Management of Cyst and Root Knot Nematodes: A Chemical Ecology

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Management of Cyst and Root Knot Nematodes: A Chemical Ecology Perspective Baldwyn Torto, Laura Cortada-Gonzalez, Lucy K Murungi, Solveig Haukeland, and Danny Coyne J. Agric. Food Chem., Just Accepted Manuscript • DOI: 10.1021/acs.jafc.8b01940 • Publication Date (Web): 24 Jul 2018 Downloaded from http://pubs.acs.org on July 24, 2018

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Journal of Agricultural and Food Chemistry

Management of Cyst and Root Knot Nematodes: A Chemical Ecology Perspective

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Baldwyn Torto,*,† Laura Cortada,‡ Lucy K. Murungi, § Solveig Haukeland,†and Danny L. Coyne§

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†

International Centre of Insect Physiology and Ecology (icipe), P.O. Box 30772-00100, Nairobi, Kenya

‡

International Institute of Tropical Agriculture (IITA), P.O. Box 30772-00100, Nairobi, Kenya §

Department of Horticulture, Jomo Kenyatta University of Agriculture and Technology (JKUAT), P.O. Box 62000-00200, Nairobi, Kenya

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AUTHOR INFORMATION

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*Corresponding author (Tel: +254-20-2000; Fax: +254-20-2001: E-mail: [email protected])

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1 ACS Paragon Plus Environment


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ABSTRACT

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Plant parasitic nematode infection of crops can be highly detrimental to agricultural production.

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Since the discovery that plant roots release chemicals that attract the infective stage of plant

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parasitic nematodes some 80 years ago, significant progress in identifying the signaling

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molecules has occurred only relatively recently. Here, we review the literature on chemical

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ecological studies of two major plant parasitic nematode groups: Root Knot Nematodes in the

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genus Meloidogyne and cyst nematodes in the genus Globodera because of the negative impact

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their parasitism has on farming systems in Africa. We then highlight perspectives for future

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directions for their management.

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KEYWORDS: Globodera spp., Meloidogyne spp., semiochemicals, solanoeclepin A, volatile

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organic compounds.


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INTRODUCTION

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Plant parasitic nematodes constitute some of the greatest threats to crop production. The two

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most important groups of plant parasitic nematodes are Root Knot Nematodes (RKNs)

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(Meloidogyne spp.) and Cyst nematodes (Globodera and Heterodera spp.). Virtually every

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cultivated crop is prone to RKN attack, with Meloidogyne incognita, being the most important

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crop pathogen globally.

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juvenile stages (J1), (J2) the infective stage, (J3), (J4) and adult stages. However, cyst nematodes

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tend to be much more host specific and require host stimulus for egg hatching. The J2 of RKN

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and cyst nematodes react to stimuli from suitable host roots to attract and guide them to their

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food source.

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Previous work has shown that with increased human mobility, the accidental introduction of

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alien species to new environments will occur, as witnessed with the recent report of potato cyst

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nematode (PCN) in Kenya.2 Global warming will also likely facilitate the further distribution of

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tropical RKN and cyst species to regions where they are currently not present, as shown by the

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spread of the tropical RKN species M incognita, M. javanica, and M. arenaria, which were

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observed among the most rapidly spreading pests globally. 3 Given that many of the nematicides

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formerly relied upon to manage plant parasitic nematodes have been withdrawn from the market

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due to environmental concerns,

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environmentally sensitive tools to effectively control RKN and cyst nematodes. In this regard,

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understanding and exploiting knowledge of the chemical ecology of RKN and cyst nematode and

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their interactions with crops for their management is critical.

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Cyst nematodes have a similar biology to RKNs with a distinct egg,

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there is even greater pressure to identify suitable and

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ADVANCES IN CHEMICAL ECOLOGY OF ROOT KNOT AND CYST NEMATODES

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Chemical ecology is the study of the role of natural chemical interactions between organisms of

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the same or different species. The mediating chemicals are commonly referred to as

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“semiochemicals” (message-bearing chemicals). Semiochemicals are low to medium molecular

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weight volatile and non-volatile organic compounds synthesized from various pathways and can

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be exploited for the management of pests including plant parasitic nematodes. During the

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previous half a century or so, we have witnessed the rapid development and sensitivity in

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chemical instrumentation, resulting in the discovery of a broad range of semiochemicals from a

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wide range of above- and below-ground (rhizosphere) interactions. Comparatively, most of the

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discoveries on semiochemicals have been made from above- as opposed to below-ground

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interactions because of the complexity of the interactions in the rhizosphere (Figure 1). To

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improve our knowledge on below-ground interactions, better techniques are needed to collect

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and identify the molecules, especially volatile organic compounds (VOCs).

