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Keywords:

  • Arthropod;
  • biological control;
  • breeding;
  • cheesmanii;
  • hirsutum;
  • host-plant resistance;
  • pennellii;
  • resistance;
  • tomato

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Trichomes of Lycopersicon species
  5. Trichome-based resistance of Lycopersicon spp. to arthropods
  6. Lethal and sublethal effects of trichomes on natural enemies
  7. Trichomes of Lycopersicon hybrids and their effect on arthropods
  8. Conclusions and future work
  9. References

1 The cultivated tomato, Lycopersicon esculentum, is an economically important worldwide crop. Current pest management techniques rely heavily on pesticides but trichome-based host-plant resistance may reduce pesticide use.

2 A review of the literature is provided on trichomes of wild Lycopersicon species and the effects of trichome-based host-plant resistance on arthropods. Solvents have been used to remove glandular trichome exudates and the resulting dimminution of their effects quantified. Correlational approaches to assess the relationship between the different trichome types and effects on pests have also been used.

3 Most studies have focused on Lepidoptera and Hemiptera, although some work has included Coleoptera, Diptera and Acarina, and both antibiotic and antixenotic effects have been demonstrated.

4 Natural enemies are a cornerstone of international pest management and this review discusses how the compatibility of this approach with trichome-based host-plant resistance is uncertain because of the reported negative effects of trichomes on one dipteran, one hemipteran and several Hymenoptera.

5 For trichome-based host-plant resistance to be utilized as a pest management tool, trichomes of wild species need to be introgressed into the cultivated tomato. Hybrids between the cultivated tomato and the wild species Lycopersicon hirsutum f. glabratum, Lycopersicon pennellii and Lycopersicon cheesmanii f. minor have been produced and useful levels of resistance to Acarina, Diptera and Hemiptera pests have been exhibited, although these effects may be tempered by effects on natural enemies.

6 This review proposes that studies on genetic links between fruit quality and resistance, field studies to determine the compatibility of natural enemies and trichome-based host-plant resistance, and a strong focus on L. cheesmanii f. minor, are all priorities for further research that will help realize the potential of this natural defence mechanism in pest management.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Trichomes of Lycopersicon species
  5. Trichome-based resistance of Lycopersicon spp. to arthropods
  6. Lethal and sublethal effects of trichomes on natural enemies
  7. Trichomes of Lycopersicon hybrids and their effect on arthropods
  8. Conclusions and future work
  9. References

The heavy reliance of agriculture on pesticides to manage arthropod pests has led to well-documented negative effects on producers and the environment (Hond et al., 2003). Alternative management strategies, such as the use of pheromones to disrupt mating behaviour, the sterile insect release, the use of natural enemies to prey on or parasitize pests and the genetic modification of plants to produce toxins, continue to be developed. Trichome-based host-plant resistance is a novel mechanism that may have the potential to reduced pesticide use during tomato (Lycopersicon esculentum Mill.) production, increasing its sustainability and reducing negative effects associated with pesticide use. This review aims to bring together literature on the effects of trichome-based host-plant resistance of Lycopersicon species on pests and natural enemies. Literature on the trichomes of hybrids between the cultivated tomato and wild species, together with the effect of trichomes possessed by these hybrids on pests and natural enemies, is also collated. The purpose of doing so is to assess the compatibility of natural enemies used in tomato crops and trichome-based host-plant resistance and to examine the progress made in the production of a tomato with trichome-based host-plant resistance and marketable fruit. Accordingly, suggestions can be made concerning further research needed.

Trichomes of Lycopersicon species

  1. Top of page
  2. Abstract
  3. Introduction
  4. Trichomes of Lycopersicon species
  5. Trichome-based resistance of Lycopersicon spp. to arthropods
  6. Lethal and sublethal effects of trichomes on natural enemies
  7. Trichomes of Lycopersicon hybrids and their effect on arthropods
  8. Conclusions and future work
  9. References

The trichomes of the wild species Lycopersicon pennellii (Correll) D'Arcy, Lycopersicon hirsutum Dunal and L. hirsutum f. glabratum C.H. Mull. have been implicated in resistance and have been the focus of research on trichomes (Kennedy, 2003). Glandular trichomes of Lycopersicon have ‘heads’ that release, on contact with pests, sticky and/or toxic exudates that entrap, irritate and potentially kill the pest. Non-glandular trichomes have no ‘heads’ and affect pests by mechanical means (e.g. constituting a barrier to movement or access to nutritious tissue). The trichomes of Lycopersicon (Table 1) were first examined by Luckwill (1943) and categorized as types I – VII, with types I, IV, VI and VII being glandular and types II, III and V being nonglandular (Fig. 1). Although the trichome categories nominated by Luckwill (1943) have been widely adopted, this system has not been without limitations. In 1943, L. pennellii was placed in the genus Solanum and, as a consequence, its trichomes were not categorized. In addition, the true identity of Lycopersicon pissisi, a species used by Luckwill (1943) (Table 1), is now uncertain (Rick & Lamm, 1955).

Table 1.  Trichome densities of Lycopersicon species
 Trichome type
SpeciesIIIIIIIVVVIVII
  • Adapted from Luckwill (1943). A, Abundant; S, sparse, VS, very sparse.

