Tabary, Lou ¹ ; Navajas, Maria ² ; Tixier, Marie-Stéphane ³ and Navia, Denise ⁴

¹UMR CBGP Institut Agro Montpellier, INRAE, CIRAD, IRD, Univ. Montpellier, Montferrier sur Lez, France.
²UMR CBGP INRAE, CIRAD, IRD, Institut Agro Montpellier, Univ. Montpellier, Montferrier sur Lez, France.
³UMR CBGP Institut Agro Montpellier, INRAE, CIRAD, IRD, Univ. Montpellier, Montferrier sur Lez, France.
⁴✉ UMR CBGP INRAE, CIRAD, IRD, Institut Agro Montpellier, Univ. Montpellier, Montferrier sur Lez, France.

2024 - Volume: 64 Issue: 4 pages: 1232-1253

Original research

Keywords

Abstract

Introduction

Trichomes are modified plant epidermal cells, forming a hairlike protuberance (Glas et al. 2012; Chang et al. 2019). The shape, length and density of trichomes can vary among species, genotypes and plant organs (Glas et al. 2012; Rakha et al. 2017b). Found in approximately 30% of vascular plant species, trichomes serve as a first line of defense against herbivorous arthropods. However, they can also hinder natural enemies by affecting feeding, oviposition, host and prey accessibility and foraging behaviour of predators and parasitoids, potentially reducing the efficiency of biological control (Duffey et al. 1986; Cortesero et al. 2000; Kennedy 2003; Glas et al. 2012; Kaur and Kariyat 2020).This review focuses on the cultivated tomato (Solanum lycopersicum L, formerly Lycopersicum esculentum Miller) and on its wild relatives (Solanum spp.) due to (i) the economic significance of tomatoes crop, with global production reaching 189 million tons in 2021 (FAOSTAT 2022); (ii) decades of research on the defensive role of trichomes against herbivorous arthropods in solanaceous plants and (iii) the possibility for trichomes to impede the survival and effectiveness of natural enemies, potentially compromising biological control efforts.

In Solanaceae, trichomes are classified into two categories based on their shape and function: glandular trichomes (GT) and non-glandular trichomes (NGT). GTs have glandular cells at their tips that can release secondary metabolites including essential oils, toxic substances and sticky compounds, which can impact the viability and dispersal of arthropods on their plant (Southwood 1986; Cortesero et al. 2000; Kennedy 2003; Glas et al. 2012). NGTs do not release any secondary metabolite but may act as a physical barrier preventing arthropods from feeding and moving (Kariyat et al. 2018, 2019).

Many herbivorous arthropods are able to'bypass' these defenses on tomato plants becoming significant pests (Wakil et al. 2017). To mitigate the impact of pesticides on human health and the environment, it is essential to identify alternative solutions. While biological control is recognized as a promising strategy, its implementation in tomato crops remains particularly challenging due to the negative effects of trichomes on natural enemies, including parasitoids and predators (Kennedy et al. 2003). Numerous studies have examined the impact of tomato trichomes on phytophagous arthropods; however, few have explored their effects on biological control agents. Additionally, research on the complex tri-trophic interactions among tomato plants, arthropod pests and their natural enemies is limited, highlighting the need for further investigation into these interactions. A deeper understanging of the impact of tomato trichomes on both pests and biological control agents is required to enhance sustainable pest management strategies, including the development of new tomato varieties and the optimization of biological control programs. To support these advancements, this paper presents a reviews the effects of tomato trichomes on the development of pests, including phytophagous mites, and their natural enemies, with a particular focus on predatory mites. Additionally, current and future challenges are also discussed.

Overview of tomato pests and associated natural enemies influenced by tomato trichomes

The key tomato pests most extensively studied in relation to trichome types and densities are the whiteflies - Bemisia tabaci (Gennadius) and Trialeurodes vaporarorium (Westwood) (Maliepaard et al. 1995; Freitas et al. 2002), the tobacco hornworm Manduca sexta (L.) (Farrar and Kennedy 1987; Kariyat et al. 2017), the fruit worm Helicoverpa zea (Boddie) (Farrar and Kennedy 1987), the tomato leafminer Tuta absoluta Meyrick (Resende et al. 2006), several aphid species such as Macrosiphum euphorbiae (Thomas) and Aphis gossypii Glover (Musetti and Neal 1997; Verheggen et al. 2009) and phytophagous mites (Rakha et al. 2017a), especially the two-spotted spider mite (Tetranychus urticae Koch), the tomato spider mite (Tetranychus evansi Baker & Pritchard) (Acari, Tetranychidae) and the tomato russet mite [Aculops lycopersici (Tryon)] (Acari, Eriophyidae). The two-spotted spider mite is one of the most significant pests globally due to its ability to feed on a diverse range of host plants (Van Leeuwen et al. 2010). The tomato spider mite became an important tomato pest, notably in Africa since the end of the 20^th century (Navajas et al. 2013). The tomato russet mite is a minute pest that feeds on various Solanaceae species causing plant death. Its small size allows it to hide beneath trichomes, making it difficult to control and reducing the effectiveness of both pesticide sprays and natural enemies (Vervaet et al. 2021).

Several natural enemies are reported to be affected by tomato trichomes: Trichogramma spp. (Kayshyap et al. 1991), Tachinidae flies (Farrar et al. 1992), Coccinellidae (Heinz and Zalom 1996), lacewings (Simmons and Gurr 2004; Gassman and Hare 2005), predatory bugs (Barbour et al. 1993; Economou et al. 2006; Bottega et al. 2017), Syrphidae (Verheggen et al. 2009) and predatory mites especially those of the family Phytoseiidae (e.g. Cédola and Sanchez 2003; Seelmann et al. 2007; Paspati et al. 2021).

