Cover Caption

The whitefly Bemisia tabaci is one of the most devastating pests in many crops. It is becoming more and more clear that B. tabaci is not just one species but a species complex consisting of numerous morphologically cryptic species. The cover picture shows a painting of whiteflies entrapped by the glandular trichomes of the tomato wild relative Solanum galapagense. The global picture of the B. tabaci species complex was updated and now consists of at least 38 groups. See pages 723–733. Painting by Syarifin Firdaus.     

不同番茄材料对B型烟粉虱个体发育和繁殖能力的影响

以甘蓝寄主上连续繁殖多代后的B型烟粉虱为对象,对其在8种番茄材料(4个栽培番茄、3个多毛番茄和1个醋栗番茄)上的产卵量、体型大小、发育历期、存活率以及第2代成虫的产卵量和寿命等生物学参数进行观察.自然情况下(10:00-14:00)接虫,烟粉虱在多毛番茄LA2329上的平均产卵量显著低于栽培番茄9706上的产卵量(分别为11粒,164粒).羽化后,烟粉虱雌虫在多毛番茄LA1777上的寿命显著低于在栽培番茄Moneymaker上的存活寿命(分别为5d,22d);而羽化后雌虫在LA1777上的平均产卵量显著低于在栽培番茄早粉2号上的产卵量(分别为7粒/头,95粒/头).在其他参数,如体型大小、存活率、发育历期等,没有显著性的变化.结果显示,较多毛番茄而言,栽培番茄是烟粉虱的较好寄主.而且,在评价抗烟粉虱番茄材料时,平均产卵量、羽化后雌虫寿命及产卵量是3个有效的评价参数.     

Evolution of TPS20-related terpene synthases influences chemical diversity in the glandular trichomes of the wild tomato relative Solanum habrochaites

A systematic screen of volatile terpene production in the glandular trichomes of 79 accessions of Solanum habrochaites was conducted and revealed the presence of 21 mono‐ and sesquiterpenes that exhibit a range of qualitative and quantitative variation. Hierarchical clustering identified distinct terpene phenotypic modules with shared patterns of terpene accumulation across accessions. Several terpene modules could be assigned to previously identified terpene synthase (TPS) activities that included members of the TPS‐e/f subfamily that utilize the unusual cis‐prenyl diphosphate substrates neryl diphosphate and 2z,6z‐farnesyl diphosphate. DNA sequencing and in vitro enzyme activity analysis of TPS‐e/f members from S. habrochaites identified three previously unassigned enzyme activities that utilize these cisoid substrates. These produce either the monoterpenes α‐pinene and limonene, or the sesquiterpene 7‐epizingiberene, with the in vitro analyses that recapitulated the trichome chemistry found in planta. Comparison of the distribution of S. habrochaites accessions with terpene content revealed a strong preference for the presence of particular TPS20 alleles at distinct geographic locations. This study reveals that the unusually high intra‐specific variation of volatile terpene synthesis in glandular trichomes of S. habrochaites is due at least in part to evolution at the TPS20 locus.     

Acylsucrose-producing tomato plants forces Bemisia tabaci to shift its preferred settling and feeding site

Background

The whitefly Bemisia tabaci (Genn.) causes dramatic damage to plants by transmitting yield-limiting virus diseases. Previous studies proved that the tomato breeding line ABL 14-8 was resistant to B. tabaci, the vector of tomato yellow leaf curl disease (TYLCD). This resistance is based on the presence of type IV glandular trichomes and acylsucrose production. These trichomes deter settling and probing of B. tabaci in ABL 14-8, which reduces primary and secondary spread of TYLCD.

Methodology/Principal Findings

Whitefly settlement preference was evaluated on the adaxial and abaxial leaf surfaces of nearly-isogenic tomato lines with and without B. tabaci-resistance traits, ‘ABL 14-8 and Moneymaker’ respectively, under non-choice and free-choice conditions. In addition, the Electrical Penetration Graph technique was used to study probing and feeding activities of B. tabaci on the adaxial and abaxial leaf surfaces of the same genotypes. B. tabaci preferred to settle on the abaxial than on the adaxial surface of ‘Moneymaker’ leaves, whereas no such preference was observed on ABL 14-8 tomato plants at the ten-leaf growth stage. Furthermore, B. tabaci preferred to feed on the abaxial than on the adaxial leaf surface of ‘Moneymarker’ susceptible tomato plants as shown by a higher number of sustained phloem feeding ingestion events and a shorter time to reach the phloem. However, B. tabaci standard probing and feeding behavior patterns were altered in ABL 14-8 plants and whiteflies were unable to feed from the phloem and spent more time in non-probing activities when exposed to the abaxial leaf surface.

