Plant-parasitic nematodes (PPNs) are one of the major constraints to crop production, and especially in high-value vegetable and fruit crops, they can cause significant economic yield loss, estimated to be more than US$100 billion annually (Bernard et al., 2017). Chemical soil fumigants have been in use for more than a century now, and remain the standard practice in many crops, especially fruits and vegetables. Although many of the early fumigants have been banned, the ones that have managed to stay, such as 1,3-dichloropropene, metam, and chloropicrin, are still considered to be the most effective products for the control of PPNs (De Cal et al., 2005; Desaeger et al., 2017; Rosskopf et al., 2005). However, environmental and safety concerns are putting more and more pressure on these products. Also, the evidence is growing of their adverse effect on beneficial soil organisms and the rapid resurgence of soilborne pathogens, including PPNs, following fumigation (Dangi et al., 2017; Martin 2003; Mazzola et al., 2015; Raupach and Kloepper, 2000; Sánchez-Moreno et al., 2010; Watson et al., 2017). As limitations of chemical soil fumigants are becoming more apparent, there is a need to find new soil fumigation compounds that are safer for the soil ecosystem and the environment. In recent years, volatile compounds (VCs) emitted from plants and microorganisms have been increasingly studied as bio-fumigant candidates for the control of various soilborne pathogens, including PPNs. Effects of VCs on plants, and soilborne pathogens such as bacteria and fungi have been reviewed elsewhere (Kai et al., 2009, 2016; Schulz-Bohm et al., 2017). Here, we summarize the recent studies of VCs that focused on PPNs as well as the challenges and knowledge gaps that remain in the future application of VCs as potential bio-fumigants for nematode management in the field.
Volatile compounds (VCs) are typically small, lipophilic, odorous, and low molecular mass compounds that can be evaporated and diffused aboveground and belowground through gas- and water-filled pores in soil and rhizosphere environments (Effmert et al., 2012; Insam and Seewald, 2010; Vespermann et al., 2007). These VCs are considered as the products of secondary metabolisms in plants and microorganisms such as bacteria and fungi (Dudareva et al., 2013; Schulz-Bohm et al., 2017; Vivaldo et al., 2017). The emission of VCs from plants and microorganisms depends on various factors such as the growth stage, nutrient availability, temperature, oxygen availability, pH, and soil moisture content (Insam and Seewald, 2010). VCs are classified into different chemical classes such as alkenes, alcohols, ketones, benzenoids, pyrazines, sulfides, and terpenes which have either beneficial or harmful effects on other organisms (Schmidt et al., 2015; Vivaldo et al., 2017).
Plant VCs that are well-known as bio-fumigants for the control of PPNs are glucosinolates which emit isothiocyanates (ITCs) as VCs under the process of biodegradation. ITCs are also the active ingredient of chemical fumigants such as metam. Plants belonging to the families Brassicaceae, Capparaceae, and Caricaceae all produce glucosinolates, and many genera within these plant families have been studied for their nematicidal effects on PPNs (Kruger et al., 2013; Monfort et al., 2007) (Table 1). Following maceration and incorporation, glucosinolates will be hydrolyzed to release ITCs which have broad-spectrum biological activities, against many soilborne pathogens and PPNs (Matthiessen et al., 2004; Schroeder and MacGuidwin, 2010). Several studies have shown the potential of these plants to control PPNs such as
Overview of studies investigating the effect of plant volatile compounds on different plant-parasitic nematodes.
Volatile compound producers | Identified volatile compounds | Experiment conditions | Target plant-parasitic nematodes | References |
---|---|---|---|---|
Brassica | Glucosinolates and isothiocyanates | Field biofumigation |
|
Thierfelder and Friedt (1995), Potter et al. (1998), Lord et al. (2011) |
White mustard ( |
Methyl sulfide, dimethyl disulfide | Field biofumigation |
|
Wang et al. (2009) |
Brassica leaf | 2-propenyl glucosinolate | Field biofumigation |
|
Lord et al. (2011) |
|
Alcohols and esters and sulfur containing compounds (mainly isothiocyanates) | In vitro and greenhouse |
|
Barros et al. (2014) |
Camellia seed cake | 18 compounds were identified | In vitro |
|
Yang et al. (2015) |
|
(Z)-3-hexenyl acetate, (Z)-3-hexen-1-ol and erucin | In vitro |
|
Aissani et al. (2015) |
Cottonseed meal | 2-methyl-1-butanol, 3-methyl-1-butanol, phenyl-ethylalcohol, benzene-1-ethyl-4methoxy (p-ethylanisole), and 4-ethyl-1,2-dimethoxybenzene | In vitro and greenhouse |
|
Estupiñan-López et al. (2017) |
Castor bean cake | Phenol, 4-methylphenol, γ-decalactone, and skatole | In vitro and greenhouse |
|
Pedroso et al. (2019) |
Citronella ( |
Dimethyl disulfide and 3-pentanol | In vitro and greenhouse |
|
Silva et al. (2018), da Silva et al. (2019) |
Watercress ( |
26 and 12 compounds were identified. 1-octanol had strong nematicidal activity | In vitro and greenhouse |
|
Silva et al. (2020) |
Seeds of papaya fruit ( |
Vinyl acetate, phenylacetaldehyde and benzylacetonitrile | In vitro and greenhouse |
|
Gomes et al. (2020) |
|
Ascaridole and citronellal | In vitro and greenhouse |
|
de Freitas Silva et al. (2020) |
Recently, many other plant VCs have been shown to have potential for controlling PPNs. Dimethyl disulfide and 3-pentanol, selected from the broccoli volatilome, were able to reduce the mobility of
The VCs ascaridole and citronella, emitted from two medicinal plants citronella grass (
Several fungal VCs have been evaluated against PPNs, mostly
Overview of studies investigating the effect of fungal volatile compounds on different plant-parasitic nematodes.
