Introduction
High population densities of plant-parasitic nematodes cause economically significant production losses in most agricultural crops, including grapevines. In South Africa, plant-parasitic nematodes impact negatively on the production of good quality grapes.

Consideration of more environmentally friendly options for the control of soil-borne plant pests and diseases has increased the interest in biofumigation. This review investigates the potential of cover crops with biofumigation properties for the suppression and control of plant-parasitic nematodes in South African vineyards.

Principles of soil biofumigation
Biofumigation takes place when certain soil-borne pests and diseases are suppressed as a result of the biocidal activity of glucosinolate-containing plants, when they are incorporated into the soil after the biomass have been macerated/bruised. The fumigant action of the volatile compounds that are released during the biodegradation of organic matter suppresses plant pathogens.

Glucosinolates (GSLs) and isothiocyanate (ITC) are the main active compounds involved in biofumigation. GSLs are sulphur-containing secondary metabolites produced by certain crops that are hydrolysed by the enzyme myrosinase (MYR) to form ITCs, in a process that is known as the GL-MYR system. The ITCs have a toxic effect on many soil-borne pathogens. Breakdown products, including the active compound ITC, are released when the plant cell walls are damaged, or broken, during maceration of the plant biomass.

nielkrugerfiguur1A

FIGURE 1. Seedlings of Eruca sativa cv. Nemat (A), Sinapis alba cv. Braco (B), Brassica juncea cv. Caliente 199 (C) and Brassica napus cv. AV Jade (D).

FIGURE 2. Slashing of crops with slasher (A); Texture of slashed crops (B); Slashed green material on the soil (C); Rotavating the green material into the soil (D).
FIGURE 3. Root-knot nematode galls and egg masses on the roots of a host plant.

Principles of soil biofumigation
Biofumigation takes place when certain soil-borne pests and diseases are suppressed as a result of the biocidal activity of glucosinolate-containing plants, when they are incorporated into the soil after the biomass have been macerated/bruised. The fumigant action of the volatile compounds that are released during the biodegradation of organic matter suppresses plant pathogens.

Glucosinolates (GSLs) and isothiocyanate (ITC) are the main active compounds involved in biofumigation. GSLs are sulphur-containing secondary metabolites produced by certain crops that are hydrolysed by the enzyme myrosinase (MYR) to form ITCs, in a process that is known as the GL-MYR system. The ITCs have a toxic effect on many soil-borne pathogens. Breakdown products, including the active compound ITC, are released when the plant cell walls are damaged, or broken, during maceration of the plant biomass.

The role played by biofumigation in integrated pest management (IPM)
The positive biological activity of the GSL degradation products used for the suppression of some pathogenic fungi and nematodes serves to open up new perspectives on IPM, because it has been proven to be effective against weeds, plant diseases, and nematodes. Research has proved that many Brassica species show nematicidal activity on plant-parasitic nematode species.

Plants containing GSL
The family Brassicaceae (brassicas) contains more than 350 genera, with 3 000 species, of which many are known to contain GSL. Most GSL-containing genera, however, are clustered within the Brassicaceae, the Capparaceae, and the Caricaceae families. Some rotation crops tested for the presence of GSLs are listed in Table 1.

The main cultivars with good biofumigation potential, and currently commercially available in South Africa are Nemat (Eruca sativa cv. Nemat), white mustard (Sinapis alba cv. Braco) and Caliente 199/Indian mustard (Brassica juncea cv. Caliente 199). Various Canola cultivars (Brassica napus), for example (Brassica napus cv. AV Jade), are also available in South Africa, but Canola are seen as a crop with a low biofumigation potential (Fig. 1).

Nemat
As Nemat reduces the size of plant-parasitic nematode populations, it can be included in a crop rotation programme. Nemat is unique in its mode of action of suppressing certain nematodes by functioning as a trap crop that also has the ability to form ITC when it is applied as a green manure.

White mustard
White mustard shows potential as a cover crop in vineyards, and as a rotation crop in rotation programmes that include annual crops. Nematodes are suppressed by this crop when the active compound is released during the incorporation process 60 – 75 days after planting. It also has an effect on the life cycle of certain nematodes by slowing down, or by preventing, the completion of their life cycle in the roots.