  • *

    Absent from some individuals.

Lycopersicon esculentumAAAAS
Lycopersicon pimpinellifoliumVSAA
Lycopersicon peruvianumA*AAS
Lycopersicon pissisiVSAAS
Lycopersicon cheesmaniiASS
Lycopersicon hirsutumASAAS
L. glandulosumAAAS
image

Figure 1. Trichomes on L. esculentum (a) and L. hirsutum (b). Letters indicate trichome type as described by Luckwill (1943). Adapted from Luckwill (1943) and used with permission of Oxford University Press.

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Earlier work relating glandular trichomes to arthropod resistance (McKinney, 1938; Gentile & Stoner, 1968; Gentile et al., 1968) has resulted in research focusing on this type of trichome. In the 60 years subsequent to the work carried out by Luckwill (1943), the density has been further assessed for those trichome types found only on L. hirsutum, L. hirsutum f. glabratum, L. pennellii, Lycopersicon cheesmanii L. Riley and L. cheesmanii f. minor (Hook. F) C.H. Mull.. Trichome types IV, V, VI have been reported on L. hirsutum and L. hirsutum f. glabratum in high densities and type I, III and VI trichomes have been reported in low densities (Eigenbrode & Trumble, 1993; Weston et al., 1989; Snyder et al., 1998; Antonious, 2001; Gurr & McGrath, 2001; Gurr & McGrath, 2002; Simmons et al., 2003; Simmons & Gurr, 2004; Simmons et al., 2004). Lycopersicon pennellii possessed all but type II and V trichomes; type IV trichomes are the most dense on this species (Table 2) (Goffreda et al., 1988; Lemke & Mutschler, 1984; Simmons et al., 2003; Simmons & Gurr, 2004; Simmons et al., 2004). Only one study (Simmons & Gurr, 2004) has examined the trichomes on L. cheesmanii and L. cheesmanii f. minor. Types V, VI and VII trichomes only were reported in low densities on L. cheesmanii whereas L. cheesmanii f. minor possessed types I, V, VI and VII trichomes in low densities and type IV trichomes in high densities.

Table 2.  Trichomes reported on wild Lycopersicon species
 Trichome type 
SpeciesIIIIIIIVVVIVIIReference
  1. Adapted from Luckwill (1943). A, Abundant (>5 mm2); S, sparse (5–1 mm2); VS, very sparse (<1 mm2).

Lycopersicon cheesmaniiSSVSSimmons & Gurr (2004)
Lycopersicon cheesmanii f. minorVSASSVSReference as for L. cheesmanii (above)
Lycopersicon hirsutumVSVSAAAVSEigenbrode & Trumble (1993); Antonious (2001); Snyder et al. (1998); Weston et al. (1989); Simmons & Gurr (2004); Simmons et al. (2003); Simmons et al. (2004); Gurr & McGrath (2002)
Lycopersicon hirsutum f. glabratumVSVSAAAVSReferences as for L. hirsutum (above)
Lycopersicon pennelliiVSVSASVSAntonious (2001); Goffreda et al. (1988); Lemke & Mutschler (1984); Simmons & Gurr (2004); Simmons et al. (2003); Simmons et al. (2004)

Trichome-based resistance of Lycopersicon spp. to arthropods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Trichomes of Lycopersicon species
  5. Trichome-based resistance of Lycopersicon spp. to arthropods
  6. Lethal and sublethal effects of trichomes on natural enemies
  7. Trichomes of Lycopersicon hybrids and their effect on arthropods
  8. Conclusions and future work
  9. References

Wild Lycopersicon spp. are generally more resistant to arthropod pests than L. esculentum, although some L. esculentum cultivars have been shown to possess comparable resistance (Heinz & Zalom, 1995). Research into trichome-based host-plant resistance has focused mainly on L. hirsutum, L. hirsutum f. glabratum and L. pennellii, although Schuster (1977) reported L. cheesmanii f. minor had lower levels of leaf damage and numbers of Keiferia lycopersicella (Walsingham) (Lepidoptera: Gelechiidae) larvae compared with L. esculentum, and were as resistant as L. hirsutum and L. hirsutum f. glabratum.

