# The carrot cyst nematode *Heterodera carotae*: a major plant-parasitic nematode requiring more investigation

Josselin Montarry, Marine Biget, Sylvain Chereau, Lionel Lebreton, Eric Grenier, Sylvain Fournet

► To cite this version:

Josselin Montarry, Marine Biget, Sylvain Chereau, Lionel Lebreton, Eric Grenier, et al.. The carrot cyst nematode *Heterodera carotae*: a major plant-parasitic nematode requiring more investigation. *Nematology*, 2024, 26, pp.1079-1089. 10.1163/15685411-bja10361. hal-04757687

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Review article

# The carrot cyst nematode *Heterodera carotae*: a major plant-parasitic nematode requiring more investigation

Josselin MONTARRY *, Marine BIGET, Sylvain CHEREAU, Lionel LEBRETON, Eric GRENIER and
Sylvain FOURNET

IGEPP, INRAE, L'Institut Agro, Université de Rennes, Domaine de la Motte, BP 35327, 35653 Le Rheu, France

ORCID iDs: Montarry: 0000-0002-6158-8464; Biget: 0000-0001-7967-4590; Chereau: 0000-0003-1898-7344;

Lebreton: 0000-0003-1759-5269; Grenier: 0000-0002-2260-1101; Fournet: 0009-0008-1232-3487

Received: 23 August 2014; revised: 27 September 2014

Accepted for publication: 30 September 2024; published online: 22 October 2024

**Summary** – The present study reviews the knowledge to date on the carrot cyst nematode *Heterodera carotae*, which has become the primary threat to the carrot sector following the withdrawal of the last chemical soil fumigants in Europe. A keyword co-occurrence network was used to structure this review into five research areas: i) biology and epidemiology of *H. carotae*; ii) molecular identification and phylogeny; iii) population genetics and genomics; iv) control methods and strategies; and v) root exudates and hatching stimulation. Our findings indicate that *H. carotae* is an under-studied plant-parasitic nematode species, with several identified alternative control methods that require further investigation.

**Keywords** – bibliographical analysis, CorTexT manager, *Daucus carota*, hatching, molecular identification, molecular phylogeny, non-chemical control.

The carrot cyst nematode, *Heterodera carotae* (Fig. 1A), was first described and named in England in 1950 by F.G.W. Jones (Jones, 1950a). It was then found in Scotland in 1970 (Osborne, 1971) before being reported across all European carrot-growing areas, including Denmark, France, Germany, Hungary, Italy, Ireland, The Netherlands, Portugal, Poland, Russia, Serbia, Slovenia, Slovakia, Sweden and Switzerland (Subbotin *et al.*, 2010). After its first report in Michigan, USA (Graney, 1985), its precise distribution in this state was described by Berney & Bird (1988, 1992) who found the nematode in 67.4% of the investigated fields. More recently, *H. carotae* was identified in the province of Ontario in Canada (Yu *et al.*, 2017), in an important Mexican carrot-producing area (Escobar-Avila *et al.*, 2018), in Algeria (Mehalaine *et al.*, 2020) and in South Africa (Subbotin *et al.*, 2010; Shubane *et al.*, 2021). The carrot cyst nematode is still not reported in Australia. Thus, this nematode is a serious threat to

Australia's vegetable industry and is classified as a notifiable plant pest in New South Wales.

In the fields, infestation by *H. carotae* results in irregular areas of stunted plants, characterised by small, abnormally developed and unmarketable carrots (Fig. 1B). Estimated carrot crop losses related to *H. carotae* damage ranged from 20 to 90% in Italy, the USA and Canada (Greco *et al.*, 1993; Koenning *et al.*, 1999; Yu *et al.*, 2017). In a glasshouse experiment, Escobar-Avila & Tovar-Soto (2020) demonstrated that carrot cyst nematodes could cause an average yield loss of 70% over a 10-month period in carrot cultivation.