Caliente 199/Indian mustard
Caliente 199 is an annual, cool season crop that requires a short growing season. To maximise biomass production, adequate soil moisture and sufficient nutrient levels should be maintained throughout the growing season. Caliente 199 can be included very successfully in a rotation programme as it suppresses soil-borne diseases, weeds and nematodes very effectively when applied correctly. Caliente 199 is seen as a very effective biofumigation crop and is compatible in planting programmes together with Nemat.

Canola
Canola is primarily planted in a crop rotation system that includes wheat (Triticum aestivum) in the winter rainfall areas of South Africa. Root-knot nematode reproduction on 14 Canola cultivars has been investigated in previous research, and all cultivars were found to be poor hosts that maintained low root-knot nematode numbers.

Aspects that influence GSL release and ITC activity
Techniques that ensure the maximum rupturing/maceration of the cells involved, as well as effective incorporation, ensure the best release of ITC. This aspect, together with a cover crop variety with high GSL content and enough water present for hydrolysis to take place, ensures optimum biofumigation. To ensure the effective release of ITC, the leaves should be slashed with a slasher, and immediately thereafter incorporated into the soil, using a rotavator or disc harrow (Fig. 2).

The growth stage of the crop, the amount of biomass produced, and the correct incorporation into the soil all contribute towards the success of biofumigation. Different types of GSLs are present in the roots and shoots of different plant species. The flowering stage of the plant has a higher GSL, with the biofumigation effect being expected to be more effective later on in the growing season, prior to seed set.

Control of plant-parasitic nematodes in vineyards
The three most important plant-parasitic nematode genera in South African vineyards, measured in terms of their presence and amount of potential damage, are root-knot nematode (Meloidogyne species), ring nematode (Criconemoides xenoplax) and dagger nematode (Xiphinema species).

Root-knot nematodes (Heteroderidae) have a wide host range, are widely distributed in agricultural soils, and can cause extensive loss of yield and quality in numerous crops. Damage symptoms on root-knot nematode-infested vines include stunted growth, poor vigour, and substandard yields.

Ring nematodes (ectoparasites) are often found on such woody perennials as vines. They feed on the epidermal cells of the feeder roots, where they cause root stunting and collapsed roots, thereby influencing the uptake of nutrients and water through the root system. Criconemoides xenoplax is the only species of ring nematode found in the vineyards of South Africa.

Dagger nematodes (Longidoridae) are ectoparasites that feed on the root tips of mostly woody perennials. Their feeding behaviour slows down the root development of susceptible cultivars. For vines, Xiphinema index is the most economically important dagger nematode in South Africa, as they not only damage the roots of susceptible vine cultivars, but are also able to transmit grapevine viruses.

Plant-parasitic nematodes can be present in the soil of the vine inter-row, or in the vine row, although most species are present in the vine row soil, where they can infect the young, active feeder roots. Nematodes are primarily controlled chemically in South African vineyards using fenamiphos, cadusafos and furfuraldehyde that are registered on grapevines, and/or by planting nematode-resistant rootstocks (Table 2).

ITC suppressed fungi, bacteria, nematodes, and weeds in numerous in vitro experiments. The question arises as to whether biofumigation crops growing in the grapevine inter-row can have an effect on the nematode population in the vine row area, after being incorporated mechanically into the soil. Research has indicated that Brassica juncea cv. Nemfix (Indian mustard), incorporated into the inter-row, or into the vine row, as a green manure, suppressed Meloidogyne javanica.

Research also showed that Brassica species planted in the grapevine inter-row reduced the root-knot nematode population over a period of three years. Biofumigation with the cover crops was observed to be as effective as were mustard seed meal and fenamiphos applications over a three-year period.

Nematode biofumigation bioassays

Green manure
The brassica green manures suppressed root-knot nematodes significantly under controlled environments. It was perceived that the suppression was not caused by the GSL content of the brassica green manures alone, but also by other secondary metabolites that are released during the biofumigation process. Another possibility regarding the suppressing effect of biofumigation on plant-parasitic nematodes lies in the stimulation of competition for food sources, which can occur after incorporating green manure into the soil. The main focus, however, is on the role that volatiles and non-volatiles play during the decomposition of plant residues in the soil.

