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Evolution of Increased Photosynthetic Capacity and Its Underlying Traits in Invasive Jacobaea vulgaris
Lin, Tiantian ; Klinkhamer, Peter G.L. ; Pons, Thijs L. ; Mulder, Patrick P.J. ; Vrieling, Klaas - \ 2019
Frontiers in Plant Science 10 (2019). - ISSN 1664-462X
evolution of increased competitive ability hypothesis - invasion ecology - photosynthetic capacity - pyrrolizidine alkaloids - root carbohydrate storage - shifting defense hypothesis
The evolution of increased competitive ability (EICA) hypothesis and the shifting defense hypothesis (SDH) predict that evolutionary changes occur in a suite of traits related to defense and growth in invasive plant species as result of the absence of specialist herbivores. We tested how this suite of traits changed due to the absence of specialist herbivores in multiple invasive regions that differ in climatic conditions with native and invasive Jacobaea vulgaris in a controlled environment. We hypothesized that invasive J. vulgaris in all invasive regions have i) a higher plant growth and underlying traits, such as photosynthetic capacity, ii) lower regrowth-related traits, such as carbohydrate storage, and iii) an increased plant qualitative defense, such as pyrrolizidine alkaloids (PAs). Our results show that invasive J. vulgaris genotypes have evolved a higher photosynthetic rate and total PA concentration but a lower investment in root carbohydrates, which supports the SDH hypothesis. All the traits changed consistently and significantly in the same direction in all four invasive regions, indicative of a parallel evolution. Climatic and soil variables did differ between ranges but explained only a very small part of the variation in trait values. The latter suggests that climate and soil changes were not the main selective forces on these traits.
Trichome Independent Resistance against Western Flower Thrips in Tomato
Bac-Molenaar, Johanna A. ; Mol, Selena ; Verlaan, Maarten G. ; Elven, Joke van; Kim, Hye Kyong ; Klinkhamer, Peter G.L. ; Leiss, Kirsten A. ; Vrieling, Klaas - \ 2019
Plant and Cell Physiology 60 (2019)5. - ISSN 0032-0781 - p. 1011 - 1024.
Insect resistance - Metabolite profiles - QTL mapping - Tomato - Trichome-derived volatiles - α-Tomatine
Western flower thrips (WFT) are a major pest on many crops, including tomato. Thrips cause yield losses, not only through feeding damage, but also by the transmission of viruses of which the Tomato Spotted Wilt Virus is the most important one. In cultivated tomato, genetic diversity is extremely low, and all commercial lines are susceptible to WFT. Several wild relatives are WFT resistant and these resistances are based on glandular trichome-derived traits. Introgression of these traits in cultivated lines did not lead to WFT resistant commercial varieties so far. In this study, we investigated WFT resistance in cultivated tomato using a F2 population derived from a cross between a WFT susceptible and a WFT resistant cultivated tomato line. We discovered that this WFT resistance is independent of glandular trichome density or trichome-derived volatile profiles and is associated with three QTLs on chromosomes 4, 5 and 10. Foliar metabolic profiles of F3 families with low and high WFT feeding damage were clearly different. We identified α-tomatine and a phenolic compound as potential defensive compounds. Their causality and interaction need further investigation. Because this study is based on cultivated tomato lines, our findings can directly be used in nowadays breeding programs.
Ultraviolet radiation enhances salicylic acid-mediated defense signaling and resistance to Pseudomonas syringae DC3000 in a jasmonic acid-deficient tomato mutant
Escobar Bravo, Rocío ; Chen, Gang ; Grosser, Katharina ; Dam, Nicole M. Van; Leiss, Kirsten A. ; Klinkhamer, Peter G.L. - \ 2019
Plant Signaling & Behavior 14 (2019)4. - ISSN 1559-2316 - p. e1581560 - e1581560.
Abscisic acid - auxin - jasmonates - light - salicylic acid - ultraviolet radiation - western flower thrips
Ultraviolet radiation (UV) is an important modulator of plant defenses against biotic stresses. We have recently described that different supplemental UV exposure times and irradiance intensities enhanced tomato (Solanum lycopersicum) resistance to Western flower thrips (Frankliniella occidentalis). UV increased jasmonic acid-isoleucine (JA-Ile) and salicylic acid (SA) levels, as well as the expression of JA- and SA-responsive genes, before thrips herbivory. Here we report how UV affects tomato defense responses upon thrips infestation, and resistance to pathogens that are susceptible to the activation of SA-associated defenses. Our experiments reveal that, at 7 days after thrips infestation, UV did not enhance the levels of jasmonates, auxin or abscisic acid. UV also did not affect the expression of JA-responsive genes in the cultivar Moneymaker, the jasmonate deficient mutant def-1, the type-VI trichome deficient mutant od-2, or their wild-type Castlemart. However, UV strongly activated SA-associated defense responses in def-1 after thrips infestation. Further bioassays showed that UV increased def-1 resistance to the hemi-biotrophic bacterial pathogen Pseudomonas syringae pv. tomato DC3000, which is susceptible to SA-mediated defenses. Our results suggest that UV might enhance tomato resistance to this pathogen in the JA deficient genotype through the activation of SA defenses.