Tomato trichomes and plant resistance to arthropod herbivory

In cultivated tomato and its closest wild relatives [i.e. Solanum cheesmaniae (L. Riley) Fosberg, S. chilense (Dunal) Reiche, S. galapagense Darwin & Peralta, S. habrochaites Knapp & Spooner, S. peruvianum L., S. pimpinellifolium L.], trichomes have multicellular structures and have been classified into different functional types based on the number of cells, shape and presence of glandular cells at the tip (Luckwill 1943; Simmons and Gurr 2005). In 1943, Luckwill was the first to describe seven types of trichomes in Lycopersicum spp. (now Solanum spp.). As this classification was incomplete (i.e. S. pennellii Correll was missing) (Simmons and Gurr 2005), Channarayappa et al. (1992) and Glas et al. (2012) proposed a revision defining eight types of trichomes (Table I, Figure 1) with basically two main categories: (i) GTs corresponding to types I, IV, VI and VII, having'heads' with one or more glandular cells releasing exudates and (ii) NGTs corresponding to types II, III, V and VIII, with no glandular cells at the tip (Simmons and Gurr 2005). In cultivated tomato and its wild relatives, types and densities of trichomes vary among plant organs (Glas et al. 2012), species and cultivars (Rakha et al. 2017b), and even in relation to plant age or biotic factors (temperature, photoperiod) (Simmons and Gurr 2005).

Trichomes can have physical and chemical effects on herbivorous arthropods. Both GTs and NGTs can physically hinder the dispersal of phytophagous arthropods, while GTs release compounds that are either repellent or toxic to arthropods (see Table 2).

Physical effects

NGTs can restrict herbivore movement, however their effects have been insufficiently studied and the role of NGTs in plant resistance to arthropods requires further investigation (Bar and Shtein 2019; Karabourniotis et al. 2020). Kariyat et al. (2019) showed that the M. sexta mean mass was lower and development time longer when feeding on leaves of Solanum elaeagnifolium Cavanilles, having higher NGT densities compared to control treatment. Kariyat et al. (2017) observed that the NGTs of Solanum carolinense L. affect pre- and post-ingestion of M. sexta, by damaging the gut of caterpillars. Regarding mites, Oliveira et al. (2018) did not observe any negative effect of high densities of NGTs on several life parameters of T. urticae; while the preferred tomato variety was S. lycopersicum L. cv. Redenção which had the highest density of NGTs.

In contrast, GTs are the most extensively studied trichomes in terms of physical role in arthropod defense. On tomato, the GT types IV and VI are the most associated with pest resistance (Simmons and Gurr, 2005). Vosman et al. (2018) showed that all varieties resistant to several insects [T. vaporariorum, Myzus persicae (Sulzer), Frankliniella occidentalis (Pergande), Spodoptera exigua (Hubner)] possess GT types I and IV on their leaves, suggesting that they are essential for plant resistance (in agreement with Firdaus et al. 2013; Lucatti et al. 2013). Arthropods die by being trapped by sticky exudates of GTs, such as acyl-sugars (Duffey 1986; Cédola and Sánchez 2003; Glas et al. 2012). GTs of cultivated tomatoes and wild relatives also act as a physical barrier, which interfere with B. tabaci feeding, oviposition and survival (Channarayappa et al. 1992; Rakha et al. 2017b).

Similarly for mites, Van Haren et al. (1987) studied the ability of T. urticae to walk on tomato stems with high density of GTs type VI (S. lycopersicum cv.'Turbo') and showed that 55% of T. urticae were entrapped after a 2 hour period. When screening tomato genotypes for resistance to T. urticae, Keskin and Kumral (2015) showed that the tomato variety with the lowest mite damage had the highest density of type V NGTs and type VI GTs. Tabary et al. (2024) showed that types I and IV GTs on the petiole had the highest impact on the settlement and dispersal of T. urticae, when studying eight tomato and wild Solanum genotypes. In contrast with observations made of Tetranychus spp., trichomes do not act as a physical barrier to the movement and development of A. lycopersici. Because of its a small size, with a length of less than 200 µm and a width of 50 µm, and a worm-like body, it can move between the trichomes, thereby protecting it from predation (Sabelis and Bruin 1996; Vervaet et al. 2021).

Chemical effects

A significant body of research has focused on the chemical effects of GTs, particularly regarding the detrimental impact of compounds secreted from their tips. These compounds are associated with three plant resistance mechanisms: antixenosis, antibiosis and tolerance. Antixenosis (or'non-preference') corresponds to a repellent effect of the resistant plant compared to a susceptible one (Rakha et al. 2017b; Santamaria et al. 2020). Antibiosis affects life history parameters of arthropods (survival, development, fecundity, etc.) after plant feeding, resulting in lower fitness, survival rate, oviposition and development (Rakha et al. 2017b; Santamaria et al. 2020). Tolerance refers to the plant's ability to sustain high densities of arthropods without experiencing damaging effects (Santamaria et al. 2020).

GTs produce a large range of (i) non-volatile compounds such as acyl-sugars (Kroumova and Waner 2003) and protease inhibitors (Glas el al. 2012); and (ii) low volatile exudates such as phenylpropanoids (Gang et al. 2001), terpenoids (Gershenzon and Dudareva 2007), phenolics (Karabourniotis et al. 2020), methyl ketones (Fridman et al. 2005), and flavonoids (Treutter 2006). In tomatoes, each type of trichome produces different compounds depending on species, cultivar; plant age and type of organs (Glas et al. 2012; Rakha et al. 2017b). The most studied compounds are acyl sugars, methyl ketones and sesquiterpenes (terpenoids).