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Chemo-ecological studies are typically driven by simple, reliable and reproducible behavioral

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assays. For plant parasitic nematode-host plant interactions two main types of behavioral assays

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are recognized: stylet thrusting and chemotaxis. In the stylet thrusting assay, measurements are

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made on the rate at which the nematode thrusts its stylet (microscopic spear-like structure) into a

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chemical stimulus obtained from the host root. Stylet thrusting has been successfully recorded in

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both water and Pluronic gel formulations (a synthetic block copolymer),

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nematode can move around freely in various liquid media and at the same time thrust its stylet to

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detect chemical stimuli. More recently, it was shown that electrophysiological recordings of the

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stylet can be made,

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breakthroughs to identifying semiochemicals associated with insect olfaction are applicable to

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suggesting that the

demonstrating that some of the techniques that have provided


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plant parasitic nematodes. However, current electrophysiological techniques developed for plant

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parasitic nematodes are yet to be optimized to isolate physiologically-active compounds.

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Although stylet thrusting indicates detection of a chemical stimulus, using this technique does

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not allow for full classification of the chemical stimulus as an attractant (stimulant) or repellent

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(deterrent).

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chemical stimuli) assays, allows for a full description of the stimulus as an attractant or repellent.

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Previously chemotaxis assays were screened in 1% agar discs,

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sand-filled dual choice olfactometer 11-15 have allowed for testing nematode directional responses

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to intact plant root secretions, extracts and synthetic compounds identified from these root

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secretions.

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Another reason why studies on below-ground interactions lag above-ground interactions is the

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complexity involved in collecting and identifying the mediating molecules from the roots in the

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sand. To collect volatile organic compounds emitted by plant roots, inert polymer adsorbents

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including solid phase microextraction (SPME) fibers, Super Q, Porapak Q, HayeSepQ, which

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have been used previously to collect odors for various interactions (e.g. plant-plant, plant-insect,

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insect-insect, plant-microbe) are used in various sampling techniques. For example, some

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researchers have used SPME fibers to collect volatiles from excised plant roots crushed at very

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low temperatures such as in liquid nitrogen.

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material crushed at even low temperatures can lead to production of artefacts in the volatile

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emissions associated with mechanical damage. Using such methods would need to be backed by

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direct sampling of the root emitted volatiles into the sand. Our research shows that pulling air

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from the sand through SPME fibers enclosed in glass tubes collects predominantly sand-

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associated volatiles. To overcome the masking of root volatiles with sand-associated volatiles,

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On the other hand, using chemotaxis (directional responses of nematodes to

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8-10

but recent successes using

The disadvantage of this method is that tissue



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other researchers have successfully developed and used a direct sampling method for roots in the

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field or for uprooted plants in the laboratory using a probe inserted directly into the sand. Air is

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then pulled through the probe and then an adsorbent attached at the end of the probe. 12,14,15 The

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advantage of this method is that it allows for comparison of laboratory-collected volatiles from

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uprooted plants and field roots to eliminate artefacts associated with uprooted plants. It also

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allows for continuous sampling of root volatiles.

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Analysis of root secretions mainly consists of two approaches depending upon whether the target

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secretion is VOCs or non-volatiles. The most common method used for the analysis of VOCs is

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coupled gas chromatography-mass spectrometry (GC-MS). The second approach is analysis of

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non-volatile compounds by coupled high performance liquid chromatography-time of flight mass

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spectrometry (LC-QTOF-MS). In the analysis by GC-MS, some researchers have argued that

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solvent extracted volatiles from inert adsorbents do not reflect the complete natural volatile

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profile since low molecular weight compounds (C-2 to C-4 derivatives) such as acetaldehyde,

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ethyl acetate, propanal and butanal may not be captured in the adsorbed volatiles. An alternative

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approach suggested is sampling on an adsorbent such as Tenax TA which can be thermally

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desorbed in the GC-MS system. Although thermal desorption is less complicated, it has the

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disadvantage of degrading sensitive samples.

