.50 hi###28.75 a###11.00 fg###33.75 gh###22.75 i###2.50 h###2.0 a

10###78.75 b###3.23 c###72.75 bc###62.75 cd###38.25 def###14.25 cd###28.00 efg###14.20 ef###15.25 fg###13.50 def###42.25 ef###32.25 gh###3.07 ef###0.86 b

20###63.75 cde###2.50 d###69.50 bcd###60.00 d###43.75 bc###16.00 cd###30.00 def###15.00 def###18.00 cdef###13.00 ef###45.25 def###37.50 ef###3.47 cd###0.76 bc

30###48.75 f###1.82 e###54.50 f###51.75 ef###47.00 ab###20.25 ab###37.50 bc###17.75 bc###18.63 cdef###16.00 bcd###54.50 bc###45.75 bc###4.47 a###0.5 de

Leaves

0###103.8 a###4.95 a###109.3 a###90.25 a###28.50 i###14.00 cd###23.50 hi###9.25 i###29.25 a###9.75 g###32.00 h###22.50 i###2.52 h###1.96 a

10###75.50 b###3.75 bc###73.75 b###74.00 b###36.75 efg###15.00 cd###25.50 ghi###11.63 gh###13.25 g###14.50 cde###39.75 efg###29.25 h###2.95 fg###0.86 b

20###71.50 bc###3.57 bc###72.25 bc###68.00 bc###41.75 cd###14.75 cd###26.50 fgh###12.88 fg###15.00 fg###12.75 ef###46.25 def###36.00 fg###3.20 def###0.76 bc

30###61.50 e###3.32 c###65.75 cde###66.25 bcd###44.00 bc###17.50 bc###27.00 fgh###13.75 efg###14.75 fg###15.75 bcd###51.00 bcd###41.75 cd###3.72 bc###0.63 cd

Whole plant

0###106.8 a###4.97 a###105.3 a###92.25 a###28.50 i###13.50 de###22.00 i###9.50 hi###24.00 b###11.00 fg###31.50 h###22.00 i###2.70 gh###1.96 a

10###71.00 bcd###3.97 b###75.00 b###64.50 cd###33.25 gh###10.25 e###29.50 defg###14.38 ef###15.75 efg###15.25 cde###42.25 ef###34.75 fg###2.97 fg###0.86 b

20###71.25 bcd###3.45 bc###70.00 bcd###60.25 cd###34.25 fgh###16.50 cd###32.25 d###15.25 de###16.75 defg###15.00 bcde###54.25 bc###40.50 de###3.37 cde###0.83 b

30###66.75 cde###2.20 de###61.00 ef###51.50 ef###38.25 def###21.25 a###41.25 b###19.50 b###20.25 bcd###17.00 bc###56.00 b###45.00 bc###4.00 b###0.73 bc

LSD values###3.93###0.28###3.89###3.92###2.11###1.84###2.1###1.14###2.11###1.26###3.31###2.11###0.18###0.15

who found that the combination of poultry refuse and Furadan 5G (@ 3 t per ha and at 2 kg per ha, respectively) effectively suppressed M. incognita on tomato plants under natural field conditions (Faruk et al., 2011). These comparisons showed the great potential of F. parviflora for the control of PPNs, even at low and targeted application dose. The researcher reported that one way of reducing the large amount of material needed for the broadcast application of amendments was to make targeted applications only in the immediate vicinity of the plants, so that the seedlings developed in a soil environment that was very rich in the amendment (Thoden et al., 2011).

In the present study, the plant growth parameters of tomato plants were promoted significantly in all those treatments, where F. parviflora amendments were applied at increasing doses both in the greenhouse and the field experiments. Even the low dose of 10 g per kg enhanced plant health, and increased the shoot and root lengths, the fresh shoot weight, the number of branches, and the number of flowers per plant in the spring and autumn experiments. The field study revealed that the number of fruits per plant increased with the amount of root powder (55.25 and 57.25) used at the highest application dose. An increase was also observed in other treatments that were amended with the stem, the whole plant, and the foliage powder. Likewise, the fruit weight of the tomato markedly increased with the root and stem amendments.