To carry out this review, we performed a bibliographical analysis using the simple query "*Heterodera carotae*" in the Web of Science core collection (on July 11, 2024). This query led to 42 papers, which have all been checked for relevance. As the bibliographical analysis was only available from 1955 to 2024, we manually added

<footnote>* Corresponding author, e-mail: josselin.montarry@inrae.fr</footnote>
<figure><img src="image_3.png" /><figcaption>**Fig. 1.** Second-stage juvenile of *Heterodera carotae* (A) and the damage it causes on carrots (B).</figcaption></figure>

two papers published by F.G.W. Jones before 1955. With
only 44 papers since the first publication (Jones, 1950a),
i.e., fewer than one paper per year, this plant-parasitic
nematode can be considered as a poorly studied species.
For comparison, similar analyses on other cyst nematodes
resulted in 561, 943, 1086, 1086 and 2257 papers, using
the queries "*Heterodera avenae*", "*Globodera pallida*",
"*Globodera rostochiensis*", "*Heterodera schachtii*" and
"*Heterodera glycines*", respectively. This analysis even
reached 6388 papers using the query "*Meloidogyne in-
cognita*". While the relevance of the papers was only
checked for *H. carotae*, results obtained for the other
nematodes clearly showed that the carrot cyst nematode
has been understudied since its identification. However,
a temporal analysis (Fig. 2) suggested that the publication
dynamic on *H. carotae* is increasing as 15 of the 44 papers
were published since 2018.

Using titles and abstracts of the 44 papers, a term co-
occurrence analysis, performed using CorTexT Manager
(Breucker et al., 2016), identified five distinct fields of
research on *H. carotae*: i) biology and epidemiology; ii) molecular identification and phylogeny; iii) population genetics and genomics; iv) control methods and strategies; and v) root exudates and hatching stimulation (Fig. 3).
The present study aims to review the existing knowledge
published on these five different fields and to identify
priorities for further research.

Biology and epidemiology

*Heterodera carotae* cysts are light brown and lemon-
shaped with small vulval cones and contain from 50 to

300 eggs (Escobar-Avila *et al.*, 2018). From the first
observations, Jones (1950a) highlighted the presence of
a gelatinous egg sac (or egg mass) attached to the cyst
of *H. carotae* and showed that this egg sac is as large
as the cyst. Second-stage juveniles (J2) in the egg sac
hatch once soil moisture and temperature conditions are
suitable regardless of host presence, while J2 in the cyst
require host presence to hatch. Full descriptions and
morphometrics of *H. carotae* females, cysts, males and
juveniles are available in the literature (e.g., Subbotin *et
al.*, 2010).

As with other cyst nematodes, *H. carotae* enters plant
roots as a second-stage juvenile (J2) and establishes a
specialised feeding structure, the syncytium, which is a
severe nutrient sink for the plant. It uses anti-oxidant
enzymes to deal with the active oxygen species produced
by the plant during the interaction (Molinari & Miacola,
1997). The penetration of J2 into carrot roots induces the
growth of secondary roots, thus increasing the number
of potential infection sites for the nematode (Bossis &
Mugniéry, 1987). Once juveniles reach the adult stage,
males exit the roots in order to mate with females. After
mating, the females continue to feed from the syncytium.
When egg development is completed, females die and
form the cysts, which protect the eggs. To complete its
life cycle, *H. carotae* requires 510 day-degrees (Greco
& Brandonisio, 1986). Thus, this polyvoltine species
can achieve between two and four generations during a
carrot-growing season, depending on the local climatic
conditions (Greco & Brandonisio, 1986; Subbotin *et al.*,
2010; Shubane *et al.*, 2021).
<figure><img src="image_4.png" /><figcaption>**Fig. 2.** Distribution of the number (A) and the cumulative number (B) of papers in the corpus by year of publication.</figcaption></figure>

Greco & Brandonisio (1980) produced the relationship between the initial population density and the yield of carrots and estimated a tolerance limit at $T = 0.8$ eggs (ml soil)$^{-1}$. The yield losses in relation to initial densities of eggs were 10% at 4 eggs ml$^{-1}$, 20% at 8 eggs ml$^{-1}$, 40% at 16 eggs ml$^{-1}$, 70% at 32 eggs ml$^{-1}$, 90% at 64 eggs ml$^{-1}$ and 100% from 128 eggs ml$^{-1}$ and above.

