Biofumigation: A Potential Aspect for Suppression of Plant-Parasitic Nematodes

Plant-parasitic nematode cause economic loss to crops throughout the world. Biofumigation is the environmental friendly control option for the suppression of plant-parasitic as well as other pathogenic soil microbes. Glucosinolates are the main active compound present in some plants which are responsible for biofumigation process. To increase the efficiency of biofumigation selection of varieties containing more glucosinolates is highly desirable. Plant growth stage, soil temperature, soil texture, moisture, soil depth and soil microbes play important role in efficient biofumigation.

INTRODUCTION Agricultural crops are attacking by d ifferent insects, fungi, bacteria, viruses and nematodes. Plant-parasitic nematodes are the most common enemy to agricultural production. The plant parasitic nematodes cause about $157 billion annual losses of economic crops world wide (Abad et al.,2008). Chemical nematicides are considered the most effective method in suppressing nematodes population. The chemical nematicides including fu migants such as Ethylene Dibro mide, 1, 2-Dibro mo-3-Chloro p ropane, Chlo ropicrin, Metam-sodiu m, Dazo met, Methyl Bro mide and Methyl Iodide whereas non-fumigants nematicides viz., Aldoxycarb, Carbofuran, Oxamyl, Fenamiphos, Cadusafos and Fosthiazate are the widespread applied methods . These synthetic soil fu migants are highly to xic to pests as well as many beneficial soil organisms (Schreiner et al., 2001).Many of these soil fu migants exhibit vertebrate toxicity, high cost, resistance phenomena and other damaging environ mental effects (Co x, 2006). Thus, all these negative impacts drive the scientists to find alternative methods of management that are sustainable, economically viable and non-polluting. For sustainable nematode management, it is important to have a holistic approach; taking into consideration cultural, b iological and chemical options as part of an integrated management approach. Biofu migation and modified/innovative biofumigation are a sustainable approach to manage soil-borne pathogens, nematodes, insects and weeds. Biofu migation is defined as a process that occurs when volatile co mpounds with pesticidal properties are released during decomposition of plant materials or animal products (Angus et al. 1994;Halberendt 1996;Kirkegaard and Sarwar, 1998;Piedra Buena et al., 2007). Nu merous studies in literature confirmed the ability of certain plants to suppress nematodes through the nematicidal activity of the secondary metabolites (Chitwood, 2002;Zasada & Ferris, 2004). Most research on biofumigation, however, has focused on using brassicaceous crops (Kirkegaard and Matthiessen, 2004). The suppressive effect of brassicaceous biofumigants on soil borne pathogens, weeds, and plant-parasitic nematodes has been demonstrated in nu merous laboratory, greenhouse, and field studies (Ploeg and Stapleton, 2001;Ploeg, 2008;Zasada et al., 2010). The mechanism responsible for the biocidal effect of decomposing Brassica crops is thought to be based on a chain of chemical reactions ultimately resulting in the format ion of biologically active products (Underhill, 1980). Cruciferous plants belonging to Brassica spp. contain glucosinolate compounds which are β-Dthioglucosides, sulphur containing stable and non-toxic compounds located in the cell vacuoles distinguished fro m one another by differences in their organic side chains (R groups) and classified as aliphatic, aromatic or indole forms, occur in all parts of the plant and degrade v ia enzy matic hydrolysis (Chew, 1988;Bro wn et al., 1991;Zasada and Ferris, 2004;Padilla et al., 2007). Glucosinolates, upon tissue disruption they come in contact with myrosinase (= thioglucosidase), an enzy me endogenously present in Brassica tissues, but stored in the cell walls or the cytoplasm, away fro m the glucosinolates (Poulton and Moller, 1993). The enzy matic hydrolysis of glucosinolates produces volatile isothiocyanates (ITCs), nitriles, SCN-, o xazo lid inethione, epthionitriles and organic thiocyanates (Cole, 1976;Fenwick et al.,1983;Wathelet et al., 2004). The fu migant action of these volatile co mpounds that are released, suppresses plant pathogens soil-borne pathogens Kirkegaard et al., 1993;Piedra Buena et al., 2007).
Although ITCs are considered the most bioactive products, other compounds such as non-glucosinolate sulphur containing compounds, fatty acids, nitriles and ionic thiocyanates may also affect pest and pathogen populations (Matthiessen & Kirkegaard, 2006) .The first observations of the unique properties of GSLs and ITCs were recorded at the beginning of the 17th century (Challenger, 1959). The Family Brassicaceae contains more than 350 genera with 3000 species of which many are known to contain GSL. However, GSLs are not confined to brassicas alone. At least 120 structurally different glucosinolates have been identified in 16 different families of angiosperms. At least 500 species of non-brassica dicotyledonous angiosperms have also been reported to contain one or mo re of the over 120 known GSLs (Fahey et al., 2001). Each of the GSLs has its own chemical property and can be placed in one of three different classes, namely aliphatic, aro mat ic or indole forms (Zasada &Ferris, 2004;Pad illa et al., 2007). There are over 100 different types of glucosinolates (Manici et al., 2000;Underhill, 1980). A single Brassica species can contain several different types of glucosinulates (Sang et al., 1984), and the types and quantities of glucosinolates are highly variable between species and even varieties (Rosa et al.,1997). As a result, the quantities and types of biocidal ITCs resulting fro m the breakdown of glucosinolates are higly variab le. The nemat icidal effect of the tested mustard may possibly be attributed to their h igh contents of certain oxygenated compounds which are characterized by their lipophilic properties that enable them to d issolve the cytoplasmic membrane of nematode cells and their functional groups interfering with the enzy me protein structure (Knoblock et al., 1989;Salem et al., 2015).