Conclusions/Significance

The distorted behavior of B. tabaci on ABL 14-8 protects tomato plants from the transmission of phloem-restricted viruses such as Tomato yellow leaf curl virus (TYLCV), and forces whiteflies to feed on the adaxial side of leaves where they feed less efficiently and become more vulnerable to natural enemies.     

Effect of tomato genotypes with varying levels of susceptibility to Tetranychus evansi on performance and predation capacity of Phytoseiulus longipes

Tetranychus evansi Baker & Pritchard (Acari: Tetranychidae) is an invasive tomato pest in several African, American, Asian and European countries, with potential to reduce yield by up to 90%. Populations of the predaceous phytoseiid mite Phytoseiulus longipes Evans (Acari: Phytoseiidae) has been reported to have high potential for controlling T. evansi. However, tomato genotypes can potentially affect the performance of T. evansi and the predation ability of P. longipes. We evaluated the performance and predation capacity of P. longipes feeding on T. evansi nymphs on the two cultivated genotypes widely grown in Western Africa and a breeding genotype. The two commercial evaluated genotypes were Tounvi (susceptible, with few trichomes), TLCV15 (susceptible, with many trichomes), and the breeding genotype was SPJ-05–2018 (partially resistant with many glandular trichomes) selected from interspecific crossing TLCV15 and PI 13447 (highly resistant wild tomato genotype). We hypothesized that the susceptible genotype (with fewer trichomes) would be more favorable for P. longipes when compared to the susceptible or partially resistant genotypes (with a higher numbers of non-glandular or glandular trichomes). Intrinsic rate of increase (r) and predation potential (ω) of P. longipes were significantly reduced on SPJ-05–2018, possibly due to a negative effect of its glandular trichomes. Although the intrinsic rate of increase was higher on both susceptible genotypes (TLCV15 and Tounvi), predation potential was higher on TLCV15. Our results refuted the hypothesis that T. evansi-susceptible genotype with fewer trichomes would be more favorable to P. longipes.

     

Interaction of fertilizer regime with host-plant resistance in tomato

The effect of fertilizer regime on trichome- and lamellar-based resistance in the wild tomato species, Lycopersicon hirsutum f. glabratum C.H. Mull accession PI 134417, to three insect pests of tomato, the tobacco hornworm, Manduca sexta (L.), the colorado potato beetle, Leptinotarsa decemlineata (Say), and the tomato fruitworm, Heliocoverpa zea (Boddie), was examined. Increasing the rate at which NPK fertilizer was applied, from 1.8 to 19.6 g/plant/week, reduced the trichome-based resistance of PI 134417 to M. sexta and L. decemlineata by lowering both the density of type VI (sensu Luckwill, 1943) glandular trichomes and the amount of 2-tridecanone contained in the tips of these trichomes. 2-Tridecanone is a toxic methyl-ketone responsible for glandular trichome-mediated resistance in PI 134417 to M. sexta and L. decemlineata. A similar increase in the application rate of NPK fertilizer reduced the lamellarbased resistance of PI 134417 to L. decemlineata and H. zea. The meachanisms for this reduction of resistance are unknown, but may be related to improved nutritional quality of hosts at higher fertilizer regimes.     

Inhibition of Telenomus sphingis an egg parasitoid of Manduca spp. by trichome/2-tridecanone-based host plant resistance in tomato