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combined with these analytical methods, have revealed that parasitic nematode chemical ecology

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is dependent on several factors including nematode species, root part (zone of elongation of

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growing roots), plant species, pH, concentration of chemical in the root exudate and interactions

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with other rhizosphere organisms especially microbes. In the following sections, we will provide

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highlights on chemical ecological studies of two of the most important plant parasitic nematode

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groups; RKN in the genus Meloidogyne and cyst nematodes in the genus Globodera because of

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However, using specific behavioral assays


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the detrimental impact of their parasitism on agricultural productivity, and then highlight

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perspectives for future directions.

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Chemical ecology of Meloidogyne spp.-Host Plant Interactions

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In nematode-plant interactions, the discovery that chemicals associated with plant roots attracted

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infective stage juveniles of parasitic nematodes was first made in 1939.

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experiments carried out after this discovery occurred almost two decades later, focusing on

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excised plant roots and interactions with infective juvenile stages of various parasitic nematode

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species from the genus Meloidogyne.

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understanding of nematode-plant interactions, they failed to identify the signaling molecules

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mediating interactions. Since then, several signaling molecules have been identified to show that

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Meloidogyne-host plant interactions are complex, involving diverse molecules derived from

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different chemical classes. Some of these chemicals may serve as long- or short-range signaling

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molecules depending upon their volatility, interaction with sand particles (adsorption and

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desorption) polarity and solubility in water. The simplest chemical identified is carbon dioxide,

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considered a long-range attractant,18 perhaps because previous work demonstrated that parasitic

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nematodes congregated around anaerobic surfaces associated with release of carbon dioxide.

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However, carbon dioxide is considered a non-specific signal because of the wide range of

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sources (decomposing plant, metabolism of root mutualistic microbes etc.) that emit it in the

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rhizosphere and which when in solution can lead to acidic gradients that attract or repel parasitic

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nematodes.

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attraction of M. hapla to acidic gradients ranging between pH of 4.5 and 5.4 formed by acetic

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acids, 5 suggesting that knowledge of the salinity of the medium in which the root is developing

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is critical to an understanding of Meloidogyne responses to root secretions. Evidently, the

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18,19

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Subsequent

Although these follow up studies improved our

Assays carried out in a 23% aqueous solution of Pluronic gel confirmed the



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complexity of the interactions with host plant roots found by other researchers and in our group,

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is because of the responsiveness shown by different Meloidogyne species to a wide range of

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volatile and non-volatile organic compounds, including phytohormones, terpenoids, esters and

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phenols.

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was shown to modulate the attractiveness of host roots to M. hapla.

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the ethylene-signaling pathway directly affecting root length did not appear to be responsible for

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modulating root attractiveness; instead other unidentified components of downstream signaling

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modulated the responses of M. hapla.

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Recently, it has been shown that small lipophilic molecules extracted in tomato (Solanum

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lycopersicum) and rice (Oryza sativa) root exudates had a nematotoxic or nematostatic effect on

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M. incognita and M. graminicola.

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downstream signaling components is yet to be established. More recent studies have shown that

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M. incognita is attracted to volatile organic compounds released by roots of different cultivars of

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the solanaceous plant pepper (Capsicum annum) (Table 1), such as methyl salicylate, α-pinene,

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limonene, and tridecane,

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salicylate was the most potent attractant in the blend of compounds identified. This study also

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showed that the host finding process in M. incognita can be disrupted by thymol, released in the

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VOCs of the root of another cultivar of pepper.

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process of developing novel eco-friendly strategies for control of M. incognita via plant

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breeding, whereby specific molecular pathways for suppressing root production of methyl

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salicylate or incorporating genes responsible for thymol production in the roots of pepper can be

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explored to protect pepper from RKN infection. Similar studies in our laboratory have

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To illustrate this complexity, the signaling pathway of the phytohormone ethylene

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21

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However, components of

Whether these small lipophilic molecules constitute

with subtractive assays demonstrating that the aromatic ester methyl

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These findings mark a significant step in the


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demonstrated the importance of plant species in altering RKN responses to root VOCs using

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tomato and spinach, (Spinacea oleracea; Amaranthaceae) (Table 1). 22

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A recent study showed that tomato root-secreted non-volatiles including phenol 2, 6-di-tert-

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butyl-p-cresol, and esters L-ascorbyl 2, 6-dipalmitate, dibutyl phthalate and dimethyl phthalate

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influenced the behavior of J2s differentially. 23 Among these compounds, only dibutyl phthalate

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repelled J2s. These compounds may be artefacts because they are typical contaminants detected

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in samples analyzed by GC-MS.