Acyl-sugars

Acyl-sugars are non-volatile secondary metabolites that contribute to physical (stickiness) and chemical plant defenses (Schilmiller et al. 2008; Glas et al. 2012; Rakha et al. 2017a). Different mixtures of acyl-sugars produced by tomato and their wild relatives can have detrimental effects on arthropods (McDowell et al. 2011; Lucatti et al. 2013). Positive correlations between acyl-sugars concentration and type IV trichomes on leaves have been observed by Alba et al. (2009) and Lucini et al. (2015). However, the same type of trichome may produce different type of exudate depending on plant species and cultivars (Rakha et al. 2017b). No relationship was found between GT type VI and acyl-sugars secretion in both cultivated and wild tomatoes (Fan et al. 2019). Several studies have demonstrated a relationship between type I and IV GTs, acyl-sugars and resistance to insect pests. According to Simmons and Gurr (2005), acyl-sugars have antixenosis effects on phytophagous insects. Dias et al. (2013) observed that high acyl-sugars concentrations (secreted by F2 generation obtained from crosses between S. lycopersicum cv.'Redenção' x S. pennellii'LA716') was associated to resistance to T. absoluta with a non-preference for oviposition (antixenosis) and the suppression of larval development (antibiosis). Similar observations were noted for B. tabaci, with a positive correlation between acyl-sugars secretions and non-preference for oviposition and suppression of larval development (Dias et al. 2016). Resende et al. (2009), studied the resistance of genotypes [crosses between S. lycopersicum cv'TOM 584' and S. pennellii (LA716)] to B. tabaci, and found that the lowest number of nymphs was observed on genotypes with high acyl sugar content. Lucatti et al. (2013), found that resistance to B. tabaci of S. galapagense accessions was correlated with high concentrations of acyl-sugars and densities of GT types I and IV. Kortbeek et al. (2021) showed that the density of GT types I and IV on leaves of a large number of cultivated tomato and wild species was a strong predictor for resistance to B. tabaci due to the production of acyl-sugars. Snyder et al. (1998) observed a lower oviposition and a reduced attractiveness of B. tabaci on S. habrochaites accessions with high densities of GTs type IV and also suggested that this might be due to acyl-sugars secretions. However, B. tabaci population growth was higher on tomato cultivars with pubescent leaves compared to hairless ones, attributed to higher oviposition rate of females (Heinz and Zalom 1995). This may be explained by the preference of B. tabaci to lay eggs at the base of leaf trichomes (Berlinger et al. 1986).

Acyl-sugars also have a negative impact on mites, particularly T. urticae, which has been the focus of extensive study. Saeidi et al. (2007) showed that density of GT type IV and resistance to mites increased with plant age. Alba et al. (2009), performing crosses between cultivated tomato and the wild species S. pimpinellifolium (TO-937), showed that a high density of GT type IV and high acyl-sugars content, both increase mortality of spider mites (antibiosis effect characterized by high mortality and reduced oviposition). Similar results were obtained by Rakha et al. (2017a), showing a positive correlation between resistance to T. urticae, density of GT type IV and acyl-sugars contents in S. galapagense, S. pimpinellifolium and S. cheesmaniae. In contrast, no clear link between GT type VI and resistance to T. urticae was observed, consisting with results of Good and Snyder (1988). Lucini et al. (2015) worked on different genotypes, including crosses between the cultivated tomato (cv. Redenção) with low acyl-sugars content and the wild genotype S. pennellii with high acyl-sugars content (LA-716). They showed that T. urticae preferred tomato genotypes with low acyl-sugars content, suggesting a non-preference resistance (antixenosis).

Methyl ketones

Methyl ketones are secondary metabolites mainly produced by GTs type VI. The 2-tridecanone (2-TD) and 2-undecanone have been associated with pest resistance in tomato (Williams et al. 1980; Farrar and Kennedy 1987; Lin et al. 1987; Chatzivasileiadis et al. 1999; Maluf et al. 2007; Ben-Israel et al. 2009). A positive correlation was observed between densities of GTs types IV and VI and the secretion of 2-TD (Aragão et al. 2000; Simmons and Gurr 2005; Ben-Israel et al. 2009). Among the three forms of glandular cells in GTs type VI, the spherical cells have been linked to a higher production of methyl ketones (Ben-Israel et al. 2009). Several studies showed that these two sticky compounds have negative effects on bollworms H. zea, tobacco hornworms M. sexta, potato aphids M. euphorbiae, cotton aphids A. gossypii, B. tabaci and T. vaporariorum (Williams et al. 1980; Maliepaard et al. 1995; Musetti and Neal 1997). By contrast, other studies have found no effect of the 2-undecanone on M. sexta (Farrar and Kennedy 1987 in Simmons and Gurr 2005). These apparently inconsistent observations might be due to different levels of methyl-ketones produced in type VI trichomes between and among Solanum spp. (Simmons and Gurr 2005) or different plant organs (concentrations of 2-TD being higher in stems trichomes) (Chatzivasileiadis et al. 1999).

Methyl ketones are also known to have deleterious effects on phytophagous mites. Chatzivalsileiadis and Sabelis (1997, 1998) showed that 2-TD and 2-undecanone are highly toxic to T. urticae, and suggested a bioaccumulation of 2-TD. Chatzivalsileiadis et al. (1999) showed that T. urticae reared on tomato accumulate 2-TD when foraging on the stems. On S. habrochaites var. hirsutum, they demonstrated that just one or two contacts of mites with GTs type VI cause 50% mortality (antibiosis). Four methyl ketones of S. habrochaites accession LA 407 (2-tridecanone, 2-undecanone, 2-dodecanone, 2-pentadecanone) revealed the presence of repellent and anti-fecundity effects on T. urticae (antibiosis and antixenosis) (Antonious and Snyder 2015). 2-TD and 2-undecanone produced by GTs are also toxic to A. lycopersici (Leite et al. 1999).

Sesquiterpenes

Sesquiterpenes are terpenoids considered to be the most diverse class of plant metabolites, with more than 50,000 known molecules (Vranová et al. 2012). Their roles are diverse, being primary metabolites involved in photosynthesis and respiration and secondary metabolites involved in plant-pathogen interactions playing a major role in plant defenses (Dudareva et al. 2006). Zingiberene (ZGB) is the most studied sesquiterpene for its role in pest resistance. Produced mostly by GTs types IV and VI in tomatoes, it has often been associated to high levels of arthropod resistance (Maluf et al. 2001; Kennedy 2003; Maluf et al. 2007; Schilmiller et al. 2009; Oliveira et al. 2018). Some studies, such as Carter et al. 2002 did not find a correlation between secretions of sesquiterpenes and GTs type IV, while others including Maluf et al. 2001, reported the opposite.