The most studied aspect of trichomes on these species is their ability to confer antibiosis. A popular method to determine the role of glandular trichomes is to use a solvent to remove trichome exudates. Exudate removal has been used to examine the effect of glandular trichomes on various pest species but, as is clear from the taxonomically based summary (Table 3), pests from the orders Hemiptera [e.g. Myzus persicae (Sulzer)] and Lepidoptera [e.g. Helicoverpa armigera (Hubner) (Lepidoptera: Noctuidae)] are the most intensively studied, with only one pest species each studied from Coleoptera [e.g. Leptinotarsa decemlineata (Say) (Coleoptera: Chrysomelidae)] and Diptera. Removal of glandular trichome exudates from plants has increased survival, decreased mortality and entrapment, and increased longevity of pests. A contrasting methodological approach to determine the effects of trichomes on pests is correlation analysis performed to identify the trichome type(s) associated with the fate and/or behaviour of a pest. This method has been used on several lepidopteran pests, M. persicae and the mite, Tetranychus urticae Koch (Acarina: Tetranychidae) (Table 4). The predominant trichomes associated with negative effects on pests (e.g. mortality, survival and entrapment) are the glandular trichomes types IV and VI. Correlation analysis has the advantage over exudate removal approaches for determining the role of nonglandular, as well as glandular, trichomes in resistance. The scarcity of studies reporting the role of nonglandular trichomes in antibiosis is likely to be at least partly a result of the reliance on solvents for removing glandular trichome exudates, and that many studies have determined only the densities of glandular trichomes. The work by Gurr & McGrath (2002) is the only example of a positive relationship between a nonglandular trichome (type V) and the survival of a pest. However, this relationship may be an artefact of plants with high densities of type V trichomes (e.g. L. esculentum) having low densities of type IV and VI trichomes, whereas plants with low densities of type V trichomes have high densities of type IV and VI trichomes. The clear limitation of regression approaches is that correlation does not establish causation.

Table 3.  The effect of glandular trichome exudate removal from Lycopersicon species on pests
OrderPest speciesLycopersicon speciesEffectReference
LepidopteraManduca sextaLycopersicon hirsutum f. glabratumIncreased survivalKennedy & Yamamoto (1979); Barbour et al. (1991)
Keiferia lycopersicellaLycopersicon hirsutum f. glabratum, L. hirsutumIncreased survivalLin & Trumble (1986)
Phthorimaea operculellaLycopersicon hirsutumDecreased mortality, increased survivalGurr & McGrath (2002)
Helicoverpa armigeraL. hirsutum f. glabratum, L. hirsutum, L. pennelliiDecreased entrapment, decreased mortalitySimmons et al. (2004)
Heliothis zeaLycopersicon hirsutum f. glabratumDecreased mortality/ increased survivalDimock & Kennedy (1983); Farrar & Kennedy (1987b), Barbour et al. (1991)
HemipteraMacrosiphum euphorbiaeLycopersicon esculentumIncreased survivalGentile & Stoner (1968)
Macrosiphum euphorbiaeLycopersicon hirsutum f. glabratumDecreased mortalityMusetti & Neal (1997a)
Trialeurodes vapororioriumLycopersicon esculentumCompleted lifecycleGentile et al. (1968)
Myzus persicaeLycopersicon hirsutum f. glabratum, L. hirsutum, L. pennelliiDecreased entrapment, decreased mortalitySimmons et al. (2003)
ColeopteraLeptinotarsa decemlineataLycopersicon hirsutum f. glabratumIncreased longevity/ increased survivalKennedy & Sorenson (1985); Barbour et al. (1991)
DipteraLiriomyza trifoliiLycopersicon pennelliiIncreased puncturesHawthorne et al. (1992)
Table 4.  The effect on pests of an increase in densities of trichome types on Lycopersicon species
OrderPest speciesLycopersicon speciesTrichome typeAssociationReference
LepidopteraHelicoverpa armigeraLycopersicon hirsutum f. glabratum, L. hirsutum, L. pennelliiType IVEntrapmentSimmons et al. (2004)
Spodoptera exiguaLycopersicon hirsutum f. glabratum, L. hirsutumType IVDecreased survivalEigenbrode & Trumble (1993)
Phthorimaea operculellaLycopersicon hirsutumTypes IV and VI Type VIncreased mortality, reduced adult emergence and numbers of mines Increased adult emergence and numbers of mines Gurr & McGrath (2002) Gurr & McGrath (2002)
AcarinaTetranychus urticaeLycopersicon hirsutumType IVMortalityCarter & Snyder (1986)
Tetranychus urticaeLycopersicon hirsutumTypes IV and VISurvivalCarter & Snyder (1986)
HemipteraMyzus persicaeLycopersicon hirsutum f. glabratum, L. hirsutum, L. pennelliiType IVMortalitySimmons et al. (2003)

Antibiosis is thought to be conferred by the chemical constituents of trichome exudates. In addition to the above methodological approaches, studies have incorporated the toxin(s) found in glandular trichome exudates in an artificial diet or placed the toxin(s) on filter paper upon which the pest has been placed. Fery & Cuthbert (1975) reported that the mortality of Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae) on L. hirsutum and L. hirsutum f. glabratum was due to an antibiotic effect; however, the chemical(s) responsible were not identified. Research has subsequently established relationships between individual trichome types and the chemical components of their exudates. Two methyl-ketones from type VI trichomes on L. hirsutum f. glabratum, 2-tridecanone and 2-undecanone, are associated with numerous negative effects on several lepidopteran pests [e.g. Tuta absoluta (Meyrick) (Gelechiidae)], as well as hemipterans [e.g. Aphis gossypii Glover (Aphididae)] (Table 5). Studies have produced conflicting findings on the methyl-ketone content of L. esculentum trichomes.Farrar & Kennedy (1991a) reported that the susceptibility of L. esculentum is likely to be the consequence of an absence of 2-tridecanone and 2-undecanone in type VI trichomes, although Chatzivasileiadis et al. (1999) found both of these methyl-ketones in type VI exudates on L. esculentum. Although many studies have reported negative effects of methyl-ketones on pests, some studies have reported no effect. Manduca sexta (L.) (Lepidoptera: Sphingidae) was not affected by 2-undecanone (Farrar & Kennedy, 1987a) and a study by Eigenbrode & Trumble (1993) found that resistance to Spodoptera exigua (Hubner) (Lepidoptera: Noctuidae) was not related to the concentration of methyl-ketones on L. hirsutum f. glabratum. It is possible that the level of methyl-ketones in type VI trichome exudates is highly variable between accessions and may account for the variable results reported.