Volatile compound producers | Identified volatile compounds | Experiment conditions | Target plant-parasitic nematodes | References |
---|---|---|---|---|
|
Unidentified | In vitro |
|
Riga et al. (2008) |
|
1β-vinylcyclopentane-1α,3α-diol, 6-pentyl-2H-pyran-2-one and 4-(2-hydroxyethyl) phenol | In vitro |
|
Yang et al. (2012) |
|
Dioctyl disulfide (2-propyldecan-1-ol or 1-(2-hydroxyethoxy) tridecane); caryophyllene; 4-methyl-2,6-di-tert-butylphenol; and acoradiene | In vitro and greenhouse |
|
Freire et al. (2012) |
|
Unidentified | In vitro |
|
Costa et al. (2015) |
Endophytic fungus |
3-methyl-1-butanol, (±)-2-methyl-1-butanol, 4-heptanone, and isoamyl acetate, | In vitro and greenhouse |
|
Liarzi et al. (2016) |
|
Alcohols, esters, terpenes, and ketones | In vitro and greenhouse |
|
Pimenta et al. (2017) |
|
More than 28 volatile organic compounds were identified. | In vitro and greenhouse |
|
Terra et al. (2017) |
|
2-methylbutyl acetate, 3-methylbutyl acetate, ethyl acetate, and 2-methylpropyl acetate | In vitro and greenhouse |
|
Terra et al. (2018) |
|
23 compounds belong to esters, alcohols, phenols, aldehydes, carboxylic acids and sesquiterpenes | In vitro and greenhouse |
|
Estupiñan-López et al. (2018) |
The VCs emitted from the endophytic fungus,
A wide diversity of bacterial VCs have been investigated for the suppression of plant pathogens (Audrain et al., 2015; Bennett et al., 2012). However, few studies focused on managing PPNs (Table 3). Gu et al. (2007) investigated VCs of 200 bacterial isolates affecting
Overview of studies investigating the effect of bacterial volatile compounds on different plant-parasitic nematodes.
Volatile compound producers | Identified volatile compounds | Experiment conditions | Target plant-parasitic nematodes | References |
---|---|---|---|---|
|
Terpineol, benzeneethanol, propanone, phenyl ethanone and nonane | In vitro |
|
Gu et al. (2007) |
|
Benzeneacetaldehyde, 2-nonanone, decanal, 2-undecanone and dimethyl disulphide,phenyl ethanone, nonane, phenol, 3,5-dimethoxytoluene, 2,3-dimethyl- butanedinitrile and 1-thenyl-4-methoxy- benzene | In vitro and greenhouse |
|
Huang et al. (2010) |
|
Unidentified | In vitro |
|
Costa et al. (2015) |
|
As 1-Undecene; Disulfide dimethyl; Pyrazine, methyl-Pyrazine, 2,5-dimethyl-; Isoamyl alcohol; Pyrazine,methyl-; Dimethyl trisulfide | In vitro |
|
Sheoran et al. (2015), Agisha et al. (2019) |
|
Acetophenone, S-methyl thiobutyrate, dimethyl disulfide, ethyl 3,3-dimethylacrylate, nonan-2 one, 1-methoxy-4-methylbenzene, and butyl isovalerate | In vitro |
|
Xu et al. (2015) |
|
Acetone, 2-heptanone, benzaldehyde, 2-nonanone, 2-nonanol, cyclopentasiloxane, decamethyl-, 11-dodecen-2-one, 2-decanone, 2-decanol, 4-acetylbenzoic acid, furfural acetone, 2-undecanone, Acetic acid, [bis[(trimethylsilyl)oxy]phosphinyl]-, trimethylsilyl ester, 2-undecanol | In vitro |
|
Cheng et al. (2017) |
|
Dimethyl disulfide, 1-undecene, 2- nonanone, 2-octanone, (Z)-hexen-1-ol acetate, 2-undecanone, and 1-(ethenyloxy)- octadecane. Of these, dimethyl disulfide, 2-nonanone, 2-octanone, (Z)-hexen-1-ol acetate, and 2-undecanone | In vitro |
|
Zhai et al. (2018) |
|
Unidentified | In vitro and greenhouse |
|
Bui et al. (2020) |
There is no standard procedure for testing the effects of VCs on PPNs in vitro. Each study has developed its own device where VCs were kept in closed conditions together with PPNs (two- or three-compartment petri dish, microtube in a vial, or microtube in a closed box). Each design has contributed a valuable test system to the ‘proof of concept’ of the potential use of VCs as bio-fumigants. However, the results might be different when VCs from one source are tested in different designs. Up to now, most of the studies used a two- or three-compartment petri dish for testing the microbial VCs in vitro (Kai et al., 2016). The advantages of this experimental design are simple, inexpensive, and separating the VC emitters and receivers. However, this design also created non-natural conditions that alternated the metabolisms of the tested microorganisms (Kai et al., 2016). For example, the high concentration of CO2 accumulation, 10 times higher than the ambient concentration (20°C, 84 μmol m−2s−1 light, 16 h/8 h light/darkness), was the most obvious observation in this design (Kai and Piechulla, 2009). Therefore, standardizing in vitro testing conditions to evaluate the efficacy of VCs is needed. Also, many of the studies did not look at the recovery of nematodes, where following the exposure of VCs, the PPNs are removed from the exposure of VCs and their recovery in the absence of VCs is observed. Also, whether the efficacy is due to an individual VC or a blend of VCs, is often not known.