ZGB was particularly associated to resistance to B. tabaci and T. absoluta (Freitas et al. 2002; Azevedo et al. 2003) and Freitas et al. (2002) showed a reduced number of B. tabaci on plants with high ZGB concentrations. Bleeker et al. (2012) also observed a negative correlation between concentration of ZGB and fecundity of B. tabaci (antibiosis). Studies also showed negative effects of ZGB on feeding and oviposition of T. absoluta (Azevedo et al. 2003; Lima et al. 2015). Azevedo et al. (2003) studying the resistance to T. absoluta of five genotypes (F2 generation from crosses between S. lycopersicum cv.'TOM-556' and S. habrochaites var. hirsutum accession'PI127826'), observed lower leaflet lesion (feeding deterrence), percentage of leaflets attacked (oviposition) and overall plant damage on genotypes with higher ZGB content. Studying resistance to T. absoluta of F2 genotypes obtained after crossing S. lycopersicum cultivar'Redenção' x Solanum habrochaites var. hirsutum (`PI-127826'), Lima et al. (2015) observed that genotypes having high ZGB concentration in leaves presented lower oviposition compared to susceptible genotypes. Maluf et al. (2010) also observed higher resistance of T. absoluta in genotypes with high acyl-sugars and high ZGB content. Other sesquiterpenes are also toxic to arthropods such as for instance 7-epizingiberene which, associated to ZGB, decreased the fecundity of B. tabaci (antibiosis) (Bleeker et al. 2012).

Sesquiterpenes also negatively affect development and survival of spider mites and Maluf et al. (2001) found a positive correlation between GTs type IV, ZGB concentration and repellence to T. evansi (antixenosis). Oliveira et al. (2018) showed that genotypes with high ZGB concentration had high densities of GTs type IV and VI and were less preferred by T. urticae, suggesting an antibiosis effect. These results are consistent with findings from several other studies (e.g. Gonçalves et al. 2006) on T. evansi. In addition, Dawood and Snyder (2020) working on compounds (alcohol and epoxy alcohol of zingiberene) secreted by trichomes of wild tomatoes showed that the alcohols of ZGB were significantly more repellent to T. urticae than ZGB.

Utilizing trichome-associated chemical compounds in tomato breeding programs

Selection of genotypes with both high concentration of toxic compounds and high density of GTs types IV and VI may be significant for tomato breeding programs. Regarding the chemical compounds mentioned above, Zeist et al. (2019) noted that resistance exists in wild tomato species as highlighted in this review, but the mechanisms underlying this resistance remain to be better elucidated.

Tomato breeding programs for pest resistance have focused on the main chemical compounds secreted by tomato trichomes mentioned above (acyl-sugars, methyl ketones and sesquiterpenes). Most of these programs were based on crosses between tomato and closely related wild species - S. pimpinellifolium, S. pennellii, S. galapagense and S. habrochaites.

To create cultivars with high acyl-sugars contents, crosses were conducted between S. lycopersicum and S. pennellii (accession'LA-716') possessing high acyl-sugars contents (Zeist et al. 2019). After several backcrosses, the descendants were resistant to B. tabaci, T. absoluta, M. euphorbiae, F. occidentalis and T. urticae (Goffreda et al. 1988; Goffreda and Mutschler 1989; Maluf et al. 2010; Leckie et al. 2012, 2016; Baier et al. 2015; Lucini et al. 2015), resulting in the production of several tomato lines (Cornell tomato breeding program, USA e.g. CU071026 with five introgressions from LA-716). Crosses were also performed between cultivated tomato and S. galapagense, resulting in tomato resistant to B. tabaci (Firdaus et al. 2013). Alongside these studies, scientists have focused on understanding the genetic basis of of acyl-sugars secretion. Resende and Maluf (2002) suggested that secretion of acyl-sugars in LA-716 is attributable to monogenic resistance. In 2013, the Quantitative Trait Locus (QTL) Wf-1 was identified as being associated to the presence of GTs type IV and acyl-sugars production (Firdaus et al. 2013). Schilmiller et al. (2012) highlighted the role of the gene Solyc01g105580 (SlAT2), expressed in the single tip cells of GTs type IV, that encodes an acetyl-CoA-dependent acyltransferase enzyme. In vitro, RNAi suppression of this gene in S. lycopersicum cv. M82 resulted in a lower acyl-sugar acetylation. Finally, Andrade et al. (2017) worked on the genetic basis of high density of GTs type IV and identified two major-effect QTLs on S. galapagense accession LA-1401. Further information on acyl-sugar biosynthesis genes and acyl-sugar pathways could enhance future breeding programs aimed to integrate resistance to arthropod pests.

Methyl ketones have also been regarded as promising candidates for developing new varieties resistant to many phytophagous arthropods. High levels of 2-TD compounds are already considered an effective screening criterion in breeding programs devoted to develop resistant cultivars, especially derived from crosses between S. lycopersicum and S. habrochaites var. glabratum (Barbosa and Maluf 1996). However, the genetic basis of high 2-TD secretions seems to be complex and requires further investigation (Zeist et al. 2019). Indeed, Barbosa and Maluf (1996) demonstrated that, in crosses between S. lycopersicum x S. habrochaites var. glabratum, heritability does not fit into a simple additive-dominant model.

Crosses between S. lycopersicum and S. habrochaites var. hirsutum (accession PI-127826) were conducted to develop plants resistant to B. tabaci, T. absoluta and T. evansi (Freitas et al. 2002; Gonçalves et al. 2006; Lima et al. 2015). Furthermore, it was observed that ZGB appears to be controlled by two genes with incomplete dominance (Lima et al. 2015).

