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First Report of Northern Root-Knot Nematode, Meloidogyne Hapla (Chitwood, 1949) on Strawberry in Turkey

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First Report of Northern Root-Knot Nematode, Meloidogyne Hapla (Chitwood, 1949) on Strawberry in Turkey JOURNAL OF NEMATOLOGY Article | DOI: 10.21307/jofnem-2021-002 e2021-02 | Vol. 53 First report of northern root-knot nematode, Meloidogyne hapla (Chitwood, 1949) on strawberry in Turkey Adem Özarslandan1,*, Dilek Dinçer2, 2 3 Şefika Yavuz and Ayşenur Aslan Abstract 1Mersin University Applied Technology and Management, Strawberry is one of the most economically important crops School of Silifke, 339400, Silifke, worldwide. Several species of plant-parasitic nematodes have been Mersin, Turkey. reported to be pathogenic on strawberries, among them the northern root-knot nematode (Meloidogyne hapla), which considered to be 2Biological Control Research strawberry most important nematode pest worldwide. In August 2019, Institute, Ministry of Agriculture, strawberry growers at Silifke (Mersin, Turkey) identified nematode-like 01321, Yüreğir, Adana, Turkey. symptoms on strawberry roots and infected seedlings were brought 3Plant Protection Department, to the nematology laboratory at of Mersin University for diagnostics. Faculty of Agriculture, Atatürk Roots were separated into small pieces and nematode extraction University, 25040, Yakutiye, was performed by a modified Baermann funnel method and identified Erzurum, Turkey. under the microscope. DNA was extracted from individual nematodes using Worm Lysis Buffer(WLB (+)). The species-specific SCAR *E-mail: [email protected] markers (JMV1, JMV2, and JMVhapla) yielded a 440 bp band specific This paper was edited by to M. hapla. The 28S rRNA gene region, obtained using the general Zafar Ahmad Handoo. primers D2\D3, sequence was analysed from. The analyzed sequence Received for publication was 100% identicle to M. hapla. The gene sequences were deposited July 12, 2020. into GenBank database with accession numbers MN897751 and MN895037. Both morphological and molecular diagnostic methods confirmed that the strawberry plants collected in Silifke were infested with M. hapla. To our best knowledge this is the first report of plant- parasitic nematode species M. hapla infecting strawberry in Turkey. Currently, the adverse effect of RKN on strawberry production in the region is unknown to strawberry growers. Keywords Meloidogine hapla, Root-knot nematode, Strawberry. Strawberry is a crop with global economic significance. 1949) and the northern root-lesion nematode (RLN) Strawberry is cultivated mostly in China, USA, Mexico, Pratylenchus penetrans (Cobb) (Filipjev and Shuurmans Egypt, Turkey, and Spain (FAOSTAT, 2019). Strawberry Stekhoven) are the most harmful nematodes production is conducted in all regions in Turkey and a worldwide (Bélair and Khanizadeh, 1994; Brown et al., total production is 486 705 ton an area of 16,089 ha. In 1993; Nyoike et al., 2012; Samaliev and Mohamedova, total, 65,998 ton strawberry is produced on an area of 2011). Foliar nematodes, such as Aphelenchoi- 1,650 ha in Mersin province Silifke district (TUİK, 2019). des fragariae (Christie, 1932; Ritzema-Bos, 1891), The nematode leads to significant yield losses and Aphelenchoides ritzemabosi (Schwartz, 1911; Steiner crop damages in several host plants due to feeding by and Buhrer, 1932), Aphelenchoides besseyi (Christie, a dense population of second-stage juvenile. Several 1942), and Ditylenchus dipsaci (Filipev, 1936; Kühn, plant-parasitic nematode species were reported to 1857) were reported as strawberry pests in the USA, cause damages in strawberries, and the northern root- Europe, Australia, and the former USSR (Brown et al., knot nematode (RKN) Meloidogyne hapla (Chitwood, 1993). Needle and dagger nematodes in Longidorus © 2021 Authors. This is an Open Access article licensed under the Creative 1 Commons CC BY 4.0 license, https://creativecommons.org/licenses/by/4.0/ First Report of Northern Root-Knot Nematode, Meloidogyne hapla on strawberry in Turkey: zarslandan et al. and Xiphinema genera were associated with the nematode individuals, plant roots were cut into transmission of viruses and decline in strawberry small pieces, placed on modified Baermann funnel, yields (Brown et al., 1993). The sting nematode, and the isolated nematodes were identified under Belonolaimus longicaudatus (Rau, 1958), significantly the microscope based on J2 morphological and restricted commercial strawberry production in Florida morphometric parameters (tail length, hyaline terminus (Noling, 2011). Stunted plants and reduced yield were length, stylet length, distance between DGO and the frequently associated with M. hapla, P. penetrans, stylet base) in Silifke district of Mersin (Hartman and D. dipsaci, and Hemicyclio phora spp. in Spain (Bascón Sasser, 1985). Pathogenicity tests were