Pratylenchus penetrans (northern root lesion nematode)

The principal symptom of P. penetrans activity is the presence of distinctive lesions on host plant feeder roots. Other species of the genus may also cause lesions, but the discolouration may be less intense. The lesions, sometimes described as resembling 'cat scratches', usually appear as discoloured yellowish to brownish elongate marks parallel to the long axis of the root. They are formed as the nematode tunnels along a series of cortical cells, moving through the end-walls from cell to cell and feeding on the contents. Roots damaged from severe lesioning are generally discoloured, frequently yellow-brown or 'rusty'. Root systems affected by the nematode may show either 'witches-broom' clusters of proliferated feeder roots, or feeder roots may be sparse in comparison with normal root systems as a result of root-terminal meristem killing. Damage on tap roots may result in forking and stunting. The nematode may also cause necrotic lesions on tubers (Olthof and Wolynetz, 1991; Holgado et al., 2009; Figueiredo et al., 2021a). These lesions can vary in size and can create entry points for other pathogens. Tubers may exhibit surface damage, including scabbing or corky areas. The nematode feeding activities can thus compromise the quality of potato tubers. This may include a reduction in size, weight and overall marketability of potatoes. Nevertheless, according to Olthof and Wolynetz (1991), P. penetrans can be found in potato peel but do not seem to proliferate in the inner core of tubers.

Aboveground plant organs do not show symptoms specific to this nematode. Commonly, leaves will appear chlorotic, pale green to yellowish; plants will be stunted and weak, with a tendency to wilt in drought situations; flowers may be reduced substantially both in number and quality and fruit may be undersized. Damage can significantly impair the development of flower bulbs, young plants, or rootstocks in infected soil. Over the years, diseased trees may decline gradually as nematode populations increase to high levels (Nyczepir and Becker, 1998). Field and vegetable crops may exhibit patches of plants with poor growth and reduced yields. Symptoms such as twig dieback can be caused by P. penetrans but may also be caused by other pathogens. Likewise, secondary root rots can result from the invasion of bacteria or fungi into entry wounds left by the nematode. Premature senescence of plants can also result from P. penetrans attack but is not specific.

Introduction

Control of P. penetrans is implemented most often with crops of high value per unit area, or for crops where failure to reduce the nematode population would result in unacceptably high yield losses. Crops like tobacco or ginseng have sufficient commercial value to allow for the expense of soil fumigation, whereas few field grains or forages generate such financial returns to the growers. Sustainable alternatives to chemical control are still vitally needed.

Integrated pest management (IPM) programmes

The extremely large host range of P. penetrans poses a challenge to the development and use of IPM programmes for this nematode species, because control by rotation is considerably more difficult. Research on wild plant species and plant resistance screening, nematode population studies, soils and soil micro-organisms, and effects of climatic conditions shows some promise toward producing information useful for IPM programme development. However, since several ecological variables can affect the nematode's life cycle, distinctions between cultural, biological and chemical control methods may become hazy. Integrating such cultural practices as winter fallowing in cool climates (Olthof, 1971) or herbicide treatments to suppress weed hosts in orchards (Marks et al., 1972b) with other farming operations would be beneficial in an IPM approach to managing root-lesion nematodes.

The result of adding an amendment to soil, or of growing a cover crop, or green-manuring the cover crop, may be seen in soil fertility responses, in direct suppression of nematodes by exuded products from the growing cover plants, or in noxious compounds released into the soil matrix. Stirling (1991) is especially eloquent on the topic of organic amendments for nematode control.

