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Morphological and Molecular Characterization of Heterodera Schachtii and the Newly Recorded Cyst Nematode, H

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Morphological and Molecular Characterization of Heterodera Schachtii and the Newly Recorded Cyst Nematode, H Plant Pathol. J. 34(4) : 297-307 (2018) https://doi.org/10.5423/PPJ.OA.12.2017.0262 The Plant Pathology Journal pISSN 1598-2254 eISSN 2093-9280 ©The Korean Society of Plant Pathology Research Article Open Access Morphological and Molecular Characterization of Heterodera schachtii and the Newly Recorded Cyst Nematode, H. trifolii Associated with Chinese Cabbage in Korea Abraham Okki Mwamula1†, Hyoung-Rai Ko2†, Youngjoon Kim1, Young Ho Kim1, Jae-Kook Lee2, and Dong Woon Lee 1* 1Department of Ecological Science, Kyungpook National University, Sangju 37224, Korea 2Crop Protection Division, National Institute of Agricultural Sciences, Rural Development Administration, Wanju 55365, Korea (Received on December 23, 2017; Revised on March 6, 2018; Accepted on March 13, 2018) The sugar beet cyst nematode, Heterodera schachtii population whereas those of H. schachtii were strongly is a well known pathogen on Chinese cabbage in the detected in H. schachtii monoxenic cultures. Thus, this highland fields of Korea. However, a race of cyst form- study confirms the coexistence of the two species in ing nematode with close morphological resemblance to some Chinese cabbage fields; and the presence of H. tri- H. trifolii was recently isolated from the same Chinese folii in Korea is reported here for the first time. cabbage fields. Morphological species differentiation between the two cyst nematodes is challenging, with Keywords : infective juvenile, morphometrics, vulval cone only minor differences between them. Thus, this study described the newly intercepted H. trifolii population, Handling Associate Editor : Lee, Yong Hoon and reviewed morphological and molecular charac- teristics conceivably essential in differentiating the two nematode species. A comparison of morphometric The clover cyst nematode (CCN), Heterodera trifolii Gof- measurements of both infective juveniles and vulval fart, 1932 and the sugar beet cyst nematode (SBCN), H. cones of cysts showed significant differences between schachtii Schmidt, 1871 constitute the H. schachtii sensu the two cyst nematodes. When total RNA and genomic stricto group, along with H. ciceri, H. betae, H. galeopsi- DNA were extracted from a mixed field population, dis, H. daverti, H. lespedezae, H. glycines, H. medicagi- COI genes and ITS regions were clearly amplified with nis and H. rosii (Subbotin et al., 2000). H. schachtii is a primers of the two Heterodera species, suggesting that predominant threat in sugar beet production, and attacks Heterodera population collected from the Chinese cab- over 200 plant species within 23 different plant families; bage field consisted of a mixture of two species. COI most notably, the Chenopodiaceae and Cruciferae families and ITS of H. trifolii were predominantly amplified (Amiri et al., 2002; Steele, 1965). The species has a wide from nucleotides prepared from H. trifolii monoxenic distribution in several Asian countries, Europe, Austra- lia, North America, Africa and South America (Baldwin †These authors contributed equally to this work as first authors. and Mundo-Ocampo, 1991; Evans and Rowe, 1998). By *Corresponding author. contrast, H. trifolii is known to attack over 86 plant spe- Phone) +82-54-530-1212, FAX) +82-54-530-1218 cies within 9 families (Goodey et al., 1965; Mercer and E-mail) [email protected] ORCID Woodfield, 1986). The species is economically important http://orcid.org/0000-0001-9751-5390 on clover and sugar beet (Ambrogioni et al., 1999; Amiri et This is an Open Access article distributed under the terms of the al., 2002), and has a wide distribution, mostly in European Creative Commons Attribution Non-Commercial License (http:// countries like Netherlands, Sweden, Germany and Italy creativecommons.org/licenses/by-nc/4.0) which permits unrestricted noncommercial use, distribution, and reproduction in any medium, (Ambrogioni et al., 1999). It is also recorded in New Zea- provided the original work is properly cited. land, UK, USA, Russia, Canada and recently Japan (Inserra Articles can be freely viewed online at www.ppjonline.org. et al., 1993; Kimpinski et al., 1993; Sekimoto et al., 2016, 298 Mwamula et al. 2017). infested cabbage fields based on field symptoms of stunted H. schachtii and H. trifolii have similarities in host range growth, yellowing and wilting of Chinese cabbage plants. and thus, coexistence as mixed populations on the same YS503 and GC147 were subsequently cultured and main- host is possible (Steele and Whitehand, 1984). Distinguish- tained as monoxenic cultures on Chinese cabbage in pots ing the two species from each other especially at field at National Academy of Agricultural