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Research
Drought Stress Impairs Communication Between
Solanum tuberosum (Solanales: Solanaceae) and
Subterranean Biological Control Agents
Mahnaz Hassani-Kakhki,
1
Javad Karimi,
1,4,
Fahim El Borai,
2,3
Nabil Killiny,
2
Mojtaba Hosseini,
1
Lukasz L. Stelinski,
2
and Larry Duncan
2
1
Biocontrol and Insect Pathology Laboratory, Department of Plant Protection, School of Agriculture, Ferdowsi University of
Mashhad, Azadi Square, Vakilabad Highway, Mashhad 9177948974, Iran,
2
Citrus Research and Education Center, University of
Florida, IFAS, 700 Experiment Station Road, Lake Alfred, FL 33850,
3
Plant Protection Department, Faculty of Agriculture Zagazig
University, Zagazig 44519, Egypt, and
4
Corresponding author, e-mail: jkb@um.ac.ir , javadkarimi10@gmail.com
Subject Editor: Chris Weldon
Received 24 May 2019; Editorial decision 30 August 2019
Abstract
The attraction of entomopathogenic nematodes (EPNs) to herbivore-injured plant roots has been documented
recently to be a common tritrophic interaction. Belowground tritrophic interactions are especially subject
to modulation by many abiotic factors including drought. In this study, complementary greenhouse experi-
ments were conducted to understand how drought stress might affect a potato plant’s impact on EPN be-
havior. In separate trials, the responses of the EPN Steinernema diaprepesi (Nguyen and Duncan) (Rhabditida:
Steinernematidae) to root herbivory by larvae of the weevil Diaprepes abbreviatus (Linnaeus) (Coleoptera:
Curculionidae), in well-watered and drought stressed potato plants, were measured using soil-matrix olfact-
ometers with two arms. The drought treatments were initiated in 30-d old plants. Drought-stressed potato
plants received water when potentiometers read approximately 20 kPa, while for well-watered plants, the
number was 8 kPa. Four weeks after initiating the treatments, 400 ml water was added to all pots, immedi-
ately before starting the experiments. The experiments revealed that S. diaprepesi infective juveniles (IJs) did
not migrate preferentially toward drought-stressed or well-watered plants when neither were subjected to
herbivory [t
(21)
= 1.13, P = 0.269]. However, plants with roots damaged by herbivory attracted more S. diaprepesi
IJs if they were well watered than if they were drought stressed [t
(24)
= 3.19, P = 0.004]. If both plants in the ol-
factometers were drought stressed, EPNs moved preferentially toward those with root herbivory than those
with undamaged roots [t
(23)
= 3.19, P = 0.004]. No difference was detected in gas chromatography profles
between droughted and well-watered plant roots subjected to herbivory [F
(24, 336)
= 0.68, P = 0.87]. GC ana-
lysis showed that three compounds, including 3-nonanone [t
(6)
= 4.83, P = 0.003], artemisyl ketone [t
(7)
= 6.21,
P = 0.000], and benzoic acid, 4-ethoxy-, ethyl ester [t
(7)
= −4.22, P = 0.004] were signifcantly higher in drought
stressed than control plant roots. These results indicate that potatoes, like other plants, can recruit EPNs in re-
sponse to root herbivory, and that drought stress dampens this tritrophic interaction where choice is involved.
Additional research that resolves the mechanisms of these interactions may provide insights to exploit EPNs
for crop protection.
Key words: entomopathogenic nematode, tritrophic interaction, herbivory, potato, drought
Entomopathogenic nematodes (EPNs) in two families,
Steinernematidae and Heterorhabditidae, are insect-specifc para-
sites that live in soil (Hazir et al. 2016). EPNs have been used in
classical and augmentation biological control programs to suppress
population density of pest insects in cryptic habitats in a variety of
agroecosystems (El-Borai et al. 2007, Denno et al. 2008). The in-
fective juvenile (IJ) stage of EPNs, the only free-living stage, relies on
endosymbiotic bacteria (Xenorhabdus spp. in steinernematid nema-
todes and Photorhabdus spp. in heterorhabditids) to kill their prey
after penetrating the insect’s body through natural openings or the
cuticle. The IJs release the bacteria into the insect’s hemocoel, re-
sulting in septicemia, with death of the insect usually in 24–48 h. The
nematodes utilize the cadaver to complete one to three generations.
Development stops at the IJ stage when host nutrients are depleted
Annals of the Entomological Society of America, 113(1), 2020, 23–29
doi: 10.1093/aesa/saz050
Advance Access Publication Date: 1 November 2019
Research
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