Table 5.  Antibiosis-related effects of trichome-based host-plant resistance on arthropod pests
OrderPest speciesLycopersicon speciesToxinEffectReference
  • a

    When compared with Lycopersicon esculentum.

LepidopteraHeliothis zeaLycopersicon hirsutum f. glabratum2-tridecanoneMortality, increased time to pupation, decreased pupal weightFarrar & Kennedy (1987a)
Heliothis zeaLycopersicon hirsutum f. glabratum2-tridecanoneMortalityWilliams et al. (1980)
Heliothis zeaLycopersicon hirsutum f. glabratum2-undecanoneIncreased pupal deformity, decreased pupal weightFarrar & Kennedy (1987a)
Heliothis zeaLycopersicon hirsutum f. glabratum2-tridecanone and 2- undecanoneMortality, increased pupation time, pupal deformity, pupal mortality, decreased pupal weightFarrar & Kennedy (1987a)
Manduca sextaLycopersicon hirsutum f. glabratum2-tridecanoneMortalityWilliams et al. (1980)
Tuta absolutaLycopersicon hirsutum f. glabratum2-tridecanoneMortalityMagalhaes et al. (2001)
Tuta absolutaLycopersicon hirsutumZingiberenedecreased leaflet lesions, leaves attacked and plant damagede Azevedo et al. (2003)
Tuta absolutaLycopersicon hirsutum f. glabratumaIncreased larval period, increased larval mortalityLeite et al. (2001)
Tuta absolutaLycopersicon hirsutum f. glabratum2-undecanoneMortalityMagalhaes et al. (2001)
HemipteraAphis gossypiiLycopersicon hirsutum f. glabratum2-tridecanoneMortalityWilliams et al. (1980)
Macrosiphum euphorbiaeLycopersicon pennelliiAcylsugarsMortalityGoffreda et al. (1989)
Macrosiphum euphorbiaeLycopersicon hirsutum f. glabratum2-tridecanoneMortalityMusetti & Neal (1997b)
Bemisia argentifoliiLycopersicon pennelliiAcylsugarsMortalityMuigai et al. (2002)
ColeopteraLeptinotarsa decelimiataLycopersicon hirsutumZingibereneMortality, decreased survivalCarter et al. (1989a); Carter et al. (1989b)

Zingiberene, a sesquiterpene found in the exudates of type VI trichomes of L. hirsutum (Weston et al., 1989), was toxic to L. deceliminata (Table 5) but absent in type IV trichomes (Carter et al., 1989a). The zingiberene content of L. hirsutum was not related to survival of T. urticae (Good & Snyder, 1988; Weston et al., 1989) or the mortality of S. exigua (Eigenbrode & Trumble, 1993). Another sesquiterpene, γ-elemene, is produced by type IV trichomes of L. hirsutum (Weston et al., 1989), but is yet to be associated with resistance to arthropods. A range of unidentified sesquiterpenes produced by type VI trichomes may also play a role in resistance (Kennedy, 2003). The predominant toxins of L. pennellii are acylsugars, which are found in the exudates of type IV trichomes (Goffreda et al., 1989; Hawthorne et al., 1992), and acylsugars have been associated with negative effects on hemipteran pests (Table 5).

Research indicating that trichome exudates may deter or repel pests suggests that antixenosis may have a potential role in the management of pests. Studies of wild species have demonstrated that oviposition by dipterans, lepidopterans and coleopterans was lower than on L. esculentum (Table 6). Correlation analysis indicated glandular trichomes to be associated with a repellency effect on pests in several orders, although most frequently for the hemipteran, Bemisia argentifolii Bellows and Perring (Hemiptera: Aleyrodidae) and mite species [T. urticae, Tetranychus evansii Baker and Prichard (Acarina: Tetranychidae) and Aculops lycopersici (Massee) (Acarina: Eriophyidae)]. Decreased oviposition by B. argentifolii has been reported on L. hirsutum, L. hirsutum f. glabratum and L. pennellii (Heinz & Zalom, 1995; Muigai et al., 2002) and several other species of Lycopersicon.Snyder et al. (1998) attributed reduced oviposition by B. argentifolii on L. hirsutum to deterrence by type IV trichomes. These effects may be due to the chemicals in trichome exudates (Table 6) because decreased oviposition of B. argentifolii on L. pennellii is associated with a deterrent effect of acylsugars in its type IV trichome exudates (Liedi et al., 1995).