It is also very important to establish whether VCs are phytotoxic or not. Many researchers have shown that VCs from different microorganisms can actually promote plant growth (Hung et al., 2013; Lee et al., 2014; Nieto-Jacobo et al., 2017; Park et al., 2015; Ryu et al., 2003; Tahir et al., 2017), whereas other studies have shown that VCs from various microorganisms can cause phytotoxicity (Blom et al., 2011; Hung et al., 2013; Lee et al., 2014; Vespermann et al., 2007; Wenke et al., 2012). Recently, Bui et al. (2019) indicated that bacterial VCs inhibited rice germination in vitro but not
Although VCs from plants and microorganisms may constitute a more sustainable approach and reduce the use of synthetic chemical pesticides, potential adverse effects of VCs on human health, the environment and the soil ecosystem also need to be addressed, as biological products are not by definition safer than chemical products. For instance, Bahlai et al. (2010) showed that organic approved insecticides in Canada (Superior 70 oil® (UAP) and Botanigard® (Laverlam)) had more adverse effects on natural enemies (Asian ladybeetle
The mechanisms of VC emission from microorganisms are not clearly understood yet, but some have suggested that VCs are waste products in the microbial lifecycle (Schulz-Bohm et al., 2017). Cheng et al. (2016) and Ossowicki et al. (2017) demonstrated that the production of VCs was triggered by the GaC-A/GaC-S two-component regulatory system in bacteria. New biotechnology techniques such as gene editing may help to better understand the mechanisms of VC emission, and potentially to manipulate microbes to more efficiently release beneficial VCs.
Microbial VCs have also been reported to induce plant resistance to pathogens (He et al., 2006; Huang et al., 2012; Kottb et al., 2015; Lee et al., 2012; Naznin et al., 2014; Park et al., 2013; Raza et al., 2016). In these studies, the mechanism of induced resistance by microbial VCs involves salicylic acid or jasmonic acid/ethylene signaling pathways, similar to the mechanisms of induced resistance by plant growth-promoting microbes in dicot and monocot plants (Balmer et al., 2013; Pieterse et al., 2014). Nonetheless, the exact mechanisms of VCs inducing plant resistance, or their nematicidal mode of action, against PPNs are still unknown. Cheng et al. (2017) suggested that VCs could kill PPNs by affecting the nervous system, surface coat, intestine, pharynx, or other tissues of PPNs. Likely, different VCs have different modes of action as well, and while certain VCs may be nematode-specific, other VCs like isothiocyanates (ITCs), which are produced by glucosinolate-containing plants, are identical to chemical fumigants like metam, and have a broad-spectrum biocidal activity, with a multi-site mode of action.
Currently, several VCs have been shown to be able to control PPNs in the laboratory and sometimes greenhouse conditions. However, field application of VCs is still in its infancy (Farag et al., 2013), and only a few studies have demonstrated success in applying VCs to induce plant resistance against bacterial pathogens and insects on cucumber and pepper under field conditions (Choi et al., 2014; Song and Ryu, 2013). Even if efficacy can be demonstrated in the field, many hurdles remain, not in the least the need to produce or synthesize commercial and cost-effective quantities of VCs. In addition, there will also be a need for technology and equipment to apply VCs, similar to the equipment that is currently used to apply chemical fumigants.
Evidence is growing that plant and microbial volatile compounds have potential as a more environmentally friendly and ecosystem sustainable alternative to chemical soil fumigants. An increasing number of VCs emitted from plants and microorganisms are studied and have shown nematicidal activity in in vitro and in greenhouse conditions. Field studies are still few and far between, and also the mechanisms of VC emission as well as their effects on host plants, plant-parasitic nematodes, the ecosystem, the environment, and human health are still not well-understood. While we do not claim to have covered all current knowledge, we hope that this review of VCs with regard to PPNs will help to stimulate more research into their use as a potential alternative source of soil fumigants.