Impact of trichomes on biological control agents of tomato pests

Efficiency of natural enemies is influenced by tri-trophic interactions involving the prey and the host plant (Kennedy et al. 2003). Tomato trichomes will affect the behaviour and biology of natural enemies, both predators and parasitoids, directly (by influencing foraging activities, dispersal, development) and indirectly (through bioaccumulation resulting from feeding on preys containing toxic compounds) (Table 3).

Effects of trichomes on parasitoids

Tomato trichomes appear to reduce parasitoid movements and to affect their life-traits through physical and toxic effects, resulting in lower parasitism success, however studies on this topic are scarce. The walking speed of Trichogramma pretiosum Riley (Hymenoptera: Trichogrammatidae) was reduced on tomato cultivars with high densities of GTs type VI on leaves, and high levels of 2-tridecanone (Kayshyap et al. 1991). A higher mortality of Archytas marmoratus (Townsend) (Diptera, Tachinidae) was observed on leaves of S. habrochaites with high densities of GTs type VI, associated with a toxic effect of 2-TD (Farrar et al. 1992). On tomato plants with a high secretion of methyl-ketones, rates of parasitism of H. zea by A. marmoratus were lower compared to tomato plants without methyl-ketones (Farrar and Kennedy 1993). Mulatu et al. (2006) studied the impact of trichomes on the development and parasitism rate of Diadegma pulchripes (Kokujev) (Hymenoptera, Ichneumonidae), a parasitoid of the potato tuber moth Phthorimaea opercullella (Zeller) (Lepidoptera, Gelichiidae). These authors showed that the moth was not affected by the plant trichome density, but D. pulchripes failed to parasitize larvae on tomato leaves. Similar observations were made for Trichogramma spp., which exhibited lower parasitism rates of Heliothis spp. on tomato varieties with high density of GTs type VI (Kauffman and Kennedy 1989).

Effects of trichomes on predators

Physical effects

Studies generally emphasise that trichomes negatively impact the foraging behaviour and predator movements, of both insects and mites. Shah (1982) found that larvae of Adalia bipunctata L. (Coleoptera, Coccinellidae) had difficulty staying on the plant and fell off after an average of 20 minutes and also observed a lower foraging efficiency, with a higher percentage of unsuccessful attempts to capture prey. Likewise, the predator Delphastus catalinae (Horn) (Coleoptera, Coccinellidae) (previously named D. pusillus) exhibited a lower walking speed on tomato leaves with a high trichome density, compared to tomato leaves with low trichome density (Heinz and Zalom 1996). Coll et al. (1997) showed that Orius insidiosus (Say) (Heteroptera, Anthocoridae) had a greater foraging ability on leaves on bean and corn, which had a low total number of trichomes, compared to tomato plants, with high trichomes density. A high GTs type IV density can also increase the number of predators entrapped by trichomes on tomato leaves, as cited by Simmons and Gurr (2004) for Mallada signatus (Schneider) (Neuroptera, Chrysopidae). Nymphs of the two predatory bugs Macrolophus pygmaeus (Rambur) (Hemiptera, Miridae) and Orius niger (Wolff) (Heteroptera, Anthocoridae) also presented a reduced mobility on leaves of tomato varieties with high density of GTS type VI (Economou et al. 2006). Movement and predation rates of the predatory larvae of Episyrphus balteatus (De Geer) (Diptera, Syrphidae) were also lower on tomatoes with high density of trichomes on the stem compared to other plant species with lower trichome densities like bean and potato (Verheggen et al. 2009).

Unlike most predators, some Miridae predators have shown good adaptation to plants with high trichome densities. Walking behaviour and T. absoluta predation rates of Campyloneuropsis infumatus (Carvalho), Engytatus varians (Distant), and Macrolophus basicornis (Stal) was evaluated on two tomato lines with different densities of glandular trichomes - TOM 587 and TOM 687, the latter with exhibiting 179% greater glandular trichome density than the former (Bueno et al. 2019); and it was also observed that the three mirid species easily climbed the sticky stems of both tomato lines and eggs of T. absoluta were found on leaflets located on plant apex. Predation rates, grooming, probing, and feeding activities as well as the time spent until prey encounter were not influenced by trichomes density for none of the three mirids. The mirid is Dicyphus errans (Wolff) is known for being a trichome-well adapted species. Studies showed that this slim-body, long-slender leg and curved-claws omnivorous predator is not hindered in its movements on plants with high densities of trichomes, including the tomato cv. Grit. Voigt et al. (2007) demonstrated a positive relationship between the diameter and length of plant trichomes and attachment forces of this predator walking on the plant surface. Subsequently, Voigt (2019) showed that fecundity, hatching rate, juvenile development and consumption rate are positively correlated with the safety factor (attachment force/body weight).

Regarding the mechanical effects of trichomes on predatory mites, studies have primarily concentrated on Phytoseiidae. Tomato trichomes can hamper phytoseiids dispersal and thus prey consumption (Cédola and Sanchez 2003; Paspati et al. 2021). Conversely, plant trichomes may also provide benefits for these predatory mites: the hair-like structures may serve as a refuge from hyper-predators or abiotic constraints aiding in food detection (pollen and prey) (Seelmann et al. 2007). Entrapment of predatory mites on GTs (physical effect), was observed on several cultivated varieties and wild species of tomato. In 1987, Van Haren et al. showed that approximately 60% of Phytoseiulus persimilis Athias-Henriot (Acari, Phytoseiidae) were trapped on stem trichomes after a 2-hours observation period. On varieties without trichomes on stems, al predatory mites reached the next leaf in a short period in 2 to 15 minutes. Type VI trichomes on stems are the most important barrier for predatory mite dispersion (Luckwill 1943). Buitenhuis et al. (2014) observed that Amblyseius swirskii Athias-Henriot walked at a lower speed on tomato plants (S. lycopersicum var. Big Dena) with high density of trichomes compared to the other host plants tested (Gerbera jamesonii Bolus ex. Hooker var. Festival, Chrysanthemum x grandiflorum Ramat var. Chesapeake, Rosa kordesii Wulff var. William Baffin).