Jones (1950b) showed that *H. carotae* has a very narrow host range as it only attacked cultivated and wild carrots (*Daucus carota*) among the 105 distinct plants tested. The 16 other Umbelliferae tested in the study, including *Pastinaca sativa* (parsnip), were found to be non-host plants for this nematode. The only other wild Umbelliferae reported to support the complete development of *H. carotae* were *Torilis leptophylla* (bristlefruit hedge parsley) (Mugniéry & Bossis, 1988) and *Daucus pulcherrimus* (Oriental Astrodaucus) (Winslow, 1954). From an evolutionary point of view, an interesting prospect would be to explore the wild component and to study the occurrence of *H. carotae* on wild *Daucus* species and the potential genetic relationship between *H. carotae* populations from wild and cultivated carrots.

## Molecular identification and phylogeny

*Heterodera carotae* belongs to the *Goettingiana* group, one of the nine groups in which the *Heterodera* species are distributed (Handoo & Subbotin, 2018). While the *Avenae*, *Humuli* and *Schachtii* groups have recently been revisited (Subbotin *et al.*, 2018, 2022, 2024), the *Goettingiana* group has not yet benefited from this update. However, two studies have proposed the addition of new species within this group: *H. persica* (Maafi *et al.*, 2006) and the new species recently described in China, *H. microulae* (Li *et al.*, 2020). Until now, the closest relatives of *H. carotae* are *H. urticae*, *H. cruciferae* and *H. goettingiana* (Sabo *et al.*, 2001; Subbotin & Skantar, 2018). For instance, a recent phylogenetic analysis grouped the *H. carotae* population identified in 2008 from the Tarlton area in South Africa together in a clade with *H. cruciferae* and *H. urticae* (Shubane *et al.*, 2021). In test carried out *in vitro*, *H. carotae*, *H. cruciferae* and *H. goettingiana* do not interbreed (Yeates, 1970).

Madani *et al.* (2004) produced a phylogenetic tree, based on the ITS-rDNA sequences, which showed a
<figure><img src="image_5.png" /><figcaption>**Fig. 3.** Network of the co-occurrence of terms. Considering only terms composed of two or three words (i.e., monograms forbidden) with a minimum frequency of two, a list of 200 terms was extracted from titles and abstracts of the 44 papers and then reduced to 153 terms through the exclusion of terms corresponding either to a nematode species name (e.g., *Heterodera carotae*), a locality (e.g., South Africa) or non-informative terms (e.g., aim of the work). This network was prepared using the network mapping tool on CorTexT Manager platform (https://www.cortex.net). Nodes represent terms; lines between nodes represent links that measure the mutual occurrence of the terms among papers. The five identified research fields are circled and numbered. An interactive version of this network is available online at https://retina.cortex.net/#/graph/?url=https%3A%2F%2Fassets.cortex.net%2Fdocs%2Fe95ab075c4f0ef84393b6a966bb5c571.</figcaption></figure>

strong homology between *H. carotae* and *H. cruciferae*. A diagnostic tool using conventional and real-time PCR has been developed specifically to recognise *H. carotae* based on a primer pair targeting the *COXI* gene sequence (i.e., the cytochrome oxidase subunit I of mito-

chondrial DNA), with a single J2 detection limit (Madani *et al.*, 2018). However, using the available molecular tools, Escobar-Avila *et al.* (2018) showed that it was not possible to differentiate *H. carotae* from *H. cruciferae*. Accordingly, Huston *et al.* (2022) showed that *COXI*
sequences enabled identification of the different *Heterodera* species except the *H. carotae/H. cruciferae* pair. As these two nematodes are morphologically identical, only a time-consuming host range test can distinguish them. To fill this significant diagnostic gap, Fouville *et al.* (2024) have developed two primer sets targeting specifically the two species and validated them through real-time PCR protocols (SYBR Green singleplex and TaqMan multiplex real-time PCR). These new diagnostic tools appear promising as they were successfully validated using a set of European populations, even if their reliability could be improved by using populations from other parts of the world.