Identification and characterization of metabolite quantitative trait loci in tomato leaves and comparison with those reported for fruits and seeds
Nunes-Nesi, Adriano ; Alseekh, Saleh ; Oliveira Silva, Franklin Magnum de; Omranian, Nooshin ; Lichtenstein, Gabriel ; Mirnezhad, Mohammad ; González, Roman R.R. ; y Garcia, Julia Sabio ; Conte, Mariana ; Leiss, Kirsten A. ; Klinkhamer, Peter G.L. ; Nikoloski, Zoran ; Carrari, Fernando ; Fernie, Alisdair R. - \ 2019
Metabolomics 15 (2019)4. - ISSN 1573-3882
Leaf metabolism - Metabolite network - Metabolite QTL - Tomato
Introduction: To date, most studies of natural variation and metabolite quantitative trait loci (mQTL) in tomato have focused on fruit metabolism, leaving aside the identification of genomic regions involved in the regulation of leaf metabolism. Objective: This study was conducted to identify leaf mQTL in tomato and to assess the association of leaf metabolites and physiological traits with the metabolite levels from other tissues. Methods: The analysis of components of leaf metabolism was performed by phenotypying 76 tomato ILs with chromosome segments of the wild species Solanum pennellii in the genetic background of a cultivated tomato (S. lycopersicum) variety M82. The plants were cultivated in two different environments in independent years and samples were harvested from mature leaves of non-flowering plants at the middle of the light period. The non-targeted metabolite profiling was obtained by gas chromatography time-of-flight mass spectrometry (GC-TOF-MS). With the data set obtained in this study and already published metabolomics data from seed and fruit, we performed QTL mapping, heritability and correlation analyses. Results: Changes in metabolite contents were evident in the ILs that are potentially important with respect to stress responses and plant physiology. By analyzing the obtained data, we identified 42 positive and 76 negative mQTL involved in carbon and nitrogen metabolism. Conclusions: Overall, these findings allowed the identification of S. lycopersicum genome regions involved in the regulation of leaf primary carbon and nitrogen metabolism, as well as the association of leaf metabolites with metabolites from seeds and fruits.
Methyl Jasmonate Changes the Composition and Distribution Rather than the Concentration of Defence Compounds : a Study on Pyrrolizidine Alkaloids
Wei, Xianqin ; Vrieling, Klaas ; Mulder, Patrick P.J. ; Klinkhamer, Peter G.L. - \ 2019
Journal of Chemical Ecology 45 (2019)2. - ISSN 0098-0331 - p. 136 - 145.
Conversion - Erucifoline - Feeding damage - Herbivory - Induced defense - Jacobaea plants - Reallocation - Seneciphylline
In this study we investigated the effect of methyl jasmonate (MeJA) application on pyrrolizidine alkaloid (PA) concentration and composition of two closely related Jacobaea species. In addition, we examined whether MeJA application affected herbivory of the polyphagous leaf feeding herbivore Spodoptera exigua. A range of concentrations of MeJA was added to the medium of Jacobaea vulgaris and J. aquatica tissue culture plants grown under axenic conditions. PA concentrations were measured in roots and shoots using LC-MS/MS. In neither species MeJA application did affect the total PA concentration at the whole plant level. In J. vulgaris the total PA concentration decreased in roots but increased in shoots. In J. aquatica a similar non-significant trend was observed. In both Jacobaea species MeJA application induced a strong shift from senecionine- to erucifoline-like PAs, while the jacobine- and otosenine-like PAs remained largely unaffected. The results show that MeJA application does not necessarily elicits de novo synthesis, but rather leads to PA conversion combined with reallocation of certain PAs from roots to shoots. S. exigua preferred feeding on control leaves of J. aquatica over MeJA treated leaves, while for J. vulgaris both the control and MeJA treated leaves were hardly eaten. This suggests that the MeJA-induced increase of erucifoline-like PAs can play a role in resistance of J. aquatica to S. exigua. In J. vulgaris resistance to S. exigua may already be high due to the presence of jacobine-like PAs or other resistance factors.