These results agree with the work reported by other researchers, in which the use of amendments with nematicidal properties was found to enhance plant growth in tomato plants (Tariq et al., 2007; D'Addabbo et al., 2009; Pakeerathan et al., 2009). The combination of these amendments at lower doses could be combined with the use of nematicides, as in the case of Furadan. However, because of the inactivation of nematicides by means of high amounts of organic matter (Oka et al., 2013) these combinations should be used with caution, and after the conducting of preliminary studies. Additionally, the application of amendments in combination with biological control agents has been proven to be effective, as in the case of neem leaves (Khan et al., 2011). Biological control agents could be integrated with other control measures in order to achieve long-lasting and favourable results (McSorley, 2011).

The beneficial effect from F. parviflora on plant growth and yield could also be attributed to improvement in the physical, chemical and microbiological properties of the soil, after incorporation of the soil organic amendment. It has been shown that an increase in organic amendments can improve soil properties, and the decomposing plant materials can provide nitrogen and other nutrients that are needed by crops (Powers and McSorley, 2000). Several studies have revealed that microbial activities and biomass is higher in fields with organic amendments than they are in fields with conventional fertilisers (Drinkwater et al., 1995). Organic amendments stimulate a broad range of organisms in the soil food web, many of which act as potential predators or parasites of PPN (Oka, 2010). It has been suggested that increased crop yields observed with amendments are due to the activities of free-living nematodes, especially bacterivores (McSorley, 2011).

The present study suggests that the reduction in nematode parasitism could be due to the decomposition of plant material (in the stem, root, leaf and whole plant powder) in the potting mixtures, and the subsequent release of such secondary metabolites as alkaloids, saponins, tannins, glycosides, steroids, flavonoids and phenols, as demonstrated by the phytochemical screening of the stem and root of F. parviflora (Naz et al., 2013a, b). The low density /parasitism of M. incognita on tomato roots could also be due to the poor invasion of the nematode larvae into the roots, as affected by the application of dry plant amendments.

In addition, the presence of other nematicidal compounds, namely nonacosane-10-ol and 23a- homostigmast-5-en-3AY-ol (Naz et al., 2013b), and cis- and trans-protopinium, reported from the roots of F. parviflora, and the higher alkaloid (0.09 0.04) and saponin (1.3 0.07) contents could have synergistically contributed to the best nematicidal performance of the roots (Naz et al., 2013a, b). Likewise, the higher phenolic contents of the stem (16.750.07) could be attributed to the better nematicidal effect of stem, as had been evident in our previous findings (Naz et al., 2013a). The leaf powder of the plant also displayed promising results in this respect. Reports of the leaves of F. parviflora containing kaemferol and quercetine glycosides are available (Tandon et al., 2011), and the nematicidal activity of these compounds from pomegranate leaves has been demonstrated against Ascaris lumbricoides (Rahmatullah et al., 2010).

These secondary metabolites are structurally highly diverse, and are produced in a vaied ecological environment (Hawa et al., 2012).

The efficacies of Fumaria powder were decreased when the plant doses were gradually reduced, which might be due to the differences in the concentration of toxic substances that were present in the plant material (Naz et al., 2013a). The exact mechanism of the action of these phytochemicals is not known, with toxicity to nematodes and hatching having been shown in a previous study (Naz et al., 2013a). Additionally, these secondary compounds in the plant parts acted as a coating around the tomato roots, hence subsequently preventing the attack of the juveniles of M. incognita by creating an unfavourable environment for the nematode activity, or by means of indirectly effecting the acquisition of resistance or tolerance by the plants against the nematode attack.

This was evident in our previous findings, in which the two compounds that were contained in the roots, for example the nonacosane-10-ol and the 23- homostigmast-5-en-3AY-ol, effectively suppressed M. incognita, and reduced the population density in tomato root tissues in greenhouse trials (Naz et al., 2013b).

Conclusion

The use of dry preparations of the plant material from F. parviflora could make the nematode control more eco- friendly and practicable in the field with attendant yield increases. The assumption is made that the local application to roots, prior to them being planted in the field, could protect the roots at the beginning of the crop cycle. The beneficial potential of these amendments could further be strengthened by their economic convenience, due to the lower cost involved than with the use of chemicals, and also their easy availability. However, more studies should be done in order to test the viability of the seeds after the drying period, or the collection of the plant before seed production, in order to prevent F. parviflora as a weed in the field.

Acknowledgements

This research, which forms part of the PhD study by Ishrat Naz, was supported by the Higher Education Commission (HEC) of Pakistan, under the indigenous scholarship programme.

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