## Population genetics and genomics

So far, the available molecular markers enabled exploration of the inter-species genetic relationship, but not the intra-specific genetic diversity. Recently, Gautier *et al.* (2019) have developed a set of 13 polymorphic microsatellite markers and used them to genotype several European populations of *H. carotae*. Their results revealed that these populations belong to two distinct genetic clusters, one located in the north of Europe and the second one located in the south of Europe. Esquibet *et al.* (2020) used these microsatellite markers to explore the genetic structure of *H. carotae* populations in a French carrot-growing area located in west Normandy and highlighted a strong gene flow among populations (with a maximum distance between fields of 120 km). The authors hypothesised that soil transport with agricultural machinery and leek seedlings was responsible for migration of *H. carotae* cysts among fields. These two studies (Gautier *et al.*, 2019; Esquibet *et al.*, 2020) also showed that, as for other cyst nematode species (e.g., Montarry *et al.*, 2015), *H. carotae* populations were characterised by a strong heterozygote deficit (i.e., $F_{IS} > 0$), which suggests consanguineous mating due to the low dispersal capability of J2 hatched from the same cyst.

In terms of genomics, Wram *et al.* (2022) recently provided the first draft genome of *H. carotae*, which was generated from short reads (Illumina HiSeq technology). This genome of 95 Mb was composed of 17 839 scaffolds and contained 17 212 predicted protein coding genes. However, an effort is still needed to produce a high-quality reference genome (i.e., with a reduced number of scaffolds and a high N50 value), using third generation sequencing technologies producing longer sequence reads, and also

RNAseq reads to help future annotation of this new cyst nematode genome.

## Control methods and strategies

Before the withdrawal of most pesticides, several studies have explored the efficiency of nematicides to control *H. carotae*. The efficacy of isazofos and benfuracarb was analysed in field trials in Italy (Greco *et al.*, 1986) and results showed that applications of isazofos gave yield increases, while benfuracarb was not effective against *H. carotae*. Under laboratory conditions, it was demonstrated that aldicarb and fenamiphos suppressed emergence and movement of *H. carotae* J2 (Greco & Elia, 2000). A survey published by Greco *et al.* (2019) highlighted the need for very effective chemical fumigation as part of an integrated pest management programme (IPM). Fritsch *et al.* (2014) and Curto *et al.* (2014) showed that dimethyl disulfide (DMDS) appeared to be a promising alternative to existing fumigants (e.g., 1,3-dichloropropene) to control *H. carotae*. However, the fumigants 1,3-dichloropropene and DMDS are now both banned in Europe for their use as fumigants on carrot crops.

Gasparic *et al.* (2022) reviewed the non-chemical methods available to control *H. carotae* populations. Among these methods, solarisation allows soil disinfection by increasing the soil temperature (up to 60°C). The best effect is achieved by placing transparent plastic sheets on moist and loose soil for 4-6 weeks during the warmest period of the year (D’Addobbo *et al.*, 2010a). This technique is particularly suitable in regions with high summer temperatures. Indeed, a former study conducted by Greco *et al.* (1998), analysing the effect of both the temperature and exposure time on the mortality of *H. carotae*, showed that solarisation could be an effective control method in warm and sunny countries but not in colder regions. Moreover, the authors showed that *H. carotae* was less affected than *H. schachtii* by heat stress. Indeed, a 24 h exposure time at 45°C was sufficient to obtain a 98.5% loss of viability for *H. schachtii*, whereas cysts of *H. carotae* required 60 h at the same temperature to reach the same result (Greco *et al.*, 1998).