The resistance of accession PI 134417 of the wild tomato Lycopersicon hirsutum f. glabratum C. H. Mull to Manduca sexta (L.) (Lepidoptera: Spingidae) and Leptinotarsa decemlineata (Say) (Coleoptera: Chrysomelidae) is conditioned by the high densities of 2-tridecanone-containing, glandular trichomes associated with the foliage. In laboratory experiments, rates of parasitism of M. sexta eggs by Telenomus sphingis (Ashmead) (Hymenoptera: Scelionidae) were lower among eggs on PI 134417 foliage than among eggs on foliage of the cultivated tomato L. esculentum Mill. (cv. Better Boy). The latter is characterized by a significantly lower density of type VI glandular trichomes than PI 134417 and an absence of 2-tridecanone. Parasitism by T. sphingis was also reduced among eggs on foliage of the F₁ hybrid between PI 134417 and L. esculentum. The hybrid foliage lacks 2-tridecanone but has a density of type VI glandular trichomes that is intermediate between those of PI 134417 and L. esculentum, indicating that elevated densities of type VI glandular trichomes adversely affect T. sphingis. This conclusion was further substantiated by the finding that there were no differences among plant lines in the levels of parasitism of M. sexta eggs when the eggs were on foliage that had been divested of glandular trichomes.In bioassays in which T. sphingis adults or immatures in host eggs were exposed to filter paper treated with 2-tridecanone at rates comparable to those associated with PI 134417 foliage, 2-tridecanone was acutely toxic and caused high levels of mortality. In addition, at high concentrations, 2-tridecanone vapors were repellent to T. sphingis adults. However, when exposed to PI 134417 foliage, few T. sphingis adults were killed.Parasitism of M. sexta eggs was unaffected when the eggs were deposited by moths reared as fifth instar larvae on diet containing 2-tridecanone and/or 2-undecanone at levels comparable to those associated with PI 134417 foliage.     

Accumulation and turnover of 2-tridecanone in Tetranychus urticae and its consequences for resistance of wild and cultivated tomatoes

In this study we assessed the dynamic changes of 2-tridecanone in a herbivorous mite (Tetranychus urticae) on tomato (Lycopersicon esculentum, cv. Moneymaker), a plant with methyl ketones in the tetracellular tips of the glandular trichomes (Type VI). We showed that spider mites accumulate 2-tridecanone when foraging on cultivated tomato. Thus, the rate of mite–trichome contact multiplied by the amount of toxin per trichome tip exceeded the relative rate of toxin turnover multiplied by the amount of toxin per mite. The relative rate of toxin turnover was estimated to be 1.1 per day on cucumber, a plant without this toxin. The amount per trichome tip varied from 0.33 ng for middle-leaf trichomes to 1.26 ng for main-stem trichomes. Hence, to achieve a static level of 2-tridecanone equal to 8–17 ng per mite – representing the level we found in mites on middle leaves – the rate of mite–trichome contact should be 26–57 per day. Because methyl ketone apparently accumulates in the spider mites on tomato, the rate of mite–trichome contact is probably higher than that. We expect the accumulation of ketones to occur especially on the stems of cultivated tomato, since this is the area most densely occupied with glandular hairs and because here the hairs have higher levels of the methyl ketones.Using dose–response relationships assessed earlier (Chatzivasileiadis and Sabelis, 1997, 1998), we estimated that the number of mite–trichome contacts causing 50% mortality per day is equal to 88 on a tomato stem, whereas it equals 70 for another strain of spider mites collected from cucumber. On wild tomato, L. hirsutum f. glabratum (PI 134417), just one to two contacts would suffice to cause 50% mortality per day. We suggest that methyl ketones from glandular hairs on tomato are an important mortality factor for spider mites on wild tomato and probably also on cultivated tomato.     

Resistance to Bemisia tabaci biotype B of Solanum pimpinellifolium is associated with higher densities of type IV glandular trichomes and acylsugar accumulation

Advances in tomato breeding for pest resistance have been achieved via gene introgression from wild Solanum (section Lycopersicon) species (Solanaceae). Ninety‐nine F₃ families derived from an interspecific cross using as parental lines Solanum lycopersicum L. ‘LAM‐148' (susceptible standard) and Solanum pimpinellifolium L. ‘TO‐937‐15’ (multiple pest resistance accession with type IV glandular trichomes and acylsugar accumulation) were evaluated for their resistance against the whitefly Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) biotype B in free‐choice and no‐choice tests for oviposition and adult colonization. The parental lines and eight F₃ families with contrasting levels of resistance against the whitefly were selected and investigated in additional assays, which included the estimation of trichome densities and foliar acylsugar levels. The F₃ families BTR‐302 and BTR‐331 exhibited low amounts of eggs of whitefly and transgressive segregation for type IV glandular trichome density with values greater than that of TO‐937‐15 plants. However, the tested families did not surpass the total foliar acylsugar content found in TO‐937‐15. BTR‐331 exhibited low colonization in the free‐choice test and it was the least preferred F₃ family in the no‐choice test. The higher resistance levels of BTR‐331 were associated with a positive combination of higher type IV trichome density and higher acylsugar levels. Some F₃ families displayed reduced fruit set due to the presence of flowers with style exertion of the antheridial‐cone. Fruit weight at harvest stage of the selected families (from 4.9 to 14.5 g) was lower than that of LAM‐148 (139.5 g) but higher than that of TO‐937‐15 plants (1.3 g). Therefore, although difficult to reach due to the simultaneous segregation of many polygenic traits, the combination of high B. tabaci resistance levels with superior horticultural traits is feasible. These results confirm TO‐937‐15 as a source of biotype B resistance. From the breeding standpoint, the genetic similarity between S. lycopersicum and S. pimpinellifolium would allow a more efficient resistance introgression by facilitating recombination and minimizing the potentially undesirable linkage drag associated with this trait.     