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Chemical Ecology of Cyst Nematode- Host Plant Interactions

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Potato cyst nematodes (PCN), comprising two species of Globodera (G. pallida and G.

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rostochiensis) represent quarantine pests in over 100 countries 24 and are considered the primary

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potato pests globally. Cysts of PCN may contain ~500-700 eggs and can persist in the soil for

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more than 20 years, withstanding extreme temperatures (-15 ˚C) and/or prolonged desiccation. 25

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The reactivation of eggs within the cysts is triggered by the presence of a suitable host crop,

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primarily potato (Solanum tuberosum) but also to a lesser extent other Solanaceae species such

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as tomato (Solanum lycopersicum), eggplant (Solanum melongena), or Capsicum spp.

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Root secretions from several plant species have been identified as the triggering factors for the

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hatching of diverse cyst nematode species. Some of these root effectors are responsible for

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prompting changes in the permeability of the PCN three-layer egg's membrane. For instance,

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calcium ions which diffuse into the soil activate osmotic changes in the membrane to release

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trehalose. This allows water to be absorbed through the egg's membrane to hydrate it, which in

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turn ceases the diapause in the cyst, leading to hatching and emergence of metabolically active

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J2s. The J2s then locate their hosts by detection of root secretions including volatile organic 9 ACS Paragon Plus Environment


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compounds. 26 Interestingly, several root secreted metabolites have been identified as stimulating

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PCN hatching, but solanoeclepin A, a tetranortriterpene derived from gonanane 27 present in the

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root exudates of potato and tomato roots is the most studied. 28 It shows nanomolar activity as a

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PCN-hatching factor, indicating the sensitivity of the hatching process in response to the

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appropriate chemical stimulus. Related studies have also identified hatching factors including

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glycinoeclepin A in soybean (Glycine max) and kidney bean (Phaseolus vulgaris), as well as

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glycinoeclepin B and C in the latter species, for the soybean cyst nematode Heterodera glycines.

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common biosynthetic origin

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oxygenated, and will bind to water molecules, low concentrations of them can be absorbed

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through the egg's membrane to trigger hatching. Because plant roots also release volatile organic

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compounds, their role in PCN J2 host location requires investigation.

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Additional molecules that play an important role in the plant-nematode recognition signaling are

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the hatching factor stimulants: their presence in the soil enhances and/or inhibits hatching

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through chemical interaction with the already existing root secretions available in the soil. The

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glycoalkaloids α-chaconine and α-solanine are both able to stimulate J2 hatching of Globodera

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spp. 31 ;the variable hatching stimulus of these two molecules 32 is linked to their concentration in

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the rhizosphere, which seems to vary with the age of the plant; for instance, α-solanine is present

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at higher concentrations in younger plants. Similarly, these two glycoalkaloids are also highly

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oxygenated, thereby potentially using a similar mechanism to that of solanoeclepin A,

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glycinoeclepin A, glycinoeclepin B and C to trigger hatching in PCNs. Hatching of cyst

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nematodes is triggered by highly specific root exudate cues, but it is additionally controlled by

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hatching inhibitors including proteases and protease inhibitors that have been identified from the

These three compounds stimulating hatching in cyst nematodes are triterpenoids sharing a 30

like solanoeclepin A. Structurally, because they are highly


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cyst wall. 33 These cyst inner inhibitors are influenced by the rhizosphere composition and appear

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in higher concentrations during unfavorable periods for cysts to be persistent in the soil until a

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suitable host crop is planted. 33,34 Such hatching inhibitors have been found in both the plant and

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cyst cuticles,

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mechanism that prevents cysts from hatching under suboptimal conditions. This points towards a

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strong adaptation by cyst nematodes to their hosts through the chemical-dialogue established at

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the rhizosphere level. 35

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While disruption of the diapause stage of PCN is highly dependent on the specific presence of

