Meloidogyne enterolobii
2014; Wiley; Volume: 44; Issue: 2 Linguagem: Italiano
10.1111/epp.12120
ISSN1365-2338
Tópico(s)Entomopathogenic Microorganisms in Pest Control
ResumoEPPO BulletinVolume 44, Issue 2 p. 159-163 EPPO Data sheets on quarantine pests Fiches informatives sur les organismes de quarantaineFree Access Meloidogyne enterolobii First published: 26 June 2014 https://doi.org/10.1111/epp.12120Citations: 11AboutSectionsPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onFacebookTwitterLinked InRedditWechat Identity Scientific name: Meloidogyne enterolobii Yang & Eisenback, 1983 Synonyms: Meloidogyne mayaguensis Rammah & Hirschmann, 1988 Taxonomic position: Nematoda: Tylenchida: Meloidogynidae Common names: non-existent Notes on taxonomy: Meloidogyne enterolobii was described by Yang & Eisenback (1983) from roots of pacara earpod trees (Enterolobium contortisiliquum), on Hainan Island in China. In 1988 Rammah and Hirschmann described M. mayaguensis from roots of eggplant (Solanum melongena) from Puerto Rico and indicated that this new species ‘superficially resembles M. enterolobii’, but shows ‘several distinct morphological features and a unique malate dehydrogenase pattern (N3c)’. Karssen et al. (2012) re-studied the holo- and paratypes of both species and confirmed M. mayaguensis as a junior synonym for M. enterolobii. EPPO code: MELGMY Phytosanitary categorization: EPPO A2 list No. 361 Hosts The root-knot nematode Meloidogyne enterolobii is polyphagous and has many host plants including cultivated crops and weeds. It attacks herbaceous as well as woody plants. The principal hosts are Phaseolus vulgaris (bean), Coffea arabica11 It is noted that while coffee can be a good host some cultivars are resistant (see details in the control paragraph). (coffee), Gossypium hirsutum L. (cotton), Solanum melongena (eggplant), Psidium guajava (guava), Solanum quitoense (naranjilla), Carica papaya L. (papaya), Capsicum annuum (pepper), Solanum tuberosum (potato), Glycine max (soybean), Ipomoea batatas (sweet potato), Nicotiana tabacum (tobacco), Lycopersicon esculentum (tomato) and Citrullis lanatus (watermelon) (Rammah & Hirschmann, 1988; Brito et al., 2007; Gomes et al., 2008; Bitencourt & Silva, 2010; Silva et al., 2010; Quénéhervé et al., 2011; Crozzoli et al., 2012; da Silva & Krasuski, 2012; Onkendi & Moleleki, 2013; Ye et al., 2013). For Gossypium hirsutum (cotton), Brito et al. (2004) reported that four Florida isolates of M. enterolobii reproduced on this host, which confirmed the original description by Yang & Eisenback (1983). Meloidogyne enterolobii has also been reported on Ajuga, Angelonia, Aquilaria malaccensis, Brugmansia, Enterolobium contortisiliquum, Euphorbia punicea, Hibiscus, Maranta arundinasea, Morinda citrifolia, Ocimum basilicum, Paulownia elongate, Rosa, Syzygium aromaticum, Thunbergia, Tibouchina and several weeds (Carneiro et al., 2006; Kaur et al., 2007; de Almeida et al., 2011b; Han et al., 2012). Experiments carried out in the Netherlands have also shown that Cactus, Ficus, Syngonium and Vitis can also be host plants of M. enterolobii. Only a few crops have been reported as non-hosts or very poor hosts for M. enterolobii, including Brassica oleracea (cabbage), Allium sativum (garlic), Citrus × paradisi (grapefruit), Zea mays subsp. mays (maize), Arachis hypogaea (peanut), Citrus × aurantium (sour orange) and Allium fistulosum (welsh onion) (Rammah & Hirschmann, 1988; Guimaraes et al., 2003; Rodriguez et al., 2003; Brito et al., 2004; Bitencourt & Silva, 2010; Dias et al., 2010a; Rosa et al., 2012). Geographical distribution Meloidogyne enterolobii has been reported from several countries in North, Central and South America, Africa and Asia (CABI, 2000). Its present distribution in warmer climates suggests that this species will not survive outside greenhouses in northern countries of Europe, but it might be able to establish itself in the Mediterranean region. For Europe M. enterolobii was first recorded in a greenhouse in France (Blok et al., 2002), but the pest is no longer present. It has also been reported from two greenhouses in Switzerland associated with severe damage on tomato and cucumber (Kiewnick et al., 2008). Meloidogyne enterolobii has been intercepted in EPPO countries such as the Netherlands, Germany and the UK several times in imported plant material from Asia, South America and Africa (e.g. Cactus sp., Syngonium sp, Ficus sp., Ligustrum sp., Brachychiton sp., Rosa sp.). EPPO region: Switzerland (Kiewnick et al., 2008). Africa: Burkina Faso, Côte d'Ivoire, Malawi, Senegal, South Africa (Fargette et al., 1996; Willers, 1997; Onkendi & Moleleki, 2013). Asia: China (Hainan, Guangdong, Liaoning) (Yang & Eisenback, 1983), Vietnam (Iwahori et al., 2009). North America: USA (Florida, North Carolina) (Brito et al., 2004; Ye