KSÜ Tarım ve Doğa Derg 27 (5), 1055-1060, 2024

KSU J. Agric Nat 27 (5), 1055-1060, 2024

https://doi.org/10.18016/ksutarimdoga.vi.1334097

First Record of Meloidogyne javanica (Treub, 1885) (Chitwood, 1949) on Lettuce (Lactuca
sativa L.) Growing Areas in the Southern Marmara Region

Ayşenur YILMAZ1, Taylan ÇAKMAK2, Uğur GÖZEL3
1,3Department of Plant Protection, Faculty of Agriculture, University of Çanakkale Onsekiz Mart, Çanakkale, Türkiye, 2Department of
Agricultural Biotechnology, Faculty of Agriculture, Düzce University, Düzce, Türkiye
1https://orcid.org/0000-0002-3873-6537, 2https://orcid.org/0000-0003-4151-5724, 3https://orcid.org/0000-0003-1363-1189

: ugozel@comu.edu.tr

ABSTRACT Plant Protection

Root-knot nematodes are the most important plant parasitic nematode
group due to their wide host range and difficulties in control and cause Research Article
significant quality and yield losses in vegetables including lettuce
plants. Root-knot nematodes are causing symptoms such as yellowing, Article History
wilting, and stunting on lettuce plants. For monitoring lettuce fields for Received : 28.07.2023
detecting nematode-infected areas, surveys were made to the lettuce Accepted : 13.11.2023
growing areas of Çanakkale province in the winter months of 2021-2022
and the plants infected with root-knot nematodes were examined and Keywords
pure nematode cultures were obtained in the laboratory. A total of 16 Lettuce
plant and soil samples were taken and 3 of them were found to be Southern Marmara Region
infected with root-knot nematodes. Species identification was made Root-knot nematode
using morphological methods and morphometric measurements from
second-stage infective juvenile and female individuals obtained from
pure cultures. As a result, the first record of Meloidogyne javanica in
lettuce-growing areas in the Southern Marmara Region was made in
this study.

Güney Marmara Bölgesi Marul (Lactuca sativa L.) Yetiştirilen Alanlarda Meloidogyne javanica
(Treub, 1885) (Chitwood, 1949)’nın İlk Kaydı
ÖZET Bitki Koruma
Bitki paraziti nematodlar arasında yer alan Kök-ur nematodları, geniş
konukçu yelpazesi ve mücadelesindeki zorluklardan dolayı en önemli Araştırma Makalesi
bitki paraziti nematod grubunu oluşturmaktadır. Sebzelerde önemli
kalite ve verim kayıplarına sebep olan Kök-ur nematodları marul Makale Tarihçesi
bitkisinin de önemli bir konukçusudur. Kök-ur nematodları marul Geliş Tarihi : 28.07.2023
üzerinde sararma, solma ve bodurlaşma gibi belirtiler meydana Kabul Tarihi : 13.11.2023
getirmektedir. Marul yaprakları tüketilen bir sebze olmasından dolayı Anahtar Kelimeler
üreticiler tarafından bu durum istenmemektedir. Bu amaçla Çanakkale Marul
ili marul yetiştirilen alanlara 2021-2022 yılları kış aylarında periyodik Güney Marmara Bölgesi
olmayan arazi çıkışları yapılmış ve Kök-ur nematodlarıyla bulaşık Kök-ur nematodu
bitkiler incelenmiş, ardından saf kültürleri oluşturulmuştur. Toplam 16
bitki ve torpak örneği alınmış 3 tanesinin kök-ur nematodları ile
bulaşık olduğu tespit edilmiştir. Morfometrik ölçümler ve morfolojik
yöntemlere göre, saf kültürlerden elde edilen ikinci dönem larva ve dişi
bireylerden tür teşhisi yapılmıştır. Bu çalışma Güney Marmara Bölgesi
Marul yetiştirilen alanlardaki Meloidogyne javanica’nın ilk kaydıdır.
Atıf Şekli: Yilmaz, A., Çakmak, T., & Gözel, U., (2024). Güney Marmara Bölgesi Marul (Lactuca sativa L.) Yetiştirilen
Alanlarda Meloidogyne javanica (Treub, 1885) (Chitwood, 1949)’nın İlk Kaydı. KSÜ Tarım ve Doğa Derg 27
(5), 1055-1060. https://doi.org/10.18016/ksutarimdoga.vi.1334097
To Cite : Yilmaz, A., Çakmak, T., & Gözel, U., (2024). First Record of Meloidogyne javanica (Treub, 1885) (Chitwood,
1949) on Lettuce (Lactuca sativa L.) Growing Areas in the Southern Marmara Region. KSU J. Agric Nat
27(5), 1055-1060. https://doi.org/10.18016/ksutarimdoga.vi.1334097