In Sweden, the application of milled peat or green manuring of apple nurseries reduced populations of P. penetrans and eliminated replant disease (Kauri-Paasuke, 1973a); it was noted that nematode-preying tardigrades were stimulated by the milled peat, and nematophagous fungi by the green manure. Kauri-Paasuke (1973b) considered that even good hosts, used as green manure and ploughed under at the appropriate time, could be used to reduce nematode density; weeds and couchgrass (Elymus repens) used in this way were effective (Kauri-Paasuke, 1973a). Halbrendt et al. (1996) shown that the green manuring of Brassica and Sinapis species effectively reduced P. penetrans populations comparably to the use of commercial nematicides. An important aspect of this process is the choice of plant species and cultivar. Halbrendt et al. (1996) had the most success with rape (Brassica napus) cv. Humus and wild mustard (Sinapis arvensis).

Miller (1977) achieved an 85% reduction of P. penetrans populations with leaf mould plus sewage sludge; mycelial residues, alone or with leaf mould, and leaf mould plus ammonium sulphate were also effective. Malek and Gartner (1975) inhibited population development of P. penetrans with 2:1 mixtures of hardwood bark: soil for greenhouse container use. Saka (1978) used similar materials to Miller (1977). Valdez (1979) discuss nematode control, including P. penetrans, using chicken manure.Rössner and Zebitz (1987) were successful in reducing P. penetrans by 8x in greenhouse and field soil using ground neem seed kernels and leaves. Schauer-Blume (1988) reduced P. penetrans in winter wheat roots to 7 and 20% of the control, using neem oilcake (crushed, de-oiled seeds) and a neem kernel extract (AZT-residue), respectively. Neem cake was also shown to reduce P. penetrans numbers by 67-90% in tomato roots grown under glasshouse conditions (Abbasi et al., 2005).

In Canada, the long-term soil incorporation of dairy manure slurry increased P. penetrans population densities in tall fescue (Festuca arundinacea) cv. Festorina relative to the non-treated control (Forge et al., 2005). However, the co-application of shredded paper with broiler manure, decreased the nematode population densities and increased the root biomass of raspberry (Forge and Kempler, 2009). Also, the application of poultry manure and compost treatments into soil, at pre-planting, decreased the P. penetrans populations nearly as well as fumigation over two growing seasons of raspberry (Forge et al., 2016). Significantly higher potato yields and fewer P. penetrans were obtained by Cole et al. (2020) in field plots treated with poultry manure, compared to the control. The authors suggested that using poultry manure as soil amendment can aid in the control of potato early die complex.

Growing marigolds (Tagetes erecta, T. minuta, T. patula and T. tenuifolia) has been shown to reduce Pratylenchus numbers by 90% (Oostenbrink, 1957). The chemistry of this suppressive effect has been studied by several researchers such as Uhlenbroek and Bijloo (1958), Gommers (1973), Gommers and Bakker (1988), Kyo et al. (1990), Chitwood (1992) and Riga et al. (2005). Experimental attempts have been made to use marigolds to manage P. penetrans in Japanese radish (Raphanus sp.) (Ohbayashi and Chikaoka, 1973; Nakajima et al., 1985), artichoke (Caubel et al., 1978), lettuce (Shibamoto et al., 1980), potato (Sieczka et al., 1991; Kimpinski et al., 2000), apple and field crops (Edwards et al., 1994; Kimpinski and Arsenault, 1994), flue-cured tobacco (Reynolds et al., 2000), potato and tomato (Alexander and Waldenmaier, 2002; Ball-coelho et al., 2003), strawberry (Evenhuis et al., 2004) and carrot fields (Kimpinski and Sanderson, 2004; Pudasaini et al., 2006). Other ornamental compositae such as Helenium, Gaillardia and Eriophyllum also suppress P. penetrans (Hijink and Suatmadji, 1967). Gommers (1973) also found these genera suppressive, as well as Melampodium, Silphium, Iva, Ambrosia, Parthenium, Milleria, Schkuhria and Echinops. Suppressive cover crops in apple orchards may become a component of a nematode control programme with minimal pesticide use (Merwin and Stiles, 1989).

