Root-knot nematodes, Meloidogyne spp.
Importance and spread
These obligate parasites have a broad host range including potato roots and tubers in addition to many other plant species. So, root-knot nematodes (RKNs) are referred to as the most economically important group of parasitic nematodes. Moreover, several pathotypes or races may constitute a species. About 100 RKN species have been known (Karssen et al. 2013). However, a few species have been parasitizing potato. Contrary to other nematode genera, which have a survival stage like the cyst in the cyst nematodes, RKN populations are decreased rapidly in the absence of a suitable host due to the lack of such a stage. Those of the temperate zone includes M. chitwoodi, M. hapla, M. fallax, and M. minor (Wesemael et al. 2014). On the other hand, three species are considered important on potato in the tropics and subtropics including Egypt. These are Meloidogyne incognita as the most broadly distributed, followed by M. javanica and M. arenaria (Niere and Karuri 2018). Ibrahim et al. (2010) reported that Meloidogyne was the most frequently sampled PPN genus associated with many host plants in Egypt. Also, Bakr et al. (2011) found that percentage of occurrence of Meloidogyne spp. was 96.26% in Egyptian fields of newly reclaimed areas, which are often planted with vegetable crops such as potato.
Symptoms and damage
Symptoms of potato damage and RKN biology are generally similar to those reported on other crops in Egypt (Abd-Elgawad 2020). For example, potato plants suffer deficiency of nutrients and water (Fig. 1). Subsequently, stunting, premature wilting, leaf chlorosis, and delayed revival to sufficient irrigation are common (Grabau and Noling 2019). Nonetheless, both potato tubers and roots are infected and galled, but the first generation usually takes place primarily on the root system with different sizes and shapes of galls. The following RKN generations can penetrate the tubers (Pinkerton et al. 1991). When tubers are infected, warty or pimple-like swellings are found on the surface (Fig. 2). The penetration depth of tubers by RKNs differs presumably due to the tuber size and composition. The females are frequently found 1–2 mm below the skin. They feed on vascular tissue. All RKN species make necrotic spots which appear between the tuber surface and the vascular ring, a reaction to the laid eggs and the gelatinous matrix. As much as 12 generations were completed by M. incognita on susceptible potato plants under favorable environmental conditions; optimal soil temperature range is 21.1 to 26.7 °C in the potato rhizosphere (Santos 2001). This range is favorable for M. incognita, M. javanica, and M. arenaria; the three common species in Egypt (Ibrahim 1985). Plants showing such symptoms usually happen in aggregations or patches, but the time of their appearance differ according to the degree of cultivar susceptibility, nematode population level, and predominant environmental conditions. Extended distribution and spread of RKNs occurs via infected tubers (seed potatoes); transplants of other susceptible plant species; mulching with infested soil; and movement of infested soil by field machinery, supplies, and watering (Abd-Elgawad and McSorley 2009).
Disease complex
It may occur when RKNs interact with other pathogens. In Egypt, potato brown rot disease caused by the bacterium Ralstonia solanacearum is one of the most important diseases since many shipments of potatoes exported abroad were refused due to quarantine restrictions imposed on the potato brown rot (Kabeil et al. 2008). The most important interaction of RKNs on potatoes is possibly facilitating the route for this bacterium (Siddiqui et al. 2014). Additionally, the invasion of M. incognita to potatoes can break the plant resistance to bacterial wilt of potatoes (Jatala and Martin 1977). Niere and Karuri (2018) reported other RKN interactions with different fungi such as Rhizoctonia solani and Verticillium spp., which aggravate the inflicted damage by RKNs to quantitative and qualitative potato yield.
The potato cyst nematodes (PCNs), Globodera spp.
Importance and spread
Species related to Globodera are highly specialized parasites of plants. Contrary to RKNs, they have a quite narrow host range. However, their biology and life cycle resemble all cyst nematodes of their previously synonymized genus Heterodera. So, nematode eggs within the cysts can keep viable for numerous years. Because of their long-term strategy of survival within the cysts, serious damage to their host plants, and difficult control measures, PCNs are listed in quarantine regulations of more than 100 countries (Niere and Karuri 2018). Globodera rostochiensis and G. pallida are the most common PCN species, but other Globodera spp. of potato were recorded (Subbotin et al. 2010). For example, Globodera ellingtonae, G. leptonepia, and G. capensis need further studies of their pathogenicity and host range. Generally, PCNs are primarily distributed in temperate regions of the world but could be detected in warmer tropical and subtropical areas. Strikingly, Globodera rostochiensis was recently isolated from potato field, as a new record of the country, from El-Nobarria, El-Behera governorate in northern Egypt. It is the only species of this genus (Ibrahim et al. 2017). Being a serious parasite and a potential pest on potato and other solanaceous crops, further investigations are required concerning its distribution, damage, and economic importance as well as other cyst nematode species in Egypt. Schemes distinguishing PCN populations according to their virulence, races, and pathotypes have been in progress for their accurate characterization. Such differential schemes are usually based on host suitability designations, i.e., cultivars with susceptibility/resistance to PCNs. However, resistance-breaking pathotypes may take place. The frequent emergence of these pathotypes indicates the dire need to minimize selection pressure on PCN populations in the field via cultivating potato in relatively long rotations with adequate and other options for PCN control. Although the selection of new virulent phenotypes will still happen, the cultivation of resistant potato cultivars remains the most available ecofriendly and economically sustainable management measure on infested fields (Niere and Karuri 2018).