INTRODUCTION over the world and live as parasites on plants,

Nematodes have adapted to almost all environments, animals, and humans (Cavaness & Jensen, 1955;
including terrestrial and aquatic habitats; and belong Boag et al., 1998). The Tylenchida (Nematoda) order
to the “Nematoda” clade, which are distributed all constitutes the most important group among the
KSÜ Tarım ve Doğa Derg 27 (5), 1055-1060, 2024 Araştırma Makalesi
KSU J. Agric Nat 27 (5), 1055-1060, 2024 Research Article

Plant Parasitic Nematodes (PPNs), containing most of consumed.

the harmful species. The lettuce plant (Balkaya et al., 2017), which
Root-knot nematodes (RKNs) are in first place among originated from Anatolia, Caucasus, Iran, and
PPNs in terms of their prevalence in the world, Turkistan region, is among the vegetables whose
difficulties in control, and the level of economic leaves are consumed in the Asteraceae family. The
damage they cause to plants (Taylor & Sasser, 1978; optimum growth temperature of lettuce, which is a
Whitehead, 1998; Karssen & Moens, 2006; one-year cool climate vegetable, is around 15-18 °C,
Kalaiarasan, 2009; Jones et al., 2013). About 100 and the temperature exceeding 20 °C negatively
RKN species have been identified in different hosts in affects its development. In addition, lettuce can
the world to date (Trinh et al., 2019), but most withstand temperatures as low as -2 or -3 °C below 0
commonly, M. incognita (Kofoid & White, 1919) °C for a short time (Splittstoesser, 1990; Günay,
Chitwood, 1949, M. arenaria (Neal, 1889) Chitwood 1992).
1949, M. javanica (Treub, 1885) Chitwood 1949 ve M. As a result of the studies, aphids (Aphis gossypii,
hapla Chitwood 1949 (Netscher & Sikora, 1990; Myzus persicae), thrips (Thrips tabaci, Frankliniella
Eisenback & Triantaphyllou, 1991; Karssen, 2000; occidentalis), leafhoppers (Empoasca decipiens,
Hunt et al., 2005) are known all over the world. Asymetresca decedens), whitefly (Bemisia tabaci) and
Root-knot nematodes are among the most important leaf worms (Spodoptera littolarigera) are among the
organisms in vegetable production because they are species that cause significant damage in lettuce
found in 52% of cultivated agricultural lands and cultivation. Apart from these, RKNs are also reported
have a wide host range (Sasser, 1977; Taylor, 1987; to cause significant yield and quality losses in lettuce
Trudgill & Blok, 2001). This is because RKNs are cultivation (Akyazı & Ecevit, 2011; Uzunoğulları et
polyphagous organisms, having about 5500 host al., 2022).
plants, and cause significant yield losses in vegetables Therefore, in this study, it was aimed to determine
reaching up to 15-85% of total production (Trudgill & the distribution of root-knot nematodes in lettuce-
Block, 2001; Anonymous, 2008). growing areas in Çanakkale and to determine the
Root-knot nematodes are distinguished from other species found in the areas by morphological and
plant parasitic nematodes (PPNs) by the typical galls morphometric methods.
they form on the roots, which gives the species its
name. Root-knot-type root galls occur as a result of MATERIAL and METHOD
hypertrophy (cell growth) and hyperplasia (increase The main material of the study consists of root and
in the number of cells) of the cells on which the soil samples taken from lettuce cultivation areas of
nematode creates a feeding site (Bridge & Starr, Çanakkale province and its districts and female and
2007). Above-ground symptoms (yellowing, wilting, second-stage infective juveniles of Meloidogyne spp.
stunting) caused by root-knot nematodes on obtained from these samples.
vegetables produce significant quality and yield
losses, especially for vegetables whose leaves are