Apart from marigolds and related compositae, various grasses, legumes and crucifers have been studied for field suppression of P. penetrans. Marks et al. (1973) found a reduced rate of nematode increase with a permanent red fescue (Festuca rubra) cover crop in peach orchards. Festuca arundinacea cvs. Kentucky 31 and Oregon B, redtop (Agrostis alba [Poa nemoralis]) cv. Z9036 and perennial ryegrass (Lolium perenne) cv. Norlea kept P. penetrans populations at low levels in peach, plum and apple orchards (Townshend and Marks, 1976; Townshend et al., 1984). Edwards et al. (1994) had similar results with red fescue and redtop; however, they found that Brassica campestris [Brassica rapa] increased the root-lesion nematode population. In contrast, Winkler and Otto (1979) found that rape, mustard, stubble and beets impeded the spread of P. penetrans, and populations were reduced by ploughing-in green manures of rape, mustard and legumes (peas, beans and vetches). Black oat (Avena strigosa) cv. Saia, red fescue and redtop, were shown to suppress the nematode populations when in red raspberry plantings (Vrain et al., 1996). Efficient suppression of P. penetrans was also obtained by LaMondia (1999; 2006) in infested soil, when black oat cv. Saia was grown as cover crop. Other plants with suppressive activity to P. penetrans include Megathyrsus maximus [Panicum maximum], Gaillardia aristata, Macroptilium atropurpureum and Rudbeckia sp. (Ohno and Hirota, 1993), Asclepias tuberosa, Gaillardia sp., Panicum virgatum and Rudbeckia hirta (McKeown et al., 1994; Potter and McKeown, 2002), Senna tora (Ito et al., 1994) and Taxus baccata (Bertrums, 1998).

The use of crop rotation is seen as a limited option to manage Pratylenchus spp., however, certain rotation schemes have been shown to reduce P. penetrans populations successfully. In potato crops, two-year rotations with lucerne or clover resulted in a decrease in P. penetrans populations, compared with 3 years of continuous potato cultivation (Chen et al., 1995). In strawberry, P. penetrans soil populations were reduced by rotation with cv. Saia black oats (LaMondia, 1999). Forage and grain pearl millet (Pennisetum glaucum [Cenchrus americanus]), in rotation with potato cv. Superior, were shown to decrease P. penetrans populations and increase tuber yields in the subsequent potato crop (Bélair et al., 2005; 2006). Rotation of potato with black oat and R. hirta reduced P. penetrans and increased tuber yields (LaMondia, 2006). Chen and Tsay (2006) observed less necrosis on strawberry roots after rotation of strawberry with rice and taro. Although the nematode populations were also suppressed following rotation with tomato, strawberry yields were reduced in 5.9% when compared to the average strawberry yield, following the bare fallow treatment.

In a few specific circumstances, methods of excluding P. penetrans have been beneficial in controlling the nematode. For example, Townshend's (1965) method of producing strawberry transplants by rooting the runners in sterilized soil has facilitated the propagation of large numbers of nematode-free seedlings. Similarly, the production of transplants by tissue-culture of shoot-tip cuttings also permits large-scale plant propagation (Sullivan, 1991). Hot-water treatment of dormant raspberry roots for 15 min at 47°C has been used to successfully eliminate the nematode (Bridge, 1975).

There has been some success in controlling P. penetrans by soil solarization (under transparent polyethylene sheets) in Australia and Canada (Porter and Merriman, 1983; 1985; Lazarovits et al., 1991). Both groups have found nematode numbers substantially reduced or eliminated to a depth of 10 cm in field soil, Lazarovits et al. (1991) achieving population reductions of 50% at temperatures elevated by 7-10°C, whereas Porter and Merriman (1983; 1985) found all pathogens were killed at soil temperatures exceeding 45°C. Porter and Merriman (1985) reported a reduction of inoculum levels but not disease of celery affected by P. penetrans in artificially infested soil, yet achieved disease reduction as well as nematode population reduction in naturally infested soil. MacGuidwin et al. (2012) reported that soil solarization decreased the levels of P. penetrans and Verticillium dahliae in commercial potato fields and tuber yields increased by 11% in year two following the solarization.