Nematicidal plants may also play an important role as biofumigants in the sustainable control of phytoparasitic nematodes through the phytochemical compounds they secrete in the soil (D’Addabbo *et al.*, 2014). For example, Brassicaceae extracts – glucosinolates and related hydrolysis products, mainly isothiocyanates – have been shown to be toxic to the carrot cyst nematode in *in vitro*
experiments (Avato *et al.*, 2013). These toxic compounds have a broad spectrum of biocidal activity against bacteria, soil-borne pathogens, insects, nematodes and weed seeds (Lazzeri *et al.*, 2009; Caboni *et al.*, 2012). Therefore, soil biofumigation using Brassicaceae plant species could be a promising solution but needs to be investigated more because the efficacy of the isothiocyanates depends on the pH, the temperature and soil moisture (Buskov *et al.*, 2002). It has also been shown that soil amendments composed of *Medicago sativa* (alfalfa) pelleted meal, containing saponins, allowed both a decrease in *H. carotae* population density and an increase in carrot yield (D’Addabbo *et al.*, 2010b, 2011). Other plants could also be biofumigated; *Sorghum bicolor* (sorghum), which produce dhurrin, has been shown to be effective against root-knot nematodes (Djian-Caporalino *et al.*, 2019) and needs to be tested against *H. carotae*. The use of *Castanea sativa* (chestnut) tannin aqueous solutions, which have a nematicidal activity, could also be favourably considered for protection of carrot against *H. carotae* (Maistrello *et al.*, 2018).

Biocontrol solutions have also been explored. An example of an alternative product against parasitic nematodes is abamectin, an anthelmintic produced by the soil bacterium *Streptomyces avermitilis* (Khalil, 2013). This anthelmintic is already registered as an insecticide and nematicide. This product can be used as a seed treatment to protect early growth stage plants from nematodes and insects that attack the root system (Khalil, 2013). Abamectin has recently been shown to have nematicidal activity against *H. carotae* (Sasanelli *et al.*, 2020). This *in vitro* study reported more than 80% mortality rate when exposing the nematode to the highest abamectin tested dose (36 µg a.s. ml⁻¹) (Sasanelli *et al.*, 2020).

In their recent reviews, McDonald & Telfer (2019) and Gasparic *et al.* (2022) considered that crop rotation using non-host plants (i.e., any cultivated plant other than a carrot) combined with resistant host plants is the most promising long-term control measure for *H. carotae*. However, several carrot cultivars have been screened for resistance (e.g., Mugniéry & Bossis, 1985) but there is currently no commercial resistant cultivar. This reinforces the needs to search for resistant carrot cultivars and to combine the above-mentioned available alternative solutions – with partial and/or variable effects – in an integrated pest management strategy.

## Root exudates and hatching stimulation

The first studies describing the hatching process of *H. carotae* showed that J2 hatched after 2 months from eggs in newly-formed cysts, whereas J2 in egg sacs hatched promptly (Greco, 1981). Hatching is reportedly greater at 15-20°C, substantial at 5-10°C and negligible at 25°C (Greco & Brandonisio, 1986). The age of carrot plants affected the hatch and most juveniles emerged with root exudates from 5- to 7-week-old carrots (Greco *et al.*, 1982).

The strong dependence for hatch of *H. carotae* on root exudates from its host plant offers an opportunity to use this feature as a new control method. This had recently motivated Ngala *et al.* (2021) to test root exudates from 33 distinct plant species for their *in vitro* ability to induce hatching of *H. carotae*. Their results showed that only exudates from carrots were efficient. Under control conditions, carrot exudates, crude or diluted 2× in water, stimulated hatching of J2 from cysts placed at 10 and 20 cm soil depth (Ngala *et al.*, 2021). In addition, Gautier *et al.* (2021) showed that populations from both genetic clusters (four from *H. carotae* cluster 1 and four from cluster 2; Gautier *et al.*, 2019) exhibited a high level of hatching with carrot root exudates. Finally, Ngala *et al.* (2024) tested a ‘lure and starve’ or ‘suicide hatching’ strategy in field trials, based on stimulating hatching of J2 in the absence of their host plant. The results showed that after two applications, one in autumn followed by another one in spring, the decline of *H. carotae* density reached up to 54% in field plots drenched with carrot root exudates.