conducted in et al., 2012; Peña-Santiago et al., 2004; Vega et al., the greenhouse at 24 ± 2°C under 16 h/8 h day/night 2002). Nematodes open the door for soil-borne photoperiod with disease-free strawberry plants in pots bacteria and fungi, and pests in the wounds they cause that contained sandy soil. Two nematode isolates were in plant root. Nematodes leads to further damages in used in six replicates and inoculation was conducted the plant with soil-borne fungi and bacteria. by releasing 1,000 juveniles per pot. Non-inoculated The strawberry cultivation is economically signi- control plants were irrigated with an equal volume of ficant in Turkish agricultural industry and cultivated water. The experiment was terminated on 60th post- mainly in Mediterranean provinces such as Mersin. inoculation day. Isolation of DNA was conducted on The production of the plant is the highest among 2 to 3 larvae based on the protocol. The larvae were agricultural products in Mersin province and the collected into Eppendorf tubes and WLB (+) was strawberry fields are mostly concentrated in Silifke added, and the samples were incubated at 65°C for district. In 2019, damages were observed in certain 1 hr and at 95°C for 10 min to obtain the genomic DNA strawberry plants that resembled the root-knot (Waeyenberge et al., 2000). The species-specific SCAR nematode (Meloidogyne spp.) such as galling on markers (JMV1, JMV2, and JMVhapla) were used for roots and stunting. The present study was conducted M. hapla (Wishart et al., 2002). The PCR was conducted to determine the type of root-knot nematode that led with the general primers D2\D3 that encode 28S rRNA to small galling on the roots of strawberry plants. gene region and PCR products were sequenced. Material and method Results Nematode isolation and identification Morphological and molecular identification of the nematode To determine the presence of Meloidogyne, soil and galled plant samples were transferred to Mersin This study was conducted to determine the species University nematology laboratory (Fig. 1). To isolate of root-knot nematode that causes galls of various Figure 1: Damage of Meloidogyne hapla on strawberry roots. 2 JOURNAL OF NEMATOLOGY sizes on strawberry roots. The inoculated strawberry (MN897751 and MN895037) were 100% identical plants exhibited typical galling on roots. Koch’s with others (MN475814, MN446015, MK2133550, postulates were confirmed by re-isolating the root- and MN752204) available in the NCBI database. knot nematodes in the inoculated plants. The second- The present study reported the first identification of stage M. hapla juveniles isolated in Silifke demonstra- M. hapla in strawberry fields. In Turkey, it was not ted the following morphometric characters: (n = 12), identified in strawberry fields in previous studies con- L = 371.3 ± 4.52 µm; a = 25 ± 1.3; b = 4.3 ± 0.2; c = 7.6 ± ducted in Zonguldak and Bartın provinces in the Black 0.2, c′ = 4.9 ± 0.3; Stylet = 11.1 ± 0.3 µm; Tail = 49.2 ± 1 µm; Sea Region, Bursa, Yalova, and Istanbul provinces hyaline = 13.8 ± 0.6 µm. The species-specific SCAR in the Marmara Region, and Mersin province in the markers (JMV1, JMV2, and JMVhapla) yielded a Mediterranean Region (Özarslandan, 2019). Several 440 bp band specific to M. hapla (Fig. 2). The PCR plant-parasitic nematode species were reported in was conducted with the general primers D2\D3 that strawberries, among which the most harmful was the encode 28S rRNA gene region and PCR products were northern root-knot nematode (M. hapla) (Nyoike et al., sequenced. The obtained sequence was 100% identical 2012). The northern root-knot nematode (M. hapla) and with M. hapla. The gene sequences were uploaded root-lesion nematode (P. penetrans) are also significant to the GenBank database with access numbers strawberry pests observed in several cultivation regions MN897751 and MN895037. Both morphological and (Esnard and Zuckerman, 1998; Medina-Minguez et al., molecular diagnostic methods confirmed that the 2012; Lopez-Aranda et al., 2016), and were likely strawberry plants collected in Silifke were infested with introduced to Florida from northern states and Canada M. hapla. To our best knowledge, the present study via contaminated transplant material (Nyoike et al., is the first report on plant-parasitic nematode species 2012). Second-stage M. hapla juveniles penetrate the M. hapla infection in strawberries in Turkey. Currently, young roots, leading to root galls that disrupt water the adverse effects of RKN on strawberry production in intake and the physiology of the infected plant, and the region is unknown to strawberry farmers. may lead to severe stunting in sandy soil (Pinkerton and Finn, 2005). P. penetrans causes severe root Discussion necrosis and could predispose infested roots to secondary infections due to opportunistic fungal The species-specific SCAR markers (JMV1, JMV2, pathogens
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