Fertilization has direct as well as indirect effects on P. penetrans and plant growth. Numbers of lesion nematodes in roots of Douglas fir (Pseudotsuga menziesii) were reduced when seeds were grown in nematode-infested soil fertilized with urea and phosphate (Sinclair, 1975) . However, Mai (1972) reported that burning fruit-tree brush did not kill P. penetrans, but Montmorency cherry trees on Mahaleb rootstock grew better (46% greater growth) on the burned sites where K, Mg, Ca and P were enhanced by the burning; growth was similarly improved where fertilizer was applied to match these elements, on unburned soil. Lower P. penetrans Pf/Pi ratios in cherry rootstocks were recorded when commercial fertilizer was applied twice weekly, rather than being applied once at planting, suggesting that the addition of fertilizer may have either increased nematode mortality in the soil or improved rootstock resistance to nematode infection (Melakeberhan et al., 1997). Later, Melakeberhan (2006) mentioned that fertilizer application in soyabean cultivars had no direct or indirect adverse effect on P. penetrans but whether the nematode was switching on/off the physiological mechanisms responsible for host mediated responses to suppress nematodes remains unknown. The effect of fertilizers may also be related to the activity of biological control agents. Following amendment of soil with nitrogenous materials, a nematicidal mechanism has been proposed involving actinomycetes and evolved toxins (Saka, 1978) (see Biological control).

Experimental flooding of bulb soils for 6 weeks has reduced numbers of P. penetrans present in pots (Zaayen, 1986).

Studies of various hosts of P. penetrans have identified resistance among several major crops, such as potato, lucerne, tree fruit and some of lesser importance such as mint, tomato, raspberry, strawberry, navy bean (Phaseolus vulgaris), Japanese radish (Raphanus sp.), roses, oats and peas.

Commercial potato cultivars show differences in tolerance and resistance to P. penetrans (Brodie et al., 1993), but breeding for P. penetrans resistance in potatoes has been challenging due to the absence of complete resistant germplasm suitable for integration into commercial cultivars (Brodie, 1998). Early indications of resistance of the potato cvs. Hudson, Katahdin and Peconic to a root-lesion nematode isolate from lucerne callus (Dunn, 1973b) were not repeatable in field experiments (Kotcon et al., 1987). In many studies, the cultivar Superior has consistently been found to have low tolerance to damage by the root-lesion nematode (Bernard and Laughlin, 1976; Kotcon and Loria, 1984; Olthof, 1986; Kimpinski and McRae, 1988), compared with intermediate cultivars such as Chippewa, Katahdin, Kennebec, Monona and Norchip. Russet Burbank appeared to be tolerant toward P. penetrans (Bernard and Laughlin, 1976), although Kimpinski and McRae (1988) noted that cv. Russet Burbank seemed less tolerant at lower nematode population densities, approaching the low tolerance level of cv. Superior. Olthof (1986) found cv. Superior least tolerant and cv. Yukon Gold most tolerant of six cultivars tested. MacGuidwin and Rouse (1990) suggested that the reaction of the cv. Russet Burbank to the combination of P. penetrans and V. dahliae might be conditioned by the moderate wilt resistance of that cultivar compared with the highly susceptible Superior. Davis et al. (1992) have reported that cv. Butte was highly resistant to P. penetrans in greenhouse and field studies, although lacking resistance to Verticillium wilt. Brodie and Plaisted (1993) identified an improved genetic source of resistance to P. penetrans derived from Solanum tuberosum subsp. andigena or S. vernei, although acknowledging that the possibility of biological races within P. penetrans could add to the problem of developing resistant potato cultivars. France and Brodie (1995) have provided evidence of biological races, having identified four distinct intraspecific variants of P. penetrans based on percentage egression of isolates from the P. penetrans-resistant potato clone L118-2, and on reproduction on three potato cultivars and two breeding lines. Nonetheless, more information on the resistance of potato cultivars that are currently commercially available to root-lesion nematodes is needed (Orlando et al., 2020). The host susceptibility of ten potato cultivars often selected for potato cultivation in Europe was investigated by Figueiredo et al. (2021b) in pot assays, through the assessment of P. penetrans penetration, egression and reproduction. Although nematode multiplication was not prevented in any of the cultivars, differences in susceptibility to the nematode among cultivars were obtained, with lower number of nematodes being recovered from roots of cv. Laura, in comparison to the other less tolerant cultivars. Nevertheless, the molecular mechanisms behind the compatible and less compatible interactions of P. penetrans and potato plants are still poorly understood and need to be further analysed.