Lower predation and oviposition rates were also noted. Cédola et al. (2001) found that tomato trichomes limited the efficiency of the predatory mite Neoseiulus californicus (McGregor) to control T. urticae compared to other host plants and other phytoseiids such as P. persimilis on bean leaves (Everson 1979) or Neoseiulus cucumeris (Oudemans) to control F. occidentalis on cucumber and sweet pepper leaves (Shipp and Whitfield 1991). In their study on the efficacy of Phytoseiulus macropilis (Banks) and Phytoseiulus longipes Evans in controlling T. urticae on tomato plants, Sato et al. (2011) found that the density of trichomes on the plant surface negatively affected the performance of both predators. However, the webbing produced T. urticae provided a way for the predators to circumvent the detrimental effect of trichomes. Webbing could thus have physical effects by reducing contact between the predator and trichomes and providing a suitable oviposition site (Roda et al. 2001). However, when plants are covered with webbing, spider mite infestation is typically so high that predatory mites may not be effective enough to control the pest.

In addition to the phenotypic traits of tomato lines, such a type and density of glandular trichomes, biotic factors (temperature and relative humidity) can influence the phenology of trichomes and, consequently, their impact on predatory mites. High mortality rates of P. persimilis on tomato plants are observed in the spring and summer due to the entrapment by trichome exudate. Glasshouse experiments revealed that the rate of immobilization was positively correlated with rising temperatures (Nihoul 1994). This factor should therefore be considered when managing pest control in greenhouses.

Toxic effects on predators

Trichomes also negatively impact on fecundity and growth of several predators. Barbour et al. (1993) worked on the impact of trichomes on two predators of H. zea, Coleomegilla maculata (De Geer) (Coleoptera, Coccinellidae) and Geocoris punctipes (Say) (Hemiptera, Lygaeidae), and observed greater mortality of both predators in presence of GTs type VI on leaves due to methyl ketones. On tomato plants with a high density of trichomes, D. catalinae had a lower fecundity compared to those with a smaller number of trichomes (Heinz and Zalom 1996). Likewise, Bottega et al. (2017) observed that the survival, adult longevity, number of consumed prey and foraging behaviour of the stink bug Podisus nigrispinus (Dallas) (Heteroptera, Pentatomidae) were negatively affected by GTs types I and IV on leaves of tomato genotypes resistant to T. absoluta, limiting the potential success of biological control.

Trichomes also negatively impact on the survival and the life history traits of predatory mites, particularly due to the toxicity of the compounds secreted by GTs. In 2003, Cédola and Sánchez observed that tomato cultivars with a high density of trichomes negatively affected the survival of N. californicus. Paspati et al. (2021) observed that A. swirskii individuals preferred to remain on sweet pepper rather than on tomato. The same authors noted that acyl sugars accumulate on the mite's cuticle, joints and mouth parts hypothesizing that these sugars likely penetrate through the cuticle. The accumulation of toxic exudates in mites that come in contact with GTs merits further investigation, as it may help explain the unsuitability of many predators on tomato plants (see details below in'Importance of tri-trophic interactions on biological control agents').

Several studies demonstrated lower efficiency of predators on tomatoes with a high density of trichomes; however, the reasons for this reduced efficiency are not addressed in the publications. Barbour et al. (1993) showed that C. maculata exhibited reduced consumption of H. zea eggs in laboratory bioassays on the wild tomato Solanum hirsutum f. glabratum (accessions PI 134417) secreting methyl ketones in the apical area of GTs. Lower attack rates of T. absoluta by P. nigrispinus on tomato plants have also been observed compared to eggplant and, sweet pepper (De Clercq et al. 2000). According to the authors, these results may be attributed to the presence of GTs on tomato although this has not been tested. Simmons and Gurr (2004) observed a lower number of aphids predated by M. signata on tomato plants with high density of trichomes.

Importance of tri-trophic interactions for biological control agents

Predation efficiency can be influenced by the impact of herbivorous arthropods on the plant physiology. For instance, Van Houten et al. (2013) observed that in presence of A. lycopersici, GTs undergo discoloration after which they dry out and fall off. This damage allows Amblydromalus limonicus (Garman and McGregor) to successfully establish in the area where the trichomes had fallen off. However, the biological control was not effective, as pest populations remained very high and russet mites had dispersed, colonizing the entire plant.

Another important aspect is the indirect prey-mediated effects of tomato on predators and parasitoids. Savi et al. (2021) hypothesized that the lower predation rates and biological performance of P. longipes feeding on T. evansi in tomato cultivars with high GT densities could be due to the consumption by the predator of a prey that has accumulated a high concentration of toxic compounds such as methyl ketones. In 2007, Koller et al. observed that N. californicus had a longer developmental time and lower oviposition rate when feeding on T. evansi strains reared on tomato compared to a bean-reared strain. These results align with findings from other studies. Moraes and McMurtry (1987) observed that P. persimilis gained more weight when fed with T. urticae reared on bean compared to T. urticae reared on Solanum douglasii (nightshade). They hypothesized that an unknown factor, possibly in the hemolymph or tissues of the prey, might explain these results. Escudero and Ferragut (2005) observed a lower efficiency of P. persimilis and N. californicus when feeding on T. evansi reared on potato. They hypothesized that this may partially be due to toxic compounds consumed by T. evansi. Ferrero et al. (2014b) showed that two populations of P. longipes collected from solanaceous plants infested with T. evansi were able to develop when feeding on T. evansi on tomato, whereas this was not possible for a P. longipes strain found on non-solanaceous plants feeding on T. urticae. One hypothesis was that both direct and indirect effects of tomato might influence the feeding behaviour of P. longipes on tomato. Further studies are needed to investigate bioaccumulation of toxic compounds across different food chain levels to better understand their impact on the biology of natural enemies and, consequently, on biological control.