Table 6.  Antixenosis-related effects of trichome-based host-plant resistance on arthropod pests
Order Pest species Lycopersicon species EffectTrichome type/chemical Reference
  • 1

    When compared with Lycopersicon esculentum.

HemipteraTrialeurodes vaporariorumLycopersicon hirsutum f. glabratumReduced oviposition1Bas et al. (1992)
Bemisia argentifoliiMany species includingReduced oviposition1Heinz & Zalom (1995); Muigai et al. (2002)
Bemisia argentifoliiLycopersicon hirsutumReduced ovipositionType IVSnyder et al. (1998)
Bemisia argentifoliiLycopersicon pennelliiReduced oviposition1 Muigai et al. (2002)
Bemisia argentifoliiLycopersicon pennelliiReduced ovipositionAcylsugarsLiedi et al. (1995)
Macrosiphum euphorbiaeLycopersicon hirsutum f. glabratumLeaf abandonment, time to first probe1 Musetti & Neal (1997a)
Macrosiphum euphorbiaeLycopersicon pennelliiIncreased time to first probe, fewer probes, decreased time probing, decreased settlingAcylsugarsGoffreda et al. (1988); Goffreda et al.(1989)
Myzus persicaeLycopersicon hirsutum, L. hirsutum f. glabratum, L. pennelliiIncreased leaf abandonmentType VIISimmons et al. (2003)
DipteraLiriomyza trifoliiLycopersicon pennelliiReduced oviposition, reduced mines and puncturesAcylsugarsHawthorne et al. (1992)
AcarinaTetranychus evansiiLycopersicon hirsutumRepelledZingibereneMaluf et al. 2001
Tetranychus urticaeLycopersicon hirsutum, L. hirsutum f. glabratumRepelled1 Weston et al. (1989)
Aculops lycopersiciLycopersicon hirsutumReduced infestation1Type VILeite et al. (1999b)

However, some pests prefer hirsute surfaces for oviposition [e.g. Phthorimaea operculella (Zeller) (Lepidoptera: Gelechiidae) on Solanum species] (Gurr, 1995), and pubescence is not always favourable for pest suppression. Furthermore, acylglucoses may act as an oviposition stimulant for H. zea (Juvik et al., 1988). Although greater oviposition rates may occur on plants with high trichome densities, the subsequent effects of antibiosis may result in decreased adult emergence (Farrar & Kennedy, 1987b).

Lethal and sublethal effects of trichomes on natural enemies

  1. Top of page
  2. Abstract
  3. Introduction
  4. Trichomes of Lycopersicon species
  5. Trichome-based resistance of Lycopersicon spp. to arthropods
  6. Lethal and sublethal effects of trichomes on natural enemies
  7. Trichomes of Lycopersicon hybrids and their effect on arthropods
  8. Conclusions and future work
  9. References

The effects of trichomes on natural enemies of tomato pests has not been well researched. However, as with pests, the removal of exudates and heads has proven effective at demonstrating significant effects. Exudate removal increases levels of successful emergence of parasitoids, levels of parasitism and reduced mortality (Table 7). Parasitism of H. zea by Trichogramma spp. is lower on L. hirsutum than on L. esculentum and correlation analysis suggested that these effects were due to higher densities of type VI trichomes. These trichomes disturb searching behaviour, although some entrapment was recorded (Kauffman & Kennedy, 1989).

Table 7.  The effect of glandular trichome exudate removal from Lycopersicon species on natural enemies
OrderNatural enemyLycopersicon speciesEffectReference
HymenopteraCampoletis sonorensisLycopersicon hirsutum f. glabratumDecreased mortalityKauffman (1987)
Trichogramma pretiosumLycopersicon hirsutum f. glabratumDecreased mortalityKashyap et al. (1991)
Trichogramma pretiosumLycopersicon hirsutum f. glabratumIncreased emergenceKashyap et al. (1991)
Telenomus sphingisLycopersicon hirsutum f. glabratumIncreased parasitismFarrar & Kennedy (1991b)
HemipteraGeocoris punctipesLycopersicon hirsutum f. glabratumIncreased consumption, reduced mortalityBarbour et al. (1993)
ColeopteraColeomegilla maculataLycopersicon hirsutum f. glabratumIncreased consumption, reduced mortalityBarbour et al. (1993)
DipteraArchytas marmoratusLycopersicon hirsutum f. glabratumDecreased mortalityFarrar et al. (1992)

Studies have found that chemicals found in exudates may have negative effects (e.g. reduced emergence and mortality) on hymenopteran [e.g. Trichogramma pretiosum Riley (Hymenoptera: Trichogrammatidae) and Campoletis sonorensis (Cameron) (Hymenoptera: Ichneumonidae)], dipteran, hemipteran and coleopteran natural enemies (Table 8). However, some studies have found no effect of trichome toxins. Kauffman (1987) reported no effect of 2-tridecanone on parasitism rates of Trichogramma species and Farrar et al. (1992) reported no effect of 2-tridecanone on Archytas marmoratus (Townsend) (Diptera: Tachinidae) and no effect of 2-undecanone on Eucelatoria bryani Sabrosky (Diptera: Tachinidae).Barbour et al. (1993) reported 2-undecanone did not affect mortality of Coleomegilla maculata (DeGeer) (Coleoptera: Coccinellidae) and Geocoris punctipes (Say) (Hemiptera: Lygaeidae) and that G. punctipes mortality was not affected by 2-tridecanone in short-term experiments. Barbour et al. (1993) also reported that trichome exudates and methyl ketones had no indirect effects on C. maculata or G. punctipes.