Glandular trichomes of Solanum berthaultii and its hybrids with potato deter oviposition and impair growth of potato tuber moth

Glandular trichomes on foliage of the wild potato species, Solanum berthaultii Hawkes, deter oviposition by the potato tuber moth (PTM), Phthorimaea operculella Zeller and negatively affect other important performance parameters. Oviposition deterring factors are localized in the glandular trichomes of S. berthaultii. When mechanically transferred to foliage of a susceptible potato cultivar, trichome contents reduced egg laying by 97%. Removal of glandular trichomes from S. berthaultii foliage using a combination of chemical and mechanical procedures increased oviposition rates ca. 210-fold. Removal of trichomes also led to increased mobility of larvae on the leaf surface, more leaf feeding, shorter larval development and larger pupae. The resistance conferred by glandular trichomes of S. berthaultii provides an important genetic trait potentially useful for management of PTM.     

A rapid method for isolating glandular trichomes

A physical method is described for the rapid isolation of plant trichomes, with emphasis on stalked glandular types. The technique involved breaking frozen trichomes with powdered dry ice and collection of glandular heads by sieving from larger tissue fragments. This method was applied to several plants that bear similar stalked trichomes: geranium (Pelargonium), potato (Solanum tuberosum), tomato (Lycopersicon esculentum), squash (Cucurbita pepo), and velvetleaf (Abutilon theophrasti). The tissue preparation was of sufficient quality without further purification for biochemical and molecular studies. The preparation maintained the biochemical integrity of the trichomes for active enzymes and usable nucleic acids. A large quantity of tissue can be harvested; for example, 351 milligrams dry weight of glandular trichomes were harvested from geranium pedicels in 12 hours. The utility of the technique was demonstrated by examining the fatty acid composition of tall glandular trichomes of geraniums, Pelargonium ×hortorum L.H. Bailey. These purified cells contained high concentrations of unusual ω5-unsaturated fatty acids, proportionally 23.4% of total fatty acids in the trichomes. When the trichomes were removed, the supporting tissue contained no ω5-fatty acids, thereby unequivocally localizing ω5-fatty acids to the trichomes. Because ω5-fatty acids are unique precursors for the biosynthesis of ω5-anacardic acids, we conclude that anacardic acid synthesis must occur in the glandular trichomes.     

Functionally Divergent Alleles and Duplicated Loci Encoding an Acyltransferase Contribute to Acylsugar Metabolite Diversity in Solanum Trichomes

Glandular trichomes from tomato (Solanum lycopersicum) and other species in the Solanaceae produce and secrete a mixture of O-acylsugars (aliphatic esters of sucrose and glucose) that contribute to insect defense. Despite their phylogenetic distribution and diversity, relatively little is known about how these specialized metabolites are synthesized. Mass spectrometric profiling of acylsugars in the S. lycopersicum x Solanum pennellii introgression lines identified a chromosome 11 locus containing a cluster of BAHD acyltransferases with one gene (named Sl-ASAT3) expressed in tip cells of type I trichomes where acylsugars are made. Sl-ASAT3 was shown to encode an acyl-CoA-dependent acyltransferase that catalyzes the transfer of short (four to five carbons) branched acyl chains to the furanose ring of di-acylsucrose acceptors to produce tri-acylsucroses, which can be further acetylated by Sl-ASAT4 (previously Sl-AT2). Among the wild tomatoes, diversity in furanose ring acyl chains on acylsucroses was most striking in Solanum habrochaites. S. habrochaites accessions from Ecuador and northern Peru produced acylsucroses with short (≤C5) or no acyl chains on the furanose ring. Accessions from central and southern Peru had the ability to add short or long (up to C12) acyl chains to the furanose ring. Multiple ASAT3-like sequences were found in most accessions, and their in vitro activities correlated with observed geographical diversity in acylsugar profiles.     