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host root secretions in the rhizosphere, some cyst nematode species, such as the soybean cyst

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nematode hatch more spontaneously. Therefore, use of its natural hatching effectors has been

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highlighted as a sustainable method to manage PCN in the absence of a suitable host. Over the

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years, these hatching factors (i.e. asparagusic acid) have been proposed to be developed into

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nematicides. 33,36 However, the complexity in the structures of these molecules have precluded

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their large-scale synthetic production. Instead, less complex oxygenated synthetic hatching

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effectors have been developed, such as metavanadate and picrolonic acid, with the latter being

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effective only with G. rostochiensis.

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identified hatching factors, a strategy currently being explored to manage PCN is the disruption

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of the chemical signaling between the potato root secretions and the J2s.

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Recently, the use of dead-end trap crops to suppress PCN in soil has been attempted with varying

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degrees of success using Solanaceae plants, for example the sticky nightshade (Solanum

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sysimbriifolium).

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but are then unable to develop on the resistant plant thus acting as a dead-end trap crop. In a

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previous study,

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and therefore these have been identified as an additional nematode-resistance

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In the absence of a commercial product derived from the

Using trap crops, PCN are stimulated to hatch by nightshade root exudates

90 accessions of Solanaceae (non-tuber bearing) were screened for their 11 ACS Paragon Plus Environment


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hatching stimulatory effect on PCN as well as for resistance. All these Solanum species induced

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hatching of PCN and was highest for the S. nigrum complex. The hatching stimulatory effects of

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these solanaceous plants may be associated with similar class of compounds previously

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identified in the root exudates of tomato and potato. Sticky nightshade and two cultivars of S.

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nigrum induced high levels of hatching as well as providing resistance against PCN, and which

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were considered good candidates as trap crops. Interestingly, other researchers,

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demonstrated the effect and potential of some non-Solanaceae crops, such as lupine (Lupinus

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mutabilis (Fabaceae)) and Oxalis tuberosa (Oxalidaceae) as trap crops for PCN. As a result,

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lupine is used as a green manure crop by Bolivian potato farmers to mitigate against PCN attack.

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The underlying mechanisms leading to lupine to serve as a trap crop needs investigating.

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In Kenya, where PCN is a recent introduction, 2 on-going studies in our laboratory indicate that

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at least two species of the African indigenous vegetables (AIVs), African nightshade (Solanum

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scabrum and S. vilosum) act as potential trap crops. Our field studies show that after three

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seasons of planting these nightshade species the PCN population density declined by 80%. Given

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these findings, elucidation of the chemicals involved and degree of hatching they cause (vital for

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success as a dead-end trap crop), and level of resistance are necessary. Furthermore, the

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sequence of cropping, in terms of re-stimulation for PCN hatching, should also be studied. Thus,

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the importance of these nightshade species as nutritious food crops and for income (unlike S.

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sisymbriifolium, which is a weed) is an added value within such a cropping system for African

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smallholder farmers. Screening of other AIVs as trap crops for PCN management therefore

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provides potential value and may result in identifying better trap crops, as well as new hatching

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factors. Regarding the effects of potential non-solanaceous crops as trap crops or inhibitors of

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PCN hatching, much work remains on the chemical ecology and interactions with PCN.


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have

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The management of plant parasitic nematodes in bio-fumigated and amended soils is attributed

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to a combination of different mechanisms, such as: i) the enhancement of the production of

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nematicide chemical molecules at the rhizosphere level; ii) the increase/introduction of

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antagonist microorganisms in the soil; and/or iii) boosting of plant defense mechanisms. 40 Neem

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(Azadirachta indica) and several species from the Asteraceae family (Tagetes spp., Artemisia

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dracunculus, Chrysanthemum spp. Calendula spp. and Crotolaria spp.) have been successfully

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used to amend soils and decrease nematode populations due to their ability to release pre-existing

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nematicidal phytochemicals, mainly limonoids, sesquiterpene lactones and polythienyls

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(especially α-terthienyl) into the rhizosphere; a few of these species have been used

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commercially, although a high variability on the efficacy of the biofumigation process has been

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reported, depending on the plant species used or on the soil type. 40-42 Botanical species of the

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Brassicaceae family are rich in glucosinolates, which transform into isothiocyanates upon

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degradation of plant tissues and are also used for their nematicidal effects in biofumigation

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programs.