Resistance to P. penetrans in lucerne was found by Townshend and Baenziger (1976), although only five clones out of 23 were considered resistant. Pierce (1984) described a method for screening lucerne plants for root-lesion nematode resistance, based on using high nematode densities to stress the plants. Christie and Townshend (1992) confirmed that a process of selection and selfing from the cv. Vernal could improve resistance to root-lesion nematodes. Meanwhile, Thies et al. (1988) and Barnes et al. (1990) identified two germplasms, MNGRN-2 and MNGRN-4, with resistance to P. penetrans in the USA, and determined the inheritance of resistance to the root-lesion nematode in lucerne (Thies et al., 1995a). Several gene-candidates associated with lucerne resistance to P. penetrans and nematode parasitism genes encoding effector proteins were identified for potential use in lucerne breeding programmes (Vieira et al., 2019).

Limited data are available on resistance to P. penetrans in tree fruit rootstocks; the studies primarily pertain to peach and apple. Costante et al. (1987) found some indication that growth of cv. McIntosh apple on MM.111 and MM.106 roots was superior to that on M.26 and M.7a, although soil numbers of P. penetrans were low. Previously, Costante et al. (1985) had determined that MM.111 feeder roots had fewer P. penetrans than MM.106, and fewer nematodes in clay soil than in loam. In an earlier study, Parker and Mai (1974) detected that East Malling M.1 rootstocks showed greatest response to soil fumigation, with lesser responses by M.2, M.7 and M.12, presumably as a result of nematode control. Relative tolerance to apple replant disease caused by P. penetrans was reported in seedling accessions of Malus domestica (Isutsa and Merwin, 2000).

In breeding studies with peach for cool climates, Layne (1974) identified the cv. Yeh Hsiemtung Tao, US clone H661203 [(Nemaguard X Okinawa) open pollinated], and Russian clones Y322, Y327 and Y461 as tolerant of P. penetrans, although Stokes (1973) found that the nematode multiplied on both Nemaguard and Okinawa, as well as Lovell. In pot trials, Allen and Marks (1977) showed that cv. Rutgers Redleaf was resistant to P. penetrans, while cvs. Bailey and Siberian were susceptible. Field and greenhouse studies confirmed that Siberian C was more susceptible to P. penetrans than cvs. Veteran, Harrow Blood or Rutgers Redleaf, which showed no difference in sensitivity (Johnson et al., 1978). Subsequently, Potter et al. (1984) established that the response of 21 rootstocks to P. penetrans was a heritable character, and that Tzim Pee Tao, Rutgers Redleaf and two progenies of a cross of these two rootstocks exhibited the least response to lesion nematode infection. In later field studies with peach, Olthof et al. (1989) determined that rootstock cultivar Siberian C supported more P. penetrans than either Bailey or Harrow Blood, although mortality of Siberian C was lowest and Harrow Blood highest. Furthermore, the peach rootstocks Bailey, BY520-8, Higama and Guardian were less susceptible to P. penetrans whereas Chui Lum Tao was more tolerant than other tested rootstocks (McFadden-Smith et al., 1998).