Figure 1. Lettuce plant roots infected by Meloidogyne javanica a: Sample No: 85, b: Sample No: 107, and c:
Sample No: 115.
Şekil 1. Meloidogyne javanica ile infekteli marul bitkisi kökleri a: Örnek 85, b: Örnek 107 ve c: Örnek 115.

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KSU J. Agric Nat 27 (5), 1055-1060, 2024 Research Article

In the winter months of 2021-2022, non-periodic land cut and put in pure glycerin between the slide and the
surveys were made to the lettuce-growing areas in coverslip (Hooper, 1986). Morphological
Çanakkale. A total of 16 plant and soil samples were identifications of female individuals were made
taken from lettuce growing areas in Çanakkale according to Jepson (1987) and Karssen (2002).
province and its districts, including 7 in the center, 3
in Ezine, 2 in Ayvacık, 2 in Biga, 1 in Çan, and 1 in RESULTS and DISCUSSION
Lapseki. The results of the diagnostic studies performed with
The plants found in these areas were examined, and morphological and morphometric methods showed
the roots of the plant samples showing signs of that the species infecting the roots of the lettuce plant
infestation with root-knot nematode were brought to was M. javanica (Table 1; Figure 2,3).
the laboratory and examined under a binocular According to the species identification, taxonomy
microscope (Figure 1). After the roots infested with studies related to root-knot nematodes conducted in
root-knot nematodes were detected, an egg pack was Turkey, 11 different root-knot nematode species (M.
taken from the root of each sample with forceps under incognita, M. javanica, M. arenaria, M. hapla, M.
a binocular microscope. The collected egg packets chitwoodi, M. artiellia, M. Arita, M. luci, M. exiqua,
were used to infect the root-knot nematode-sensitive M. Thames and M. Ethiopia) were identified
tomato cultivar "Troy F1" and pure nematode (Kepenekçi et al., 2002; Devran & Söğüt, 2009;
cultures were formed ahead. After about 60 days, Özarslandan & Elekçioğlu, 2010; Aydınlı et al., 2013;
female individuals of root-knot nematodes grown in İmren et al., 2014; Aydınlı & Mennan, 2016; Aydınlı,
pure cultures for diagnostic studies and second-stage 2018; Ataş, 2021; Yılmaz et al., 2023). In previous
infective juveniles (J2s) were obtained from the egg studies, M. javanica species were detected in
packages laid by these females using the sieve tomatoes, cucumber, eggplant, bean, celery, okra
method. plants, and lettuce (Uysal et al., 2017; Yağcıköse,
J2s obtained from egg packs were fixed in TAF 2021).
solution and then fixed on a slide in pure glycerin In previous studies in our country, M. incognita
according to the method of Seinhorst (1959) and made species was detected in lettuce-growing areas (Akyazı
ready for species identification. Twenty-five root-knot & Ecevit, 2011: Uzunoğulları et al., 2022). Uysal et al.
nematode second-stage infective juveniles were (2017) detected the M. javanica species in the lettuce-
measured for each infected sample. Standard growing areas of the Lake District. However, M.
identification characters used in the morphological javanica has not been detected in lettuce-growing
and morphometric diagnosis of second-stage infective areas in the Southern Marmara Region.
juveniles were made using a Leica DM1000 light In this study, a survey was made in the lettuce-
microscope according to Jepson (1987), and species- growing areas of the Southern Marmara Region and
level diagnosis was made according to Whitehead it was confirmed that the species obtained from the
(1968) and Özarslandan (2009). After the female lettuce plant was M. javanica by morphological and
individuals were obtained, they were kept in 45% morphometric methods.
lactic acid. After that step, 1/3 of the vulva region was

Figure 2. The perineal pattern of Meloidogyne javanica from lettuce a: Sample No: 85, b: Sample No: 107, and c:
Sample No: 115 (Scale Bar: 20 μm).
Şekil 2. Maruldan elde edilen Meloidogyne javanica’ya ait perineal pattern a: Örnek 85, b: Örnek 107 ve c: Örnek
115 (Ölçek Çubuğu: 20 μm).