et al., 2013), Mexico (Ramirez-Suarez et al., 2013). Central America and Caribbean: Costa Rica (Humphreys et al., 2012), Cuba (Decker & Rodriguez Fuentes, 1989), Martinique (Carneiro et al., 2001), Puerto Rico (Rammah & Hirschmann, 1988), Trinidad and Tobago. South America: Brazil (Alagoas, Bahia, Ceara, Goias, Mato Grosso, Maranhao, Minais Gerais, Parana, Pernambuco, Piaui, Rio de Janeiro, Rio Grande do Norte, Rio Grande do Sul, Santa Catarina, Sao Paulo, Tocantins) (Carneiro et al., 2001, 2006; de Torres et al., 2004, 2005, 2007; da Silva et al., 2006, 2008; de Oliveira et al., 2007; de Almeida et al., 2008, 2011b; Gomes et al., 2008; Charchar et al., 2009; de Siqueira et al., 2009; Castro & Santana, 2010; de Almeida & Santos, 2011; dos Reis et al., 2011; dos Paes et al., 2012), Venezuela (Lugo et al., 2005; Perichi & Crozzoli, 2010). Biology Meloidogyne enterolobii is a sedentary endoparasite. Second-stage juveniles (J2) hatch from eggs in the soil or root debris and migrate towards the root tip of candidate host plants. Using their stylet or wounds, juveniles enter the unsuberized epidermal cells near the root tip and migrate within the cortical tissue until they initiate a permanent feeding site in close proximity to the vascular tissue. Juveniles soon lose their mobility and become sedentary. At the same time, feeding of the J2 on root cells induce those cells to differentiate into multinucleate nursing cells, so-called giant cells. At the same time the surrounding tissue starts to divide giving rise to a typical root gall or root-knot. During their further development juveniles swell to become sausage-shaped and undergo three moults before they reach adult stages. Adult females are pear-shaped and found almost completely embedded in the host tissue. Eggs are laid by the female in a gelatinous sac near the root surface. Adult males are vermiform and found free in the rhizosphere or near the protruding body of the female. As for other Meloidogyne species, reproduction is nearly almost parthogenetic. The life cycle of M. enterolobii takes 4–5 weeks under favourable conditions and females produce around 400–600 eggs. Detection and identification Symptoms Meloidogyne enterolobii affects growth, yield, lifespan and tolerance to environmental stresses of infested plants. Typical above-ground symptoms include stunted growth, wilting and leaf yellowing. Typical root galls are found below-ground which can be large in size and numbers (Cetintas et al., 2007). Overall, damage due to M. enterolobii may consist of reduced quantity and quality of yield. Plant infection with secondary plant pathogens might be enhanced following M. enterolobii infestation, such as being described for Fusarium solani on guava (Gomes et al., 2011). Morphology Second-stage juveniles are vermiform, annulated, tapering at both ends, 250–700 μm long, 12–18 μm wide, tail length 15–100 μm and hyaline tail part 5–30 μm in length (Yang & Eisenback, 1983; Rammah & Hirschmann, 1988). Females are characteristically globular to pear-shaped, pearly-white and sedentary. Their body is annulated, 400–1300 μm long, 300–700 μm wide and shows lateral fields each with 4 incisures. The stylet is dorsally curved, 10–25 μm long, with rounded to ovoid stylet knobs, set off to sloping posteriorly. The perineal pattern is round to ovoid; the arch is moderately high to high and usually rounded. The vermiform males are annulated, slightly tapering anteriorly, bluntly rounded posteriorly, 700–2000 μm long and 25–45 μm wide. The stylet is 13–30 μm long, with stylet knobs, variable in shape. Meloidogyne enterolobii closely resembles other tropical root-knot nematodes such as M. incognita, M. arenaria and M. javanica. In general, it can be separated from other species within the genus by perineal pattern shape, male and female stylet morphology; morphology of the male; body length and morphology of the lip region, as well as tail and hyaline tail part in second-stage juveniles according to EPPO Standard PM 7/103 (EPPO, 2011). The other two Meloidogyne species which are on the EPPO lists of pest recommended for regulation, namely M. chitwoodi and M. fallax, are usually not associated with M. enterolobii and can also be clearly distinguished by their demarcated hyaline tail end. Detection and inspection methods The presence of M. enterolobii in infested soil and planting material can be determined by sampling of suspected material and subsequent extraction of second-stage juveniles using standard methods described in the EPPO Standard PM 7/119 on Nematode Extraction (EPPO, 2013a). Microscopic examination at 800–1000 times magnification is necessary for correct identification of the nematode species. Presence of females and males can assist in identification. However, as morphological characters of M. enterolobii are often