Investigations of nematode problems on mint in Japan indicated that spearmint (Mentha spicata) appeared to be more resistant to P. penetrans than Japanese (Oba) mint (M. arvensis) in field trials (Inagaki et al., 1972). Studying three cultivars of peppermint (M. x piperita, M. spicata cv. Native and M. cardiaca (M. x gracilis) cv. Scotch) in Indiana, USA, Bergeson and Green (1979) detected a difference in reaction to nematodes between cvs. Black Mitcham (Verticillium-susceptible) and Todd's Mitcham and Murray Mitcham (both Verticillium-resistant); they suggested that nematode injury may have been attributed to, or masked by, Verticillium symptoms. However, Pinkerton (1984) determined that Murray Mitcham is most susceptible to P. penetrans, Todd's Mitcham is intermediate, and Black Mitcham is most tolerant.

In tomato, P. penetrans penetrated only the cortex of roots of Nemared and Hawaii 7153, whereas they penetrated into the stele of B-5 (Hung and Rohde, 1973); the latter cultivar contained a low concentration of chlorogenic acid in the endodermis, while Nemared contained the highest concentration suggesting that chlorogenic acid is important in the resistance mechanism.

There was evidence of partial nematode resistance in red raspberry seedlings of Rubus idaeus strigosus [R. strigosus] and R. crataegifolius (Vrain and Daubeney, 1986). The inheritance of this resistance was later characterized (Vrain et al., 1994); susceptible cultivars include Skeena, Chiliwack and Chilcotin, whereas Willamette, Nootka and R. strigosus 'Dalhousie Lake' were resistant.

Evidence of resistance and tolerance to root-lesion nematode has been found in cultivated strawberry (Fragaria x ananassa) cultivars, as well as in some genotypes of beach (F. chiloensis) and woodland (F. virginiana) strawberry (Potter and Dale, 1994). The presence of P. penetrans also seems to predispose strawberry to Verticillium wilt, and to black root rot (McKinley and Talboys, 1979; Wing et al., 1995). Several genotypes of wild Fragaria and commercial strawberry cultivars F. × ananassa were shown to own resistance to P. penetrans, when compared with the reproduction of a susceptible commercial cv. F. × ananassa (Pinkerton and Finn, 2005). Nonetheless, results suggested that commercial F. × ananassa cultivars may provide better sources for resistance to either Meloidogyne hapla and P. penetrans, than the wild Fragaria germplasm.

Some navy bean (Phaseolus vulgaris) cultivars (Gratiot, Saginaw, Kentwood) also appear to have tolerance (Elliott and Bird, 1985), based on better growth and yield and a lower nematode reproductive rate on these cultivars than on the susceptible cvs. Sanilac, Seafarer and Tuscola. Of the nine Japanese radish cultivars tested, Shogoin was most resistant, and Kameido and Miyashige most susceptible, to the nematode (Chikaoka, 1976). Varying degrees of resistance have been found in rose (Ohkawa and Saigusa, 1981), with Rosa indica cv. Major being the most resistant to P. penetrans of the eight cultivars tested. Partial resistance to the nematode was also detected in R. virginiana and R. multiflora rootstocks, while the greatest numbers of nematodes were found in the accessions of R. canina cvs. Pollmeriana and Superba (Peng and Moens, 2002b). Tolerance to P. penetrans varied in oat cultivars (Townshend, 1989); the cv. Saia was a poor host compared with the cv. OAC Woodstock.

With peas, perhaps the most significant effect of P. penetrans on the crop was that in the presence of the nematode, resistance of the cv. Alaska Express to Fusarium oxysporum f.sp. pisi race 1 was partially broken, although the damage was less intense than in the Fusarium-susceptible cv. Szlachetna Perla (Szerszen, 1980).

Attempts to control P. penetrans with specific biological agents have concentrated mainly on various fungi, but include a few studies with actinomycetes, bacteria and predatory soil animals. Stirling (1991) suggests that of all the groups of plant parasitic nematodes, the migratory endoparasites are likely to be one of the most difficult to control with natural enemies. Nematodes such as Pratylenchus and Radopholus spend much of their lives in roots and tend to be found in soil only when their host plants are stressed, senescing or diseased, or when their hosts have been ploughed out after harvest. It is difficult to envisage biological control agents being of more than limited value against them.