Tomato stem trichomes and dispersal success ofPhytoseiulus persimilis relative to its preyTetranychus urticae

Tomato varieties used at present for commercial production in Dutch glasshouses have a high density of glandular trichomes on the stem, but a very low density on the leaves. The two-spotted spider mite,Tetranychus urticae Koch, and the predatory mite,Phytoseiulus persimilis Athias-Henriot, usually disperse from leaf to leaf via the stem, thereby incurring high risks of entrapment (and death) in the exudate of the glandular trichomes. These risks have been quantified on the tomato cv. Turbo and an accession ofLycopersicon peruvianum almost free of glandular trichomes. The possible consequences for biological control are discussed and new perspectives for predator release strategies and for plant breeding are considered.     

Trichomes of Lycopersicon species and their hybrids: effects on pests and natural enemies

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.     

Tomato-produced 7-epizingiberene and R-curcumene act as repellents to whiteflies

How whiteflies (Bemisia tabaci) make the choice for a host plant prior to landing, is not precisely known. Here we investigated whether they respond to specific volatiles of tomato. Zingiberene and curcumene were purified from Solanum habrochaites (PI127826), characterised by NMR and X-ray analysis and identified as 7-epizingiberene and R-curcumene. In contrast, oil from Zingiber officinalis contained the stereoisomers zingiberene and S-curcumene, respectively. Using a combination of free-choice bio-assays and electroantennography, 7-epizingiberene and its dehydrogenated derivative R-curcumene were shown to be active as semiochemicals to B. tabaci adults, whereas the stereoisomers from ginger were not. In addition, R-curcumene elicited the strongest electroantennographic response. Bio-assays showed that a cultivated tomato could be made less attractive to B. tabaci than its neighbouring siblings by the addition of the tomato stereoisomer 7-epizingiberene or its derivative R-curcumene. These sesquiterpenes apparently repel adult whiteflies prior to landing, presumably because it informs them that after landing they, or their offspring, may be exposed to higher and lethal concentrations of the same compounds.     

α-Santalol derivatives from Santalum album and their cytotoxic activities

A bioassay-guided fractionation of the heartwood of Santalum album led to the isolation of seven α-santalol derivatives including (9S,10E)-9-hydroxy-α-santalal, (10R,11S)-10,11-dihydroxy-α-santalol, (9E)-11,13-dihydroxy-α-santalol, and (10E)-12-hydroxy-α-santalic acid. Their structures were determined on the basis of results of spectroscopic analysis, including two-dimensional (2D) NMR spectroscopic data. The isolated compounds and derivatives were evaluated for cytotoxicity against HL-60 human promyelocytic leukemia cells and TIG-3 normal human diploid fibroblasts. Of these (9S,10E)-9-hydroxy-α-santalal, exhibited tumor-selective cytotoxicity. The apoptosis induction properties of sesquiterpenes with cytotoxic potency in HL-60 cells are also described.     

A Novel Pathway for Sesquiterpene Biosynthesis from Z,Z-Farnesyl Pyrophosphate in the Wild Tomato Solanum habrochaites

In the wild tomato Solanum habrochaites, the Sst2 locus on chromosome 8 is responsible for the biosynthesis of several class II sesquiterpene olefins by glandular trichomes. Analysis of a trichome-specific EST collection from S. habrochaites revealed two candidate genes for the synthesis of Sst2-associated sesquiterpenes. zFPS encodes a protein with homology to Z-isoprenyl pyrophosphate synthases and SBS (for Santalene and Bergamotene Synthase) encodes a terpene synthase with homology to kaurene synthases. Both genes were found to cosegregate with the Sst2 locus. Recombinant zFPS protein catalyzed the synthesis of Z,Z-FPP from isopentenylpyrophosphate (IPP) and dimethylallylpyrophosphate (DMAPP), while coincubation of zFPS and SBS with the same substrates yielded a mixture of olefins identical to the Sst2-associated sesquiterpenes, including (+)-α-santalene, (+)-endo-β-bergamotene, and (−)-endo-α-bergamotene. In addition, headspace analysis of tobacco (Nicotiana sylvestris) plants expressing zFPS and SBS in glandular trichomes afforded the same mix of sesquiterpenes. Each of these proteins contains a putative plastid targeting sequence that mediates transport of a fused green fluorescent protein to the chloroplasts, suggesting that the biosynthesis of these sesquiterpenes uses IPP and DMAPP from the plastidic DXP pathway. These results provide novel insights into sesquiterpene biosynthesis and have general implications concerning sesquiterpene engineering in plants.