In a pot trial with vines, conducted by Rahman et al., 2011, the suppression of root-knot nematodes by fenamiphos, two Brassica species applied as green manure, and Indian mustard seed meal was evaluated. No statistical differences were observed over a period of three years.

Nematode host status of different biofumigation crops
The ideal cover crop to be applied in vineyards for nematode suppression should either be resistant, or it should have a poor host status, in addition to having a biofumigation suppressing effect on the target nematode, when applied as a green manure to the soil. The possibility exist that Brassica species, when used as cover crops in vineyards, might also be susceptible to a nematode species that requires suppressing. If the target pest manages to reproduce effectively on the cover crop before it is incorporated into the soil as a green manure, these Brassica species should not be used as cover crop.

Although root-knot nematodes (Fig. 3) can complete their life cycle on several Brassica species, there are major differences in their susceptibility. In glasshouse studies, certain brassicas were rated as poor, or as non-hosts (resistant), as maintenance hosts (tolerant), or as good hosts (susceptible). Nemat was evaluated for its potential as a trap crop for root-knot nematode. No eggs were produced in 80% of the plants, indicating it to have the potential to act as trap crop for Meloidogyne hapla.

Conclusion
Biofumigation is a concept that has been studied for a long time, with definite potential and good results being shown, where the method has been applied correctly, for the management of nematodes, soil-borne diseases, and weeds. The challenge is to understand the complex interactions during biofumigation, and to ensure that the different factors that play a role in optimal biofumigation are applied. The main factors concerned include the basic principles of fumigation, Brassica species selection and biomass production, glucosinolate concentration and spectrum, isothiocyanate concentration and spectrum, and the maceration and incorporation process.

The potential for biofumigation as part of an IPM approach consists primarily of the role played by isothiocyanates in suppressing soil-borne diseases, nematodes, and weeds. However, the incorporation of the plant fibre into the soil has a secondary effect, which plays a very important role in promoting microbial and other micro-organism diversity in the soil. Such incorporation can, therefore, be expected to have a positive impact on the stimulation of competition among soil micro-organisms in the rhizosphere. The susceptibility, or the resistance, of brassica crops, which are considered for biofumigation, to nematodes could also impact on the suppression of nematodes.

Applied correctly, and with proper medium to longterm planning, biofumigation could play a substantial role, as part of a cover crop rotation programme in vineyards.

Acknowledgements
The authors would like to thank Winetech, Dried Fruit Technical Services, and the National Research Foundation of South Africa (NRF-THRIP TP2011060100026) for their funding of the project.

References
Kruger, D.H.M., 2013. The role of cover crops with biofumigation potential for the suppression of plant-parasitic nematodes in vineyards. Department of Conservation Ecology and Entomology, Stellenbosch University, Stellenbosch, 97 pp.
Kruger, D.H.M., Fourie, J.C. & Malan, A.P., 2013. Cover crops with biofumigation properties for the suppression of plant-parasitic nematodes: A Review. South African Journal of Enology and Viticulture 34(2): 287 – 295.

Summary
Plant-parasitic nematodes are a problem in vineyards worldwide, with some species acting as vectors of grapevine soil-transmitted viruses. Global pressure on the use of soil-applied nematicides has led to a search for new control options, or for alternative methods for the suppression of plant-parasitic nematodes, as part of an integrated pest management system. This paper summarises previous research on the use of cover crops with biofumigation properties for the suppression of plant-parasitic nematodes in vineyards.

* This article is adapted from a review manuscript entitled: Kruger, D.H.M., Fourie, J.C. & Malan, A.P., 2013. Cover crops with biofumigation properties for the suppression of plant-parasitic nematodes: A Review. South African Journal of Enology and Viticulture 34(2): 287 – 295.

Niel Kruger1, Johan Fourie2 & Antoinette Malan1
1 Department of Conservation Ecology & Entomology, Stellenbosch University
2 ARC Infruitec-Nietvoorbij, Stellenbosch

For more information contact Niel Kruger at niel@terason.co.za.

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