similar to other Meloidogyne species, identification to species level is usually based on a combination of morphological/morphometrical characters and biochemical or molecular methods (isozymes or PCR). For details see the EPPO Diagnostic Protocol (EPPO, 2011). Means of movement and dispersal As is the case for other plant-parasitic nematodes M. enterolobii's own movement is limited at most to a few tens of centimetres in the soil. The main routes for nematode dissemination are by infested planting material and soil, such as traded host plants or cuttings with roots, traded soil bearing products such as potatoes, soil attached to equipment and machinery and irrigation water. Pest significance Economic impact Meloidogyne enterolobii is considered as very damaging due to its wide host range, high reproduction rate and induction of large galls (Castagnone-Sereno, 2012). Severe damage caused by M. enterolobii has been reported for Psidium guajava (guava; da Silva & Krasuski, 2012; Martins et al., 2013), Lycopersicon esculentum (tomato) and Citrullis lanatus (water melon; Cetintas et al., 2007; Kiewnick et al., 2009; Ramirez-Suarez et al., 2014) and Enterolobium contortisiliquum (pacara earpod tree, Yang & Eisenback, 1983). Compared with other root-knot nematode species, M. enterolobii displays virulence against several sources of root-knot nematode-resistance genes and therefore is considered particularly aggressive. For example, M. enterolobii develops on crop genotypes carrying resistance to the major species of Meloidogyne, including resistant cotton, sweet potato, tomatoes (Mi-1 gene), potato (Mh gene), soybean (Mir1 gene), bell pepper (N gene), sweet pepper (Tabasco gene) and cowpea (Rk gene) (summarized in Castagnone-Sereno, 2012). In countries where M. enterolobii is regulated, traded plants and plant products infested with M. enterolobii may need to be destroyed. Control General management strategies for root-knot nematodes have been recently reviewed by Coyne et al. (2009) and Nyczepir & Thomas (2009). Taking into account the banning of most chemical nematicides, growing non host crops or black fallow are the most efficient methods for reducing M. enterolobii populations. Unfortunately, the list of non host plants is very small, including cabbage, garlic, grapefruit, maize, peanut, sour orange and welsh onion. Brito et al. (2007) reported on two carrot cultivars and collard allowing very little or no nematode reproduction. Of various selections of Phaseolus vulgaris, P. lunatus, Vigna radiata, V. unguiculata and Canavalia ensiformis being tested for their susceptibility to M. enterolobii only P. vulgaris cv. Alabama was resistant (Crozzoli et al., 2012). Squash and lettuce showed some resistance towards M. enterolobii (Bitencourt & Silva, 2010) and eight genotypes of soybean turned out to be tolerant to M. enterolobii while 60 genotypes were susceptible (Dias et al., 2010b). Compared to annual crops, more sources of resistance towards M. enterolobii have been reported for perennial crops such as the R Mia resistance gene in peach rootstocks (Claverie et al., 2004; Nyczepir et al., 2008), the Ma gene in Myrobolan plum (Rubio-Cabetas et al., 1999) and some newly detected resistance in wild Psidium sp. accessions that might serve in the future as rootstock for guava (Carneiro et al., 2007; de Almeida et al., 2009). Although coffee has been reported as a principal host for M. enterolobii (Decker & Rodriguez Fuentes, 1989), all seven coffee cultivars tested by Alves et al. (2009) turned out to be resistant, thus leaving the host status of coffee unresolved. Phytosanitary risk Recent reports of M. enterolobii in glasshouses in the EPPO region clearly demonstrate that it has the potential to enter Europe (Blok et al., 2002; Kiewnick et al., 2008). It was also recently detected in the USA during routine regulatory sampling at ornamental nurseries in South Florida which has a comparable climate to Southern Europe (Han et al., 2012). It is very likely that this species can survive in the warmer parts of the EPPO region and in glasshouses throughout the EPPO region. In addition, this species was detected on roses (plants for planting) originating from China (see EPPO RS 2008/107), thus suggesting that it can also survive slightly cooler temperatures. Once root-knot nematodes have been introduced, it is in general difficult to control or eradicate them. Phytosanitary measures No specific quarantine requirements for M. enterolobii are yet in force. However, measures similar to those recommended by EPPO for Meloidogyne chitwoodi and M. fallax (EPPO, 2013b) seem to be relevant, i.e. that consignments of rooted plants should come from areas where the pest does not occur or from fields found to be free of M. enterolobii. 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