Symptoms and damage
As with other PPNs, symptoms associated with PCN infections result from root injury and consequent stresses of reduced water and nutrient uptake (Fig. 1). Thus, the only method to determine the nematode genus/species infecting the potato plant is via isolation and identification of the infecting nematodes. Trudgill and Cotes (1983) reported early plant senescence as frequently associated with PCN infection. Also, tuber weight decrease usually happens (Schomaker and Been 2013). The distribution of PCN infestation foci in fields may often lead to dispersed patches of infected plants. It is apparent that these symptoms are not specific to PCN infestations but such patchy distribution (Fig. 1) of generally PPN-infected plants is quite common (Abd-Elgawad and Hasabo 1995). Admittedly, the magnitude of plant damage is highly impacted by the PCN population density in the soil, potato cultivar-tolerance or resistance level, agricultural practices, and environmental conditions. The PCNs, like other PPNs, often spread passively due to their very limited movement in soil. This passive spread can be via potato crop residues, PCN-contaminated machinery, soil mulching, especially to modify soil texture in newly reclaimed areas, infested-potato seeds, irrigation water, and field supplies (e.g., contaminated bags, containers). Composting and heat treatment are effective against PCNs. Clean planting material along with clean equipment is the best way to prevent the introduction and spread of PPNs such as PCNs. Needless to remind that absence of nematode-specific symptoms can further embarrass early detection. Fields unknowingly infested may help nematode spread to uncontaminated fields/areas. Although PCNs are host specific, other plant species are involved in their limited host range. These may comprise eggplant, tomato, and a few solanaceous weeds. However, Evans and Stone (1977) reported that these plant species are not considered as efficient hosts.
Disease complex
As other sedentary, endoparasitic nematodes, PCNs usually furnish entry sites for fungi and bacteria which aggravate potato yield losses via disease complexes (Storey and Evans 1987). Such interactions have been recorded between Globodera pallida and Verticillium dahliae (Franco and Bendezu 1985), Ralstonia (Pseudomonas) solanacearum (Jatala et al. 1976), and Rhizoctonia solani (Back et al. 2006). Although PCNs are considered the most important nematode pests of potato, yield losses are shaped by such factors as PCN species, virulence type, potato cultivar, and population density, as well as ecological and biological factors (Niere and Karuri 2018). Turner and Subbotin (2013) recorded 9% losses of potato yield due to PCNs. Moreover, such losses may end with total loss of the crop when PCNs are left uncontrolled. On the other hand, increased potato production costs in the presence of PCNs will be due to increased amounts of fertilizers, application of nematicides, and limitations on using PCN-infested area as phytosanitary measures. Hence, in large scale potato-production systems, economic consequences are likely to be higher than that of small scale systems.
Other plant-parasitic nematodes of potato
It should be stressed that PPN genera/species of potential economic importance on potato cultivation usually differ from one country/region to another. Therefore, their economic importance as major parasites of potato may vary from one region to another. For example, those important in Florida, USA are Meloidogyne spp., Belonolaimus longicaudatus, and Nanidorus minor (Grabau and Noling 2019). Moreover, other PPNs such as Nacobbus aberrans and Ditylenchus spp. have been studied in details on potato in a few countries except Egypt. In Egypt, such nematode species were mostly found in association with other field crops. In this respect, few species of the genus Ditylenchus were common on certain host plants including potato, i.e., Allium cepa, Arachis hypogaea, Cynodon dactylon, Hordeum vulgare, Oryza sativa, Phoenix dactylifera, Plantago major, Solanum tuberosum, Thymelaea hirsuta, Vicia faba, and Zea mays with 21.7% frequency of occurrence (Ibrahim et al. 2010). To the best of my knowledge, Nacobbus sp. was detected only from a tomato field (Oteifa 1960) hitherto. Nevertheless, PPN species such as those related to nematode genera Pratylenchus, Tylenchorhynchus, Longidorus, Rotylenchulus, Xiphinema, and Hoplolaimus are scattered mostly with variable population densities and much less frequencies of occurrence than RKNs in various cropping systems of Egypt, especially in light, followed by silty soils. Therefore, their suspected pathogenicity and threshold levels deserve more studies especially on potato plants. Action thresholds for managing RKNs are as low as they equal just one individual of any RKN species per 100 cm3 of potato-cultivated soil as pre-plant population density (Abd-Elgawad and Askary 2015). As in Florida, USA, the latter authors reported these thresholds to be 1, 80, 1, 40, and 10 individuals of the nematode genera Belonolaimus, Pratylenchus, Trichodorus, Tylenchorhynchus, and Dolichodorus (the awl nematodes), respectively per 100 cm3 of soil prepared for potato cultivation. Damage thresholds of the cyst nematodes for tuber yield may differ according to edaphic and biotic factors and environmental conditions (CABI 2020). On the other hand, host suitability designations of many potato cultivars against both Meloidogyne javanica and R. reniformis were recently reviewed and appraised (Montasser et al. 2019). Also, Pratylenchus spp. were so abundant in an Egyptian field located at Giza governorate that their nematicidal control could increase potato cv. Spunta yield production by 30% relative to the untreated check (Mohammed and Elkelany 2017). Globally, Orlando et al. (2020) stressed that certain lesion nematode species like P. neglectus, P. penetrans, and P. scribneri can degrade quantitative and qualitative tuber yield of potato. In contrast, in newly reclaimed area in North West Egypt, the most predominant nematode genera were Meloidogyne, Tylenchorhynchus, Helicotylenchus, and Rotylenchulus reniformis; they had both the highest population levels and percentage frequency of occurrence (Korayem et al. 2015). Generally, one or more of these PPN species may be found in some potato fields at both high frequencies of occurrence and population levels. So, such species require further studies at least to investigate their economic significance, and consequently, action thresholds may be defined.