The application of host root exudates can reduce the population densities of *H. carotae*, but the required quantities of root exudates to treat large cropping areas is clearly the main technical and industrial challenge to solve. So, the next step would be the identification of the molecule(s) which is(are) exuded in the soil by carrots and stimulate *H. carotae* J2 hatching.

## Conclusion and prospects

Despite decades of research, *H. carotae* still remains a poorly known species, even though it is a major threat to carrot production all over the world. Found worldwide in cultivated areas, nothing is known about its presence in wild ecosystems and its evolutionary history. Its genetic and morphological proximity to *H. cruciferae* also raises questions even though their host ranges are radically different. Recently, the withdrawal of nematicides
(e.g., 1,3-dichloropropene) creates a favourable context for the development of more specific new control strategies, which require the acquisition of new specific knowledge and thus new research efforts. In this sense recent studies have provided valuable information on its biology, molecular identification, population genetics and alternative control methods. Among the various topics of interest regarding *H. carotae*, we first observed that the impact of climate change on the epidemiology and management of the carrot cyst nematode is poorly studied (only one among the 44 publications on *H. carotae*). Using a modelling approach, Colagiero & Ciancio (2011) showed that a mean daily temperature increase of 1.5°C or 2.0°C would cause an additional *H. carotae* generation during the cropping season. In addition to this important topic, we propose a list of actions that we consider to be priorities.

A first interesting prospect would be to explore the wild component and to study the genetic relationship, potential gene flow and life history traits between *H. carotae* populations from wild and cultivated carrots. Indeed, populations of crop pathogens have necessarily wild relative populations on wild host plants that may be considered as potential reservoirs of diversity. As an example, Gracianne *et al*. (2014) showed that *H. betae*, which was previously described as a crop species in the field in The Netherlands, was largely distributed from the south to the north of Europe on the wild sea beet *Beta maritima*. Thus, there is no reason for assuming that *H. carotae* is present only in the field. We have initiated investigation into this aspect by sampling soil in Brittany (France) under the wild species *Daucus carota* subsp. *gummifer*, and some samples contained cysts that morphologically resemble *H. carotae* cysts but which need now to be biologically and genetically characterised. These investigations would be extended to other wild *Daucus* and larger geographic areas in order to explore the co-evolution between *H. carotae* and the genus *Daucus* and to measure potential gene flow between both (wild and cultivated).

In terms of control methods, the control of pest populations is now quickly changing with the demand and the need for more agro-ecological environmentally-friendly methods. Plant-parasitic nematodes and *H. carotae* are no exception to this new direction, especially with the ban of the last nematicides with a wide target broad spectrum. Thus, pest management will no longer be based on a single solution but on several complementary solutions, each being less effective than the replaced solution but

together enabling a satisfactory control level. In the case of *H. carotae*, exploring alternative and more specific control methods as well as combining them in an integrated pest management (IPM) approach has become a matter of urgency. This means first to be sure of the identity of the target. It is therefore crucial to deploy the recently developed molecular tools (Fouville *et al.*, 2024) to allow carrot farmers to distinguish *H. carotae* from *H. cruciferae*. Second, IPM involves pursuing the development of a control strategy based on plant resistance, on the biofumigation (e.g., sorghums), on the stimulation of *H. carotae* hatching in the absence of the host plant, and on the use of soil antagonists.

Identifying organisms within the soil microbiota with direct regulatory capacities is also a promising avenue that can provide effective answers where high population densities of *H. carotae* occur. Current technology makes it possible to scan a large number of candidate bacteria and fungi in a relative short time. Two methods would then be available: using the identified and validated organism as a biocontrol agent by inoculating it into the soil, or managing the soil and the crop rotation in a way that allows natural enemies to play a role in managing nematode populations.

Discovering the molecules involved in the chemical dialogue established between the host plant and the nematode is obviously a challenge for developing new biocontrol strategies. To do so, one may rely on recent advances in LC- or GC-(HR)MS based metabolomics approaches to be compatible with the low concentrations expected in the analysed matrices (root exudates). Once identified, the molecule could be bio-sourced to ease its use in fields. The identification of the molecule(s) which is(are) exuded in the soil by carrots and stimulate(s) *H. carotae* hatching may also make it possible to understand the J2 hatching process better and to define more precisely the factors that play a role in this critical step in the *H. carotae* life cycle.