One early success using nematode-trapping fungi was that of Rama Rao (1973), who found that Arthrobotrys arthrobotryoides, A. dactyloides, Dactylaria thaumasia and Dactylella doedycoides greatly reduced penetration of lucerne roots by P. penetrans; A. dactyloides was the most effective species. Wimble and Young (1984) described in detail the fine structure of invasion of P. penetrans by Dactylella lysipaga, noting similarities between the invasion peg of D. lysipaga and the ring trap of A. dactyloides. Timper and Brodie (1993) stated that A. dactyloides as well as Arthrobotrys oligospora, Monacrosporium ellipsosporum [Dactylellina ellipsospora] and M. cionopagum killed most P. penetrans adults and juveniles in cultures. They also found that Hirsutella rhossiliensis and M. ellipsosporum [Dactylellina ellipsospora] reduced P. penetrans in sand by up to 53%. On potato, H. rhossiliensis made it difficult for P. penetrans to invade into roots, causing a 25% reduction in the nematode penetration. In Sweden, the application of milled peat or green manuring of apple nurseries reduced populations of P. penetrans and eliminated replant disease (Kauri-Paasuke, 1973a, b); it was suggested that the milled peat and green manure may have favoured nematophagous fungi and nematode-preying tardigrades. In a different approach, Miller and Anagnostakis (1977) applied chopped mycelium of the non-trapping fungus Trichoderma viride to cups of soil containing P. penetrans and achieved a 90% population reduction in 3 weeks. Kimura et al. (1996) achieved nematicidal activity of 80% towards P. penetrans with a culture filtrate from Aspergillus melleus; the active compound being aspyrone.

In contrast, Jansson and Nordbring-Hertz (1980) found P. penetrans attracted only two species (Arthrobotrys conoides and Dactylaria candida) of 13 nematophagous fungi tested; Voss and Yyss (1990) found no parasitism of the developmental stages of P. penetrans by Catenaria anguillulae; and Jansson et al. (1987) found adhesion of conidia of Drechmeria coniospora to the head and tail of P. penetrans, but no parasitism of the nematode. The nematicidal activity of filtrates from 53 strains of the biocontrol fungus Clonostachys rosea against P. penetrans was reported by Iqbal et al. (2020). Culture filtrates from 21 strains caused a 25-66% increase in nematode mortality, when compared with an 18% increase in the potato dextrose broth medium control. Culture filtrates from ten strains lowered mortality by 8-12% and for the remaining 23 strains, the effects were not significantly different from the control. Differences obtained in P. penetrans correlated with antagonism against the soybean cyst nematode (Heterodera glycines) suggesting a lack of host specificity in C. rosea. In the same study, strains with deletion of non-ribosomal peptide synthetase genes (nps4 and nps5) had reduced nematicidal activity and showed less biocontrol efficacy against root-lesion nematode disease and Fusarium foot rot on wheat cv. Stava.

Actinomycetes were also proposed as a cause of reduction of P. penetrans on tomato in glasshouses, following amendments with nitrogenous materials such as crab chitin and sewage sludge (Saka, 1978); it was suggested that a toxin from the actinomycetes works in conjunction with ammonia and nitrates. A clear example of the control of P. penetrans by an actinomycete was provided by Dicklow et al. (1993), who showed that a novel species of Streptomyces isolated from a suppressive soil in Costa Rica reduced numbers of lesion nematodes in roots of strawberry in a field trial in Massachusetts, USA, and also decreased the incidence of black root rot disease.