Table 8.  Antibiosis-related effects of trichome-based host-plant resistance on natural enemies
OrderNatural enemyLycopersicon speciesEffectTrichome type/chemicalReference
  • a

    Results from short-term experiments.

  • b

    Results from long-term experiments.

HymenopteraTrichogramma pretiosumLycopersicon hirsutum f. glabratumReduced emergence, increased development time, induced mortality2-tridecanoneKashyap et al. (1991)
DipteraEulactoria bryaniLycopersicon hirsutum f. glabratumReduced puparia per host2-tridecanoneFarrar et al. (1992)
Archytas marmoratusLycopersicon hirsutum f. glabratumDecreased parasitism, reduced emergence2-undecanoneFarrar et al. (1992)
HemipteraMallada signataLycopersicon cheesmanii, L. cheesmanii f. minor, L. hirsutum, L. hirsutum f. glabratum, L. pennelliiIncreased cannibalism, decreased predationType IVSimmons & Gurr (2004)
Mallada signataLycopersicon cheesmanii, L. cheesmanii f.minor, L. hirsutum, L. hirsutum f.glabratum, L. pennelliiIncreased mortalityTypes IV and IIISimmons & Gurr (2004)
Geocoris punctipesLycopersicon hirsutum f. glabratumReduced consumptiona,b, increased mortality22-tridecanoneBarbour et al. (1993)
Geocoris punctipesLycopersicon hirsutum f. glabratumReduced consumptionb, increased mortality22-undecanoneBarbour et al. (1993)
ColeopteraColeomegilla maculataLycopersicon hirsutum f. glabratumReduced consumptiona,b, increased mortality22-tridecanoneBarbour et al. (1993)
Coleomegilla maculataLycopersicon shirsutum f. glabratumReduced consumptionb, increased mortality22-undecanoneBarbour et al. (1993)

Simmons & Gurr (2004) observed Mallada signata (Schneider) (Hemiptera: Chrysopidae) on the foliage of wild Lycopersicon species and recorded predation of M. persicae. Correlation analysis indicated that type IV trichomes are associated with cannibalism and a decrease in predation. In addition, the mortality of M. signata was found to be associated with increased densities of type IV and type III trichomes.

Trichomes of Lycopersicon hybrids and their effect on arthropods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Trichomes of Lycopersicon species
  5. Trichome-based resistance of Lycopersicon spp. to arthropods
  6. Lethal and sublethal effects of trichomes on natural enemies
  7. Trichomes of Lycopersicon hybrids and their effect on arthropods
  8. Conclusions and future work
  9. References

Research on trichome-based host-plant resistance to arthropod pests has been perfomed primarily to examine its suitability for use as a pest control mechanism, should appropriate traits be transferred to L. esculentum. It is therefore surprising that the density and types of trichomes on hybrids between L. esculentum and wild species has received little attention. Snyder & Carter (1985) determined densities of types I, III, IV, V and VI trichomes on a on F1L. esculentum × L. hirsutum and found only that densities of type III trichomes were greater on the hybrid than on the L. esculentum parent. They also reported that the type VI trichomes found on F1 hybrids had a head morphology, lipid and phenol type and lipid content that was intermediate between the two parents. Carter & Snyder (1985) reported relationships between the densities of each trichome type and all other trichome types, leaflet surface and leaflet length for F2L. esculentum × L. hirsutum hybrids (Table 9).

Table 9.  Relationships between trichome types on F2Lycopersicon esculentum × Lycopersicon hirsutum hybrids
 Trichome type
 IIIIIVVVI
  1. +, Positive relationship; –, negative relationship; NR, no relationship.

IIINR    
IV+   
V  
VINRNRNR+ 
Leaflet surfaceNR++NR
Leaflet lengthNRNRNRNR

Densities and head morphology of type VI trichomes on F1L. esculentum × L. hirsutum f. glabratum hybrids are also intermediate (Fery & Kennedy, 1987; Kauffman & Kennedy, 1989), although the latter authors reported that methyl-ketones were absent from the exudates of the hybrids.

Although the resistance exhibited by hybrids is relatively unstudied, the small amount of literature available suggests that F1 hybrids using L. pennellii as a wild parent may possess greater resistance to arthropods than the L. esculentum parent. Hawthorne et al. (1992) reported that the removal of exudates from F1L. esculentum × L. pennellii progeny increased the number of punctures by Liriomyza trifolii (Burgess) (Diptera: Agromyzidae). When Macrosiphum euphorbiae (Thomas) (Hemiptera: Aphididae) were placed on leaflets of F1L. esculentum × L. pennellii progeny, the numbers nonprobing on the F1 were greater than the numbers on L. esculentum, and the same as on the L. pennellii parent. The time to first probe was also greater on the F1 and the number of probes and time spent probing were reduced (Goffreda et al., 1988). These authors also found that the removal of exudates from the F1 progeny increased the number of probes, but the time to first probe, time spent probing and the average probe duration were unchanged. The repellent effect reported by Goffreda et al. (1989) for L. pennellii may also be effective in F1L. esculentum × L. pennellii hybrids because F1 progeny were infested with fewer M. euphorbiae than the L. esculentum parent, probably due to acylsugars in the exudates of type IV trichomes of F2L. esculentum × L. pennellii hybrids (Goffreda et al., 1990).