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Figure 3. J2s of Meloidogyne javanica from lettuce a: anterior region of Sample No: 107, b: posterior region of
specimen 107 (Scale Bar: 20 μm).
Şekil 3. Maruldan elde edilen Meloidogyne javanica’ya ait J2s a: Örnek 107 anterior bölgesi, b: Örnek 107
posterior bölgesi (Ölçek Çubuğu: 20 μm).
Table 1. Morphometric measurements of J2s of Meloidogyne javanica obtained from lettuce plant roots
Çizelge 1. Marul bitkisi köklerinden elde edilen Meloidogyne javanica’ya ait J2s’lerin morfometrik ölçümleri
Diagnostic This Study This Study This Study Whitehead Özarslandan
Characters Sample 85 Sample 107 Sample 115 (1968) (2009)
416.93±19.14 428.97±17.94 431.33 ±13.01
Body length 387-459 408-454.4
(392.92-456.24) (401.30-450.00) (405.15-450.80)
15.32±0.76 15.89±0.37 15.66±0.49
Greatest body width
(14.07-16.86) (15.10-16.54) (14.46-16.54)
Body width at stylet 9.75±0.37 9.94±0.34 9.99±0.54
base (9.13-10.63) (9.11-10.50) (8.48-10.85)
Body width at the 9.80±0.52 9.93±0.45 10.17±0.52 (9.21-
anus (8.60-10.63) (9.00-10.73) 10.91)
15.66±0.42 15.54±0.38 15.42±0.37
Stylet length 9.4-11.4 11.20-14.40
(14.80-16.30) (15.01-16.19) (14.60-16.09)
2.98±0.36 2.78±0.37 2.93±0,41
DGO 4 3.2-4
(2.15-3.58) (2.04-3.37) (2,27-3.98)
52.14±2.05 54.22±1.57 53.66±2.10
Tail length 36-56 46.40-59.20
(48.39-56.28) (51.30-57.84) (49.63-57.22)
Excretory pore to 84.54±2.01 84.79±1.21 84.45±1.62
head end (81.71-89.79) (82.94-87.83) (81.55-87.45)
Body width at the 13.32±0.65 14.51±0.46 13.93±0.69
excretory pore (12.03 -14.38) (13.35-15.33) (12.57-15.13)
27.24±1.23 26.98±1.16 27.46±1.10
a 27.1-35.9 30.33
(24.92-30.38) (25.18-28.91) (25.36-29.27)
3.90±0.19 4.08±0.14 4.06±0.14
b
(3.63-4.21) (3.81-4.34) (3.80-4.34)
8.00±0.37 7.91±0.36 8.01±0.37
c 7.3-11.1 8.31
(7.39-8.81) (7.39-8.71) (7.39-8.72)
5.33±0.34 5.46±0.29 5.27±0.28
c’
(4.83-6.13) (5.02-5.97) (4.83-5.97)
Note: Note: All measurements are in µm Body length/Body width, b: Body length/ Intestine to the head end, c:
Body length/Tail length, c': Tail length/Body width at the anus) and in the form: mean ± s.d. (range) n: 25.

This study is the first record of M. javanica detected ground (yellowing, wilting, and stunting) and root
on lettuce in the Southern Marmara Region. Above- symptoms caused by M. javanica in the lettuce plant

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cause significant yield and quality losses in this plant. and concentration of nematodes and their eggs
For this reason, it is recommended to carry out more from soil and plant tissue. Proceedings of the
comprehensive studies in the future, in lettuce Helminthological Society of Washington, 22, 87–
growing areas to monitor and conduct control 89.
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rotation, use of resistant varieties, and solarization identification of Root-knot nematodes from
applications. Turkey. Journal of Nematology, 41(2), 128.
Eisenback, J. D., & Triantaphyllou, H. H. (1991).
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