What would happen to herbivorous and predators if trichomes were removed from tomato plants? The effect of tomato mutant lines presenting distorted trichomes on aerial tissues (which disrupt the accumulation of sesquiterpene and polyphenolic compounds; see Kang et al. 2010b) on the performance of predatory mites – P. persimilis and A. limonicus – in controlling mite pests (T. urticae and A. lycopersici) has been evaluated. Legarrea et al. (2022) showed that predatory mites perform better and can reduce phytophagous mite densities more quickly on'hairless' tomato mutants than on cultivated tomatoes (cv. Ailsa Craig).

Perspectives on using predatory mites for the biocontrol of tomato pests

While the biological control of tomato pests presents a promising strategy, it remains challenging, particularly due to the detrimental effects of trichomes on natural enemies. For predatory mites, all the most commonly used species for the control of phytophagous mites and thrips - the phytoseiid mites P. persimilis, P. macropilis, N. californicus and A. swirskii - have showed to be negatively affected by tomato trichomes (Van Haren et al. 1987; Cédola and Sánchez 2003; Sato et al. 2011; Paspati et al. 2021). This has prompted efforts to identify alternative predatory mite species that might be better adapted to tomato. One of the strategies could be prospection for adapted species or wild populations on tomato, other solanaceous, or even other phenotypically similar host plants.

In the review by Tixier et al. (2020 a) on Phytoseiidae biodiversity on Solanaceae worldwide, 215 species of Phytoseiidae were reported on 99 species of Solanaceae, and authors indicate that the adaptation of Phytoseiidae to Solanaceae seems to be a recent occurrence, except in the Neotropical region. This may explain why many European phytoseiid species are not adapted to tomato. The Neotropical region has the highest number of reports and species of phytoseiid mites, likely because it is also the area of the origin of Solanaceae (Olmstead 2013). The currently cultivated tomato crops have originated in the central area of South America (Blanca et al. 2012, 2015; Razifard et al. 2020), making this region particularly promising for the study of biological control agents. Many surveys have been carried out in Brazil, especially to search for natural enemies of T. evansi on tomatoes (Rosa et al. 2005; Furtado et al. 2006, 2014; Fiaboe et al. 2007; Silva et al. 2008). Among the species found, P. longipes performed well when fed on T. evansi and T. urticae on tomato plants. Biological parameters of this predator were widely studied (see Furtado et al. 2007; Ferrero et al. 2007, 2014a; Savi et al. 2021) and promising results were obtained on its capacity to control T. evansi on different tomato genotypes (Savi et al. 2021), and some field studies confirmed its efficacy (Ferrero et al. 2014b). The ecological risk of releasing this predator on a large scale outside its natural range, particularly in areas where T. evansi is a pest in Africa, should be carefully assessed.

Surveys of predatory mites in South America have also focused on identification of predators of the tomato russet mite A. lycopersici and on the Tarsonemidae mite Polyphagotarsonemus latus (Banks) (Silva et al. 2016; Duarte et al. 2021). Based in the distribution, abundance, number of host plants, and the association with the target pest, the Phytoseiidae species considered as potential biological control agents were, Typhlodromalus aripo De Leon, Euseius sibelius (De Leon), Phytoseius guianensis De Leon, Euseius citrifolius Denmark and Muma, and Neoseiulus idaeus Denmark and Muma. It is worth note that species of the genera Phytoseius and Typhlodromalus, are classified as subtype IIIA, according to McMurtry et al. (2013); i.e. generalist predators that live on pubescent leaves. These phytoseiid mites possess morphological features, such as a small and laterally compressed idiosoma, which facilitate movements between leaf trichomes. This adaptation allows the mites to colonize microhabitats that larger species do not occupy, thereby avoiding potential competition while benefiting from the presence of prey that also prefers the same microhabitats, e.g. A. lycopersici (McMurtry et al. 2013). The efficacy of some of these predatory mites on tomato and other Solanaceae host plants remains to be fully evaluated.

In addition to the predatory mites identified as potential biological control agents from prospection surveys in the area of origin of tomato, species associated with trichome-rich plants in Europe have also been considered. From surveys conducted in Southern France, the Phytoseiidae Typhlodromus (Anthoseius) recki Wainstein shows promising characteristics (Tixier et al. 2020 b; Tabary et al. 2024). Evaluation of the effect of tomato trichome types on the development, survival and dispersal of T. (A.) recki on six tomato cultivars and two wild Solanum genotypes showed that this predator was not affected by plant characteristics when testing a favourable predator/prey (T. urticae) ratio (1:1) (Tabary et al. 2024). Typhlodromus (A.) recki is also the most reported species on Solanaceae in Europe. This generalist predator efficiently feeds on A. lycopersici, T. urticae and T. evansi, demonstrating promising dispersal abilities on plants with trichomes including in vitro tomato stems (Tixier et al. 2020b).

Another predatory mite family, besides the Phytoseiidae, the Iolinidae family, has been considered for biological control in tomato. Although previously understudied, species in this family are now considered promising, particularly for the control of A. lycopersici. Two species, Pronematus ubiquitus (McGregor) and Homeopronematus anconai (Baker), have been reported to feed and reproduce on A. lycopersici (Kawai and Hacque 2004; Pijnakker et al. 2022). In laboratory conditions, P. ubiquitus with an adult size of 200-300 μm, showed to be small enough to walk across trichomes and prey on A. lycopersici. This mite shows a predation efficacy up to 78% in field conditions (Vervaet et al. 2021). Pijnakker et al. (2022) showed that when P. ubiquitus was released on tomato plants 14 weeks before the introduction of A. lycopersici (the period during which mites were giving supplementary feeding with pollen), the predator successfully prevented pest damages on plants. These authors also showed that P. ubiquitus was able to reduce powdery mildew [Pseudoidium neolycopersici (L. Kiss) L. Kiss] and stated that these Iolinidae mites can offer dual protection for tomato plants by controlling both a pest and a pathogen. Regarding spider mites, the suppression of T. urticae associated with P. ubiquitus releases was suggested by Van de Velde (2021) but this would need to be clarified further. Likewise, greenhouse trials demonstrated that P. ubiquitus and H. anconai are able to reduce damages of A. lycopersici, especially preventing outbreaks in short-term trials (Pijnakker et al. 2020, 2022). It is worth noting that this mite is already mass-produced and commercialized in Europe.