An isolate of Bacillus thuringiensis, tested in both the field and in the greenhouse against other nematodes, reduced P. penetrans populations in roots of strawberry in a greenhouse trial in Massachusetts, USA (Zuckerman et al., 1993). In a survey in Turkey, P. penetrans and 13 other nematode species were found with bacteria of the Pasteuria penetrans group attached to the cuticle, a first record of Pasteuria for that region (Elekcioglu, 1995). A report by Hackenberg et al. (1997) claims a significant reduction of P. penetrans in roots of strawberry as a result of the presence of a strain of Pseudomonas chlororaphis.

Different endophytic bacteria isolated from the marigolds Tagetes erecta and T. patula (=T. erecta) were shown to affect P. penetrans mortality. Out of the 49 bacterial species isolated from these plants, Microbacterium esteraromaticum, Pseudomonas chlororaphis, Kocuria varians, K. kristinae and Tsukamurella paurometabola exhibited efficacy against the nematode. Among them, M. esteraromaticum and K. varians demonstrated the highest level of mortality against P. penetrans without causing a reduction in the tuber yield (Sturz and Kimpinski, 2004). In another study, three actinomycetes (Streptomyces fulvissimus A12, S. venezuelae A30 and S. annulatus A34) and two pseudomonads (Pseudomonas sp. P3 and P. donghuensis P17) isolated from sweet cherry, decreased P. penetrans populations in onion roots below 50% of the mean level of infestation in the nematodes-only treatment, and enhanced root parameters, by possibly producing nematicidal hydrolytic enzymes and biofilms. Some of these bacteria also had anti-fungal activity against pathogenic fungi involved in cherry plant disease, such as Fusarium oxysporum C1-1, Ilyonectria macrodidyma C1-1 and Ilyonectria spp. C2-1 (Marin-Bruzos et al., 2021).

A systematic bibliographic review of the effects of arbuscular mycorrhizal fungi (AMF) on Pratylenchus spp. can be found in Gough et al. (2020). The interactions between AMF and P. penetrans were investigated through glasshouse or microplot experiments in bean (Phaseolus vulgaris) (Elliot et al., 1984), carrot (Daucus carota) (Talavera et al., 2001), dune grass (Ammophila arenaria =Calamagrostis arenaria) (Peña et al., 2006), tomato (Solanum lycopersicum) (Vos et al., 2012) and apple (Malus domestica) (Ceustermans et al., 2018). The adverse effects of P. penetrans on bean growth and yield were reduced by the presence of AMF, however the increased plant tolerance did not appear to be related to the nematode population densities (Elliot et al., 1984). The beneficial effect of AMF on crops in the presence on P. penetrans has been reported suggesting that, in general, AMF seem to lighten the plant damage caused by the nematode (Gough et al., 2020).

For many annual hosts of P. penetrans, the only effective chemical control is preplant soil fumigation. Currently, in many countries, the choice of soil fumigants is limited to metam-sodium and dazomet, both yielding methyl isothiocyanate when contacted by soil moisture and used individually, or in mixtures. The mixtures may also contain chloropicrin, if fungicidal activity is also required. 1,3 dichloropropene and methyl bromide are no longer approved in Europe (Orlando et al., 2020).

Another important group of synthetic nematicides are those based on non-fumigant products. These are non-volatile chemicals that can be applied at preplant, planting, or after planting to soil by drenching and irrigation, or by spraying the crop foliage. They can be classified as contact or systemic, whether they kill nematodes by direct exposure to the product, or while they feed on the plant, respectively. Non-fumigants such as fosthiazate are commonly used in P. penetrans control (e.g. Olthof et al., 1985; Kimpinski, 1986; Townshend and Olthof, 1988; Olthof, 1989; Kimpinski et al., 1997; Sturz and Kimpinski, 1999; Zasada et al., 2010; Han et al., 2014; Zasada and Walters, 2016). Control with non-fumigants that have been commercialized in recent years, such as fluensulfone and fluopyram, has also been reported but the efficacy appears to be variable, depending on factors such as nematode developmental stage and chemical concentration (Oka, 2014; Grabau et al., 2019; Han et al., 2023).