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potential management option for the control of PCN, RKN and other plant parasitic nematodes.

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42,44

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juncea), both in liquid and in gas phase, can successfully inhibit G. pallida hatching (50%

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decline) in vitro, although it was less successful under field conditions.

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mechanisms linked to PCN hatching inhibition being unclearly elucidated, it has been observed

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that 2-propenyl isothiocyanate triggers the expression of heat-shock proteins in the free living

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nematode Caenorhabditis elegans; the overexpression of such proteins has been linked to an

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acceleration of the metabolic activities of J1 within the egg and the subsequent depletion of their

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energetic reserves that leads to its death and/or prevents J2s from infecting its hosts. It has been

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The incorporation of Brassica species as green manures has been reported as a

Studies show that the precursors of 2-propenyl isothiocyanate excreted by mustard (Brassica


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Despite the


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proposed that soil micronutrient composition, specifically sulfur, could also have an impact on

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the efficiency of the metabolism of the glucosinolate production by Brassica species and should

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be further investigated. The degradation of soil organic acids into short-chain fatty acids under

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anoxic conditions has also been reported to have a suppressive effect on PCN. 46,47

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As shown in Figure 1, plant hormonal signaling pathway can also influence RKN and cyst

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nematode host finding. For instance, an active ethylene (ET) signaling pathway has been

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reported to repel M. hapla

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beet cyst nematode (Heterodera schachtii),

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ethylene were found to be more susceptible to the cyst nematodes. 49 For G. pallida, both volatile

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and non-volatile compounds have been reported to play a role in plant-nematode signaling: the

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water-soluble components combined with volatile cues elicit hatching and localization of the

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feeding site by J2s, 50 although the identity and proportion in each of these fractions contributing

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to bioactivity is yet to be determined.

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Some studies have demonstrated the involvement of plant hormonal signaling in PCN host plant

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interaction. For example, salicylic acid (SA)-deficient mutants were found to be more susceptible

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to the beet cyst nematode, H. schachtii, than non-mutants, suggesting that an intact salicylic (SA)

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pathway is required for the defense mechanisms of sugar beet.

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reported with tomato for jasmonic acid, which requires an intact signaling pathway to retain the

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Mi-1 mediated resistance response against RKN. These findings suggest that more studies are

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needed to elucidate the chemical ecology of the interactions between these plant parasitic

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nematodes and their host plants.

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FUTURE PERSPECTIVES

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and the soybean cyst nematode H. glycines but attracts the sugar 48

while Arabidopsis mutants over-expressing


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Similar findings have been

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What we know from the review of the chemical ecology of the two genera Meloidogyne and

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Globodera is that most studies have exclusively focused on their interaction with roots of crops,

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which is a binary system. However, crop roots typically have a close association with mutualistic

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rhizosphere microorganisms. Therefore, what we have yet to establish is how these mutualistic

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associations influence the chemical ecology of plant parasitic nematodes and how such

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knowledge can be exploited for RKN and cyst nematode management. The rhizosphere is

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characterized by a complexity of interactions (Figure 1); for instance, microbial root mutualists

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may influence plant fitness by altering the composition and concentration of secondary

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metabolites and nutrients. Similarly, plant chemistry may also influence microbial root mutualist

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fitness. For instance, a trap crop or bio-transformed crop may be effective against plant parasitic

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nematodes due to the secondary metabolites of the plant, or alternatively the composition of

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microbial root mutualists, or even both. As such, it would serve a useful exercise to identify

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beneficial microbial root mutualists for a specific crop or cropping system and investigate their

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influence on the chemical signaling in the rhizosphere, via studies such as microbe-microbe,

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microbe-plant, plant-plant, and microbe-plant-nematode interactions. Also, the interaction

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between microbial root mutualists and nematodes may influence, or even determine, the fitness

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of the nematode to locate host roots. Understanding the chemical communication of such

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microbe-nematode interactions may be critical to developing effective nematode management

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methods. Furthermore, studies on the effects that these interactions have on plant parasitic

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nematode natural enemies in the rhizosphere are also warranted. Understanding these

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interactions would provide opportunities for developing methods to enhance and exploit the use

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of natural enemies in nematode control.