II.
BIOFUMIGATION PROCESS Incorporation the fresh mass of plant residues into the soil can be done directly if the mass is co ming fro m gro wn crop or plant mass taken fro m elsewhere and brought into the plot or field. If the mass is transported to the field, the soil should be well prepared before the incorporation. During transportation of these organic materials in the field, care must be taken to retain the gases produced fro m biodegradation, by covering the piles of the bio -fu migant with p lastic until the t ime of applicat ion. Generally a dose of 50 t to 100 t per ha is recommended depending on nematode population in the field. The bio-fu migant should be distributed uniformly and the field should be watered until the soil is saturated and cover the soil surface tightly with a transparent plastic film for at least 2 weeks. The film is removed 3-4 weeks after and the soil slightly removed in order to permit the gases to escape from soil. Planting of the desired crop can be done 24 hours later.

III. ASPECTS THAT INFLUENCE GSL RELEAS E AND ITC ACTIVITY 3.1. Plants containing GSL
Most GSL-containing genera, are within the Brassicaceae, Capparaceae and Caricaceae families (Rod man, 1981). The Family Brassicacea (brassicas) contains more than 350 genera with 3000 species, of which many are known to contain GSL. However, GSLs are not limited to brassicas alone. At least 500 species of non-brassica dicotyledonous angiosperms have also been reported to contain one or more of the over 120 known GSLs (Fahey et al., 2001). The GSL concentration in the cells of the various plants in the families differs substantially. Therefore, it is important to identify species that will be effective in suppressing soilborne pests and diseases, including nematodes. The plant species that generally are considered for bio fu migation are found mostly in the family Brassicaceae, and include Brassica oleracea (broccoli, cabbage, cauliflo wer, kale), Brassica rapa (turnip), Raphanus sativus (radish), Brassica napus (canola, rapeseed), cv. A V Jade, Eruca sativa (salad rocket, arugula), cv. Nemat, , B. juncea (Indian mustard) cv. Caliente 199, and various mustards, such as Sinapis alba . This may be explained by quick decomposition of the tested residue in soil on the basis that nematic idal activ ity by nitrogenous by products depends on the C: N ratio of the amendment (Stirling, 1991). One way to ensure the effective release of ITC is to slash the leaves with a slasher and then to plough the slashed residues into the soil as soon as possible, using a rotavator or d isc harrows. A flail chopper ensures the best macerat ion results and, consequently, a good GL-M YS interaction for the release of ITC. The latter technique remains applicable particularly for the Brassica spp. such as mustards, which have a high GSL concentration in the above-ground parts of the plant. The growth stage of the crop (emergence, rosette, flowering, seed filling, ripening), the amount of bio mass produced and the correct incorporation into the soil all contribute towards the success of biofumigation (Bellostas et al., 2004).The flowering stage of the plant maintains a higher GSL content than the vegetative plant parts. The GL-MYS interaction can be expected to take p lace mo re effectively later in the growing season, prior to seed set. In the root tissue, the concentration of GSL is higher in the earlier root growth stage, with decreasing concentrations during the root growth cycle. Different types of GSLs are present in the roots and shoots of different plant species (Van Dam et al., 2009). Studies that were conducted by Van Dam et al. (2009), in wh ich the root and shoot GSL of 29 plant species were evaluated for their GSL concentration and profiles, showed that the roots had a higher GSL concentration, as well as more d iversity than the shoots. The root and shoot concentration of specific GSLs was found to differ fro m one another, with the most prominent indole GSL in the shoots being 1H-indol-3-yl GSL, and with the roots having higher concentrations of aromatic 2phenylethyl GSL. The inclusion of sulphur fertilizers may imp rove the nutritional value of Brassica spp. Sulphur forms part of the process that takes place in the formation of secondary metabolites. The level of GSLs is dependent on the genetic factors of the plant, but can also vary according to environmental condit ions and the availability of soil sulphur (De Pascale et al., 2007).