Insufficient research has been conducted on L. esculentum × L. hirsutum hybrids to determine the extent to which resistance is inherited. Carter & Snyder (1985) reported that the survival and fecundity of T. urticae on F2L. esculentum × L. hirsutum progeny was related to densities of types I, III, IV and VI trichomes and mortality was related to densities of type IV and VI trichomes. By contrast, resistance to T. urticae (Snyder & Carter, 1984) and L. trifolii (Sorenson et al., 1989) was the same for F1 progeny as it was for the L. esculentum parent. Erb et al. (1993) reported that the F1 progeny produced by crossing L. esculentum × L. cheesmanii f. minor was highly resistant to L. trifolii and resistance was greater than for L. esculentum × L. pennellii hybrids in a no-choice test. In a choice test, resistance was similar to L. pennellii, L. hirsutum and L. hirsutum f. glabratum. Erb et al. (1993) also reported that the removal of exudates decreased resistance, suggesting that glandular trichome exudates played a role. Although these effects appear to be promising, another study by Erb et al. (1994) reported that L. cheesmanii f. minor hybrids possessed little resistance to Trialeurodes vaporariorum (Westwood) (Hemiptera: Aleyrodidae) in choice and no-choice tests.

Trichomes possessed by hybrids may also reduce the effectiveness of natural enemies. Parasitism of M. sexta eggs by Telenomus sphingis (Ashmead) (Hymenoptera: Scelionidae) was lower on an F1L. esculentum ×L. hirsutum f. glabratum hybrid than the L. esculentum parent, but higher than levels recorded on the BC1P2 hybrid and L. hirsutum f. glabratum parent. This trend was observed in both choice and nonchoice tests (Farrar & Kennedy, 1991a). These same authors also reported that the removal of exudates from the F1 progeny increased parasitism rates. Mortality of A. marmoratus on F1L. esculentum × L. hirsutum f. glabratum progeny was greater than the L. esculentum parent and lower than the BC1P2 progeny and L. hirsutum f. glabratum parent. Removal of exudates resulted in reduced mortality on the F1 and equal mortality rates for L. esculentum, L. hirsutum f. glabratum and the F1 rogeny (Farrar et al., 1992).

Conclusions and future work

  1. Top of page
  2. Abstract
  3. Introduction
  4. Trichomes of Lycopersicon species
  5. Trichome-based resistance of Lycopersicon spp. to arthropods
  6. Lethal and sublethal effects of trichomes on natural enemies
  7. Trichomes of Lycopersicon hybrids and their effect on arthropods
  8. Conclusions and future work
  9. References

Research has shown that trichomes of wild Lycopersicon species confer resistance to many pest taxa, although lepidopterans and hemipterans have been the focus of most research reflecting their overall status as pests of tomato. Glandular trichome exudate removal from Lycopersicon species suggests that glandular trichomes may be responsible for the observed negative effects. This has been confirmed by correlation analysis, as well as by others using the chemicals found in glandular trichome exudates topically or in an artificial diet. Arthropod resistance is most often associated with high densities of types IV and VI trichomes on L. hirsutum, L. hirsutum f. glabratum and type IV trichomes on L. pennellii.

Exudate removal studies also indicate that glandular trichomes may negatively affect natural enemies and the one such study to use correlation analysis found that type IV trichomes negatively affected M. signata. However, other studies indicate that natural enemies may not be negatively influenced. More research is required to fully understand the impact of trichome-based host-plant resistance on natural enemies. Although research into direct effects on natural enemies (e.g. mortality) is valuable, there is also a need to investigate the influence of indirect effects (e.g. suitability of prey/host exposed to trichome exudates).