General considerations

Methodologies, achievements and next steps

As discussed in this review, numerous studies have been conducted to understand how trichomes may impact arthropod survival in tomato. With respect to the specific role of each type of trichome, the knowledge of the effect of NGT on arthropods in comparison to GT is rather limited and indicate that very high densities of NGT restricts the dispersal of arthropods. It should be noted that many of the studies focus primarily on herbivorous arthropods, with significantly less emphasis on natural enemies.

When studying the impact of trichomes on natural enemies, lower efficiency is associated with high densities of GTs; however, the underlying mechanisms (chemical, physical) are not well understood. In general, studies focusing on the impact of trichomes on parasitoids are limited. The few studies available describe various deleterious effects. Predatory arthropods, including insects and phytoseiid mites have both a lower survival and development rates in presence of high densities of GTs. Few studies are available on direct and indirect (bioaccumulation) toxicity of the molecules secreted by trichomes. Detailed information on the relationships between predators and phenotypic traits of plants could assist breeders in incorporating traits are favourable to natural enemies into the selection processes for tomato lines.

Most studies have been conducted in the laboratory settings, often performed on detached leaves or leaf disks. However, trichome densities can vary significantly among different plant organs, even of the same plant cultivar. Therefore, a preliminary step would involve conducting further studies on the entire plant, followed by field studies.

The studies included in this review vary in their methodologies, making it challenging to compare trichome densities across publications. Additionally, there is significant variability across plant species, cultivars, organs, and plant age.

Perspectives of tomato pest control

Tomato trichomes have physical and chemical deleterious effects on arthropods, both on pests and on biological control agents. GTs tend to have more detrimental effects on arthropods than NGTs. This explains why most studies have concentrated on them. Small GTs of Solanaceae, as types IV and VI, are more likely to act both as physical and chemical defenses. Toxic effects of trichomes affecting several life history parameters, such as survival, fecundity, and duration of life-stages by different resistance mechanisms (antixenosis, antibiosis and tolerance) have been found for several pests and natural enemies. A more detailed understanding of these interactions is still necessary to support the development of effective pest management strategies. The quest for more sustainable approaches to control pests that circumvent tomato trichome defense mechanisms remains a challenge for researchers. Efforts have focused particularly on enhancing plant genetic resistance and identifying of biological control agents that perform well on tomato.

Secretion of acyl-sugars, methyl ketones and sesquiterpenes have been considered as promising traits to be selected for pest resistance in tomato breeding programs, while focusing mostly on crosses between tomato and closely related wild species – S. pimpinellifolium, S. pennellii, S. galapagense, S. habrochaites. Toxic compounds can exert antixenotic and antibiotic effects in both phytophagous insects and mite populations; therefore, tomato breeding programs can produce genotypes with resistance to a wide range of arthropod pests. For breeders, such aspects may offer a significant advantage. However, a better understanding of genetic basis of such resistance is still necessary to ensure its sustainability, whether if it is monogenic or polygenic. Furthermore, distribution and density of trichomes vary among plant organs that can also be affected by biotic and abiotic parameters, which adds complexity to the development of genetic resistance.

There is widespread consensus on the critical need for biological control solutions for tomato pests; however, most species in the diverse group of natural enemies, both parasitoids (i.e. Trichogrammatidae, Tachinidae, Ichneumonidae,) and predators (Coccinellidae, Anthocoridae, Chrysopidae, Syrphidae, Pentatomidae, Phytoseiidae), are not well adapted to tomato trichomes. Concerning predatory mites, efforts have mainly focused on the prospection for tomato/Solanaceae adapted species in South America, the region of origin for tomato, as well as on trichome rich plants in Europe. Field surveys have identified promising candidates, and the efficiency of some of these candidates has begun to be evaluated. Besides, reduced-size iolinid predatory mites can keep A. lycopersici populations below damage threshold and are already available commercially in Europe. Therefore, while further research is necessary, it can be stated that the prospects for using predatory mites as biological control agents on tomatoes are encouraging. It is important to emphasize that, similar to any other cropping system, biological control must be integrated with other pest management strategies.

How to integrate plant resistance and biological control to manage tomato pests

Different pest management strategies must be combined to achieve satisfactory efficacy. However, the known conflict exists between bottom-up (e.g. plant defenses) and top-down (e.g. biological control) strategies (Riddick and Simmons 2014; Peterson et al. 2016), as constitutive plant defense traits can affect top-down control negatively.

In the context of the tomato pest control, the trade-off between plant resistance and biological control should be adressed. This balance could be achieved by breeding tomato lines with a moderate arthropod resistance level that does not render them entirely unsuitable for biological control agents, thereby allowing for the survival and development of most trichome-adapted species of natural enemies. Most research to date has concentrated on either one strategy or the other; however, success in the field will depend on an integrated approach. It is evident that breeding programs should incorporate the evaluation of biological control agents, and their efficacy should be assessed on cultivars with contrasting phenotypes. In addition, tri-trophic interactions, which have implications for biological control programs, and considered in the development of pest control strategies, as they can strongly influence the efficiency of natural enemies.

It would be wise to exercise caution when considering the suggestions from breeders to explore the option of removing resistance traits from tomato lines (see Legarrea et al. 2022). These suggestions have been based on experimental studies that demonstrated higher performance of mutants in which plant defenses were removed or minimized, thereby allowing them to more effectively suppress mite pest populations. It is important to note that only one group of pests and natural enemies was evaluated in these studies. Before implementing breeding programs aimed at removing tomato defenses, it is crucial to assess the effect on all major groups of pests and natural enemies, as well as on plant physiology and performance.

Acknowledgements

This work was supported by the European Union's Horizon2020 research and innovation program (grant 773 902-SuperPests). We would like to thank the Reviewer and the Editor for the detailed correction and valuable suggestions.

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