Soil temperature
Lopez-Perez et al. (2005) used some plant residues of broccoli, melon, and tomato with addition of chicken manure in pot experiments with Meloidogyne incognita infested soils and was observed that biofumigation to control M. incognita is unlikely to be effective under cool conditions but that at soil temperatures around 25ºC, broccoli is more effect ive than melon and to mato, and that the addition of chicken manure at this soil temperature may enhance the efficacy.This corresponds with earlier results by Ploeg and Stapleton (2001) and with reco mmendations by Bello et al.(2004). Low soil temperature slows down the enzy matic reaction during biofu migation, and therefore incorporation of green manure is not recommended at soil temperatures close to 0°C. The presence of organic matter seems to have an immob ilizing effect on the degradation products, thus preventing them fro m reaching the target pests. Roubtsova et al. (2007) studied the direct localized and indirect volatile effects of amending soil with broccoli tissue on M. incognita infested soil. A mending a 10cm layer lowered M. incognita than in the non-amended layers of the tubes by 31 to 71%, probably due to a nematicidal effect of released volatiles of broccoli. These results suggest that the fumigant nemat icidal act ivity is limited and its effect requires a thorough and even distribution of the biofumigant material through the soil profile where the target nematodes occur. Furthermore, the concentration of ITCs produced is also influenced by soil texture, pH, and microbial co mmunity (Bending & Lincoln, 1999

IV. BIOFUMIGATION IN INTEGRATED PEST MANAGEMENT (IPM)
Biofu migation is a definite choice as part of an integrated approach for nematode management and can be implemented as a biological alternative or in co mbination with certain chemical options. This will reduce the demands on chemical nematicide use. The positive biolog ical activity of the GSL degradation products used for the suppression of some pathogenic fungi (Manici et al., 1997) and nematodes (Lazzeri et al., 1993) serves as an integral part of IPM (Lazzeri et al., 2004), because it has been proven to be effective against weeds, pathogenic fungi and nematodes (Van Dam et al., 2009). In addition to providing some disease control, growing and incorporating the biofu migant plant improves soil structure, assists in weed control, reduces soil erosion and provides organic matter to the organic producer for controlling diseases and pests (Griffiths et al., 2011).The potential for Brassicaceous amend ment as part of an IPM approach consists of the role of the active co mpounds, in the direct suppression of nematodes, and also the secondary effect in the soil. The secondary effect plays a very significant part in pro moting microbial and other microorganism diversity in the soil, and therefore can be expected to have a positive impact on the stimulat ion of competition among soil-borne diseases in the rhizosphere.

VI.
CONCLUSION Soil disinfestation is a major approach against soil borne micro -organisms. The practical value of using biofu migant crops to the farmers should be accessed through several factors which include extent of pesticide efficacy, effect on crop growth and yield as well as cost of production. The benefits of using biofu migant crops and agronomic practices in improving sustainable agricultural production require further exp lo itation of GSL and ITC to realize the goal of sustainable production with minimal environ mental impacts.