As with parent plants of wild species, the removal of exudates from hybrids indicates that trichome-based host-plant resistance may influence pests, although the trichome type(s) associated with these effects is relatively unstudied. Similarly, studies based on removal of exudates indicate that glandular trichomes may influence natural enemies. The next logical step in introducing trichomes from wild Lycopersicon species into L. esculentum is understanding the genetics of resistance traits such as trichome densities and chemicals in exudates. Research has determined the numbers of genes responsible for (Lemke & Mutschler, 1984; Goffreda & Mutschler, 1989; Freitas et al., 2002), and the quantitative trait loci associated with (Mutschler et al., 1996; Blauth et al., 1998; Blauth et al., 1999), some resistance traits. The goal of a breeding programme is the introduction of trichome-based host-plant resistance into L. esculentum at the same time as maintaining fruit quality. Unlike L. esculentum, the wild species L. hirsutum, L. hirsutum f. glabratum and L. pennellii have fruits that are green when ripe. The research reviewed here suggests that this goal is feasible, but one report (Hartman & St Clair, 1998) found that resistance and the negative fruit characteristics of L. pennellii were genetically correlated. Does this mean that the focus on L. hirsutum, L. hirsutum f. glabratum and L. pennellii is misplaced? Whether or not the research on these species has led to a dead end will be known only when the basis of any genetic correlation is established. Therefore, further studies are needed to examine the genetic correlations between fruit characteristics and resistance for L. hirsutum, L. hirsutum f. glabratum, and to confirm correlations in L. pennellii. If such correlations do exist, further analysis will be required to determine whether they are the result of linkage or a pleiotropic effect (i.e. one gene controls both traits). A genetic correlation due to linkage between genes can theoretically be overcome during recombination of genes, but a pleiotropic effect would make the production of the desired hybrid using L. hirsutum, L. hirsutum f. glabratum or L. pennellii extremely difficult. These genetic studies should determine whether any of these species will be able to produce the desired hybrid and, if so, the most appropriate species for use as the wild parent.

Lycopersicon cheesmanii f. minor may offer a viable alternative to the three much-studied species because it has a closer phylogenetic relationship to L. esculentum and produces fruit that are red–orange when ripe (Rick et al., 1990). Very few studies have examined the resistance of L. cheesmanii f. minor and further research is required to determine the suitability of this species as a wild parent in a breeding program. Bioassays need to be conducted on pests from multiple taxa to determine the level of resistance that L. cheesmanii f. minor exhibits and whether this resistance is associated with the densities of any trichome type(s). Research is also required to identify the toxins, if any, in the exudates of glandular trichomes of L. cheesmanii f. minor.

Due to the ultimately applied nature of this research, field experiments are needed in the early stages of the breeding programme. Variables such as temperature (Nihoul, 1993a; Nihoul, 1993b), photoperiod (Gianfagna et al., 1992; Nihoul, 1993b; Gurr & McGrath, 2001) and plant age (Leite et al., 1998; Leite et al., 1999a; Gurr & McGrath, 2001; Leite et al., 2001) influence resistance and/or trichome densities associated with resistance. Field experiments will allow an understanding of how resistance may change as a result of these variables and indicate when the plants would be most susceptible. Perhaps the most important objective of field experiments is to determine whether trichome-based host-plant resistance will suppress pest densities below a level that requires the use of natural enemies and, if not, whether trichomes will reduce the effectiveness of natural enemies to the point of redundancy. Three scenarios, in order of preference, are possible in this tritrophic system: (i) trichome-based host-plant resistance is effective enough to suppress pest densities to below the relevant economic thresholds with little support from natural enemies; (ii) trichome-based host-plant resistance alone does not maintain pest densities below the thresholds but, despite some ill effects of trichomes, natural enemies are effective enough to maintain pests suppression; or (iii) pests exceed thresholds despite trichome-based host-plant resistance and natural enemies are unable to adequately reduce densities, necessitating the use of other methods, such as insecticides.

It is clear that further research is required to produce a hybrid with trichome-based host-plant resistance and marketable fruit. The challenges faced by Lycopersicon breeders are very similar to those faced by breeders trying to introduce trichome-based host-plant resistance of the wild potato, Solanum berthaultii Hawkes, into the cultivated potato, Solanum tuberosum (L).Kalazich (1991) reported strong associations between trichome-based host-plant resistance and the undesirable agronomic characteristics of S. berthaulii.Plaisted et al. (1992) also indicated that the multigenic inheritance of resistance would make the production of S. tuberosum with trichomes extremely difficult. Even with these expected difficulties, research continues in this field (Yencho et al., 1996; Douches et al., 2001; Coombs et al., 2002; Coombs et al., 2003).

The long-term viability of trichome-based host-plant resistance, if introduced into L. esculentum and used in a crop system to manage pests, remains uncertain. Although yet to be documented, it is possible that arthropods may develop resistance to trichome-based toxins. For example, resistance to the toxin of Bacillus thuringiensis was predicted by Fitt et al. (1994) and is now widely documented. However, glandular trichome-based defences may be more durable because of the multiple toxins found in the glandular trichomes exudates of some wild Lycopersicon species, and the fact that physical (e.g. entrapment) as well as chemical, mechanisms are at play. The antixenotic effect of glandular trichome exudates may also increase the durability of this mechanism by repelling pests. These factors make the pursuit of this form of host-plant resistance attractive despite the paucity of available information in some areas and any practical difficulties in breeding.

Whether or not trichome-based host-plant resistance of a wild Lycopersicon species can be introgressed into L. esculentum and successfully used to manage arthropod pests remains uncertain. However, the negative effects of pesticides and the increasing numbers of pests that are becoming resistant to synthetic pesticides, together with the negative aspects associated with resistance, justifies continued research into this resistance mechanism.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Trichomes of Lycopersicon species
  5. Trichome-based resistance of Lycopersicon spp. to arthropods
  6. Lethal and sublethal effects of trichomes on natural enemies
  7. Trichomes of Lycopersicon hybrids and their effect on arthropods
  8. Conclusions and future work
  9. References
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