Science laboratories, level may not be feasible since both exhibit similar mor- Wanju, Korea. Mixed populations (TB372) were sampled phological body characteristics and symptoms of damage. from Chinese cabbage fields of Taebaek. Cysts were ex- However, there exist some minor morphological and mor- tracted from infested field soil samples and Chinese cab- phometrical differences useful in distinguishing all species bage roots using modified Cobb’s decanting and sieving of the H. schachtii sensu stricto group from each other at method (EPPO, 2013). Cysts were recovered from a 250 laboratory level (Amiri et al., 2002). μm sieve and filtered through Whatman® 150 mm filter The SBCN has been identified as one of the serious pests paper (GE Healthcare Life Sciences, Marlborough, USA) of economic importance on Chinese cabbage production in before handpicking using fine forceps under a stereomicro- Korea (Lee et al., 2013). Reports indicate increasing dis- scope Nikon SMZ 1000 (Nikon, Tokyo, Japan). Infective semination and infestation rates within the highland Chi- second stage juveniles (J2s) were extracted from the soil nese cabbage growing areas of Gangwon-do province (from using a modified Baermann funnel method (EPPO, 2013). 11.2 ha in 2011 to 70 ha in 2015) (Kwon et al., 2016). However, a race of cyst nematode with close morphologi- Morphological identification. Twenty J2 specimens of cal resemblance to H. trifolii was recently isolated from each species emerging from monoxenic cultured cysts (H. the same Chinese cabbage fields manifesting symptoms of trifolii YS503 and H. schachtii GC147 populations) were damage similar to H. schachtii. Chinese cabbage, Brassica heat-killed on temporary slides and directly observed or rapa chinensis L. (Bae-chu) is a highly valued economic first fixed and mounted in pure glycerin (Seinhorst, 1959). crop and the leading vegetable in both production and con- Ten vulval cones were prepared from undamaged cysts us- sumption in Korea (Chang et al., 2008; Kim et al., 2014). ing a method described in Van Bezooijen (2006). Undam- Thus, pest and disease management is very crucial, and aged cysts were soaked in water before vulval cones were efforts to combat cyst nematodes are underway (Kim et al., excised and transferred into a drop of glycerin-gelatin mix- 2016). However, correct species identification of plant par- ture. Measurements and pictures were made using Zeiss asitic nematodes is a vital milestone preceding successful imager Z2 microscope (Carl Zeiss, Gottingen, Germany), nematode control and management strategies. Therefore, fitted with a software AxioVision; Material Science Soft- this study aimed at providing a detailed morphological, ware for Research and Engineering (Carl Zeiss, Gottingen, morphometric and molecular description of the newly in- Germany), and identification was made based on the key tercepted H. trifolii population in Korea and review char- provided by Wouts and Baldwin (1998). All measurements acteristics conceivably essential in distinguishing the two were recorded in μm. Standard deviation and measurement nematode species. range were calculated and recorded for each arithmetic mean. Materials and Methods Molecular characterization. For molecular characterization, Cyst nematode populations. Samples of H. trifolii two procedures were performed using species specific (YS503) and H. schachtii (GC147) populations were taken and universal primers, respectively. Sequences of COI, from Jeongseon cabbage fields (Table 1), as part of a sur- ITS and beta-tubulin of the two Heterodera species were vey to determine the dispersal rate of cyst nematodes in the compared and species-specific primers were designed for Table 1. The nematode populations used in this study Population Date Host plant Coordinates GC147 27th Jul 2016 Chinese cabbage 37.3330700, 128.8464880 YS503 16th Aug 2017 Chinese cabbage 37.4397300, 128.8565550 TB372 9th Oct 2017 Chinese cabbage 37.2558180, 128.9830310 Coordinates for GC147 and YS503 represent individual cabbage fields where samples were taken in Jeongseon, respectively while Coordinates for TB372 represent cabbage field where mixed populations were sampled in Taebaek. Heterodera trifolii in Korea 299 COI and ITS, while conserved regions of beta-tubulin were Briefly, 10 cysts from each monoxenic population were selected for positive control amplification (Supplementary separately transferred into a drop of water on a glass slide Table 1, Supplementary Fig. 1). Total RNA and genomic and crushed gently with a piece of filter paper (smaller than DNA were extracted from cysts with TRI Reagent® (MRC, 2 mm × 2 mm in size) and small tweezers, by exertion of Cincinnati, OH, USA) according to the manufacturer’s pressure onto the filter paper. The crushed cyst contents protocol with some modifications. Six cysts (from TB372 were then transferred into the 0.2 ml PCR tubes containing
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