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Since genetic pathways may drive these binary and tri-trophic interactions, some researchers

322

have investigated the expression of genes and demonstrated that certain genes are either up- or

323

down-regulated due to nematode infection in certain crops. These studies have also exclusively

324

focused on the binary system: nematode-plant interaction. Therefore, knowledge of the genes

325

that are expressed due to the microbial root mutualist associations and understanding how they

326

influence the chemical ecology of nematode-host interactions is required. Such knowledge can

327

be exploited for use in the biotransformation of crops to mitigate against nematode attack.

328

To conclude, sedentary RKN and cyst nematodes pose a serious threat to crop productivity

329

across the globe, but especially in the tropics and SSA.

330

chemical signaling between nematode pest and crop host roots for host recognition, host finding

331

and location there appears a whole gamut of potential avenues to explore for exploiting this

332

towards nematode pest management in small holder farming systems.

52

333

334

AUTHOR INFORMATION

335

ORCID

336

Baldwyn Torto: 0000-0002-5080-9903

337

Laura Cortada: 0000-0002-5953-3798

338

Lucy K. Murungi: 0000-0002-3917-7474

339

Solveig Haukeland: 0000-0003-0671-5798

340

Danny Coyne: 0000-0002-2030-6328


Given the apparent importance of

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341

342

Funding

343

We gratefully acknowledge the financial support for this research by the following organizations

344

and agencies: Swedish International Development Cooperation Agency (SIDA), UK's

345

Department for International Development (DFID); the Swiss Agency for Development and

346

Cooperation (SDC); the Austrian Development Agency (ADA); USAID; and the Kenyan

347

Government. The views expressed herein do not necessarily reflect the official opinion of the

348

donors.

349

REFERENCES for nematode control.

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Table 1. Compounds Identified in the Volatiles Emitted by Host Plant Roots of the Root Knot Nematode Meloidogyne incognita Compound

Source

α-pinene

pepper, tomato, spinach

camphene

tomato

β-pinene

tomato, spinach

δ-3-carene

tomato

6-methyl-5-hepten-2-one

tomato

myrcene

tomato

decane

pepper

limonene


(Z)-β-ocimene

pepper, tomato

p-cymene

pepper

undecane

pepper

camphor

pepper

sabinene

tomato

2-isopropyl-3-methoxypyrazine

tomato, spinach

2-methoxy-3-(1-methylpropyl)-pyrazine


dodecane

pepper

methyl salicylate

pepper, tomato

thymol

pepper

tridecane

pepper, tomato

tetradecane

pepper

geosmin

spinach

α-cedrene

tomato, spinach

β-cedrene

tomato, spinach



γ-himachalene

pepper

allo-aromadendrene

pepper

α-muurolene

pepper

4,5-di-epi-aristolochene

pepper

γ - gurjunene

pepper


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497


FIGURE CAPTIONS

498 499

Figure 1. Physico-chemical, physiological and microbiological factors influencing populations'

500

dynamics of plant parasitic nematodes at the rhizosphere level. Plant roots produce

501

semiochemical molecules (volatile and non-volatile) as defense cues to repel nematodes and

502

minimize root infestation (blue-dotted arrow-shaped icon). Conversely, some of these root

503

allelochemicals are used by plant parasitic nematodes as indicators of the presence of a suitable

504

host, and once these are detected they trigger a cascade of hatching mechanisms in the nematode

505

that end up in the releasing of infective juveniles into the soil to infest the plant root system (red

506

solid arrow-shaped icon); additionally, a few cyst nematodes species (i.e. PCN) can maximize

507

their chances of persisting in the soil until a suitable host is planted by reducing spontaneous

508

hatching through inner inhibiting hatching mechanisms (i.e. proteases and proteases inhibitors)

509

hosted in the cuticle of the cysts (green- dotted arrow-shaped icon). Population dynamics of root-

510

knot nematodes (RKN) and potato cyst nematodes (PCN) are further influenced by the presence

511

of microbiological control agents in the soil that act either as obligate parasites or as antagonist,

512

both with the ability of reducing the incidence of parasitic nematodes in the soil under adequate

513

environmental

conditions.



Figure 1


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TOC Graphic


Management of Cyst and Root Knot Nematodes: A Chemical Ecology

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