Within cyst nematodes, a notable feature of *H. carotae* is its parasitic hyper-specialisation, which makes it a biological model for research questions about the specialisation (as opposed to polyphagia) both from an evolutionary and functional point of view. Using an improved reference genome, comparative genomics approaches would be performed to compare *H. carotae* with *H. cruciferae*, which are genetically close with distinct size of host ranges, i.e., distinct level of specialisation.

To improve both our fundamental and applied knowledge of this plant-parasitic nematode, further research on
<figure><img src="image_6.png" /><figcaption>**Fig. 4.** Co-authorship network using the 44 papers. This network was prepared using the network mapping tool on CorTexT Manager platform (https://www.cortex.net).</figcaption></figure>

*H. carotae* is essential. However, it is equally important to enhance international collaborations among research teams. Indeed, a network based on the co-authorship of the 44 publications on *H. carotae* (Fig. 4) highlighted eight distinct groups of authors. While two of these groups involve authors from different institutions/countries, the other six are limited to national collaborations. More dynamic international partnerships are therefore crucial to define the best strategies to manage *H. carotae* populations in a sustainable and eco-friendly way.

## Acknowledgements

This work was supported by the French ANR project ECLODERA (ANR-21-ECOM-0003). We acknowledge Anne-Sophie Grenier (DipSO-INRAE) for introducing us to CorTexT Manager, and Emilie Robilliard (SILEBAN) for providing the picture of carrots.

## References used in the bibliographical analyses (n=44)

* Avato, P., D'Addabbo, T., Leonetti, P. & Argentieri, M.P. (2013). Nematicidal potential of Brassicaceae. *Phytochemistry* 12, 791-802. DOI: 10.1007/s11101-013-9303-7

* Berney, M.F. & Bird, G.W. (1988). Distribution of *Heterodera carotae* in Michigan. *Journal of Nematology* 20, 628.

* Berney, M.F. & Bird, G.W. (1992). Distribution of *Heterodera carotae* and *Meloidogyne hapla* in Michigan carrot production. *Journal of Nematology* 24, 776-778.

* Bossis, M. & Mugniéry, D. (1987). Variability within *Heterodera carotae* in the ability to stimulate production of secondary roots in carrots. *Nematologica* 33, 322-327. DOI: 10.1163/187529287X00452

* Colagiero, M. & Ciancio, A. (2011). Climate changes and nematodes: expected effects and perspectives for plant protection. *Redia-Giornale di Zoologia* 94, 113-118.

* Curto, G., Dongiovanni, C., Sasanelli, N., Santori, A. & Myrta, A. (2014). Efficacy of dimethyl disulfide (DMDS) in the control of the root-knot nematode *Meloidogyne incognita* and the cyst nematode *Heterodera carotae* on carrot in field condition in Italy. *Acta Horticulturae* 1044, 405-410. DOI: 10.17660/ActaHortic.2014.1044.55
D'Addabbo, T., Miccolis, V., Basile, M. & Candido, V. (2010a). Soil solarization and sustainable agriculture. *Sociology, Organic Farming, Climate Change and Soil Science* 3, 217-274. DOI: 10.1007/978-90-481-3333-8_9

D'Addabbo, T., Radicci, V., Avato, P. & Tava, A. (2010b). Use of pelleted *Medicago sativa* meal for the control of root-knot and cyst nematodes. *Acta Horticulturae* 883, 303-308. DOI: 10.17660/ActaHortic.2010.883.37

D'Addabbo, T., Carbonara, T., Leonetti, P., Radicci, V., Tava, A. & Avato, P. (2011). Control of plant parasitic nematodes with active saponins and biomass from *Medicago sativa*. *Phytochemistry Reviews* 10, 503-519. DOI: 10.1007/s11101-010-9180-2

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