Induced resistance against western flower thrips by the pseudomonas syringae-derived defense elicitors in tomato
Chen, Gang ; Escobar-Bravo, Rocío ; Kim, Hye Kyong ; Leiss, Kirsten A. ; Klinkhamer, Peter G.L. - \ 2018
Frontiers in Plant Science 9 (2018). - ISSN 1664-462X
Coronatine - Frankliniella occidentalis - Induced plant defenses - Jasmonic acid - Pseudomonas syringae - Salicylic acid - Solanum lycopersicum - Type VI glandular trichomes
Western flower thrips (WFT) Frankliniella occidentalis (Pergande) is a key agricultural pest of cultivated tomatoes. Induced host plant resistance by activating jasmonic acid (JA) signaling pathway constitutes a promising method for WFT control. The phytotoxin coronatine (COR), produced by Pseudomonas syringae pv. tomato DC3000 (Pst), mimics the plant hormone JA-Isoleucine and can promote resistance against herbivorous arthropods. Here we determined the effect of Pst and COR on tomato resistance against WFT, induction of JA and salicylic acid (SA) associated defenses, and plant chemistry. Additionally, we investigated the presence of other components in Pst-derived and filtered culture medium, and their interactive effect with COR on tomato resistance to WFT. Our results showed that infiltration of COR or Pst reduced WFT feeding damage in tomato plants. COR and Pst induced the expression of JA-associated gene and protein marker. COR also induced expression of a SA-related responsive gene, although at much less magnitude. Activation of JA defenses in COR and Pst infiltrated plants did not affect density of type VI leaf trichomes, which are defenses reported to be induced by JA. An untargeted metabolomic analysis showed that both treatments induced strong changes in infiltrated leaves, but leaf responses to COR or Pst slightly differed. Application of the Pst-derived and filtered culture medium, containing COR but not viable Pst, also increased tomato resistance against WFT confirming that the induction of tomato defenses does not require a living Pst population to be present in the plant. Infiltration of tomato plants with low concentrations of COR in diluted Pst-derived and filtered culture medium reduced WFT feeding damage in a greater magnitude than infiltration with an equivalent amount of pure COR indicating that other elicitors are present in the medium. This was confirmed by the fact that the medium from a COR-mutant of Pst also strongly reduced silver damage. In conclusion, our results indicate that induction of JA defenses by COR, Pst infection, the medium of Pst and the medium of a Pst COR- mutant increased resistance against WFT. This was not mediated by the reinforcement of leaf trichome densities, but rather the induction of chemical defenses.
Type VI glandular trichome density and their derived volatiles are differently induced by jasmonic acid in developing and fully developed tomato leaves : Implications for thrips resistance
Chen, Gang ; Klinkhamer, Peter G.L. ; Escobar-Bravo, Rocío ; Leiss, Kirsten A. - \ 2018
Plant Science 276 (2018). - ISSN 0168-9452 - p. 87 - 98.
Developmental stages - Frankliniella occidentalis - Induced defenses - Phytohormone - Solanum lycopersicum
Variation in the induction of plant defenses along the plant canopy can determine distribution and colonization of arthropod herbivores within the plant. In tomato, type VI glandular trichomes, which are epidermal defensive structures, and their derived volatiles are induced by the phytohormone jasmonic acid (JA). How JA-mediated induction of these trichome-associated chemical defenses depends on the leaf developmental stage and correlates with resistance against herbivory is unknown. We showed that application of JA reduced thrips-associated damage, however the amplitude of this response was reduced in the fully developed leaves compared to those still developing. Although JA increased type-VI trichome densities in all leaf developmental stages, as well as JA-inducible defensive proteins, these increases were stronger in developing leaves. Remarkably, the concentration of trichome-derived volatiles was induced by JA to a larger degree in developing leaves than in fully developed leaves. In fully developed leaves, the increase in trichome-derived volatiles was explained by an enhanced production per trichome, while in developing leaves this was mainly caused by increases in type-VI trichome densities. Together, we showed that JA-mediated induction of trichome density and chemistry depends on leaf development stage, and it might explain the degree of thrips-associated leaf damage in tomato.
Thrips advisor : Exploiting thrips-induced defences to combat pests on crops
Steenbergen, Merel ; Abd-El-Haliem, Ahmed ; Bleeker, Petra ; Dicke, Marcel ; Escobar-Bravo, Rocio ; Cheng, Gang ; Haring, Michel A. ; Kant, Merijn R. ; Kappers, Iris ; Klinkhamer, Peter G.L. ; Leiss, Kirsten A. ; Legarrea, Saioa ; Macel, Mirka ; Mouden, Sanae ; Pieterse, Corné M.J. ; Sarde, Sandeep J. ; Schuurink, Robert C. ; Vos, Martin De; Wees, Saskia C.M. Van; Broekgaarden, Colette - \ 2018
Journal of Experimental Botany 69 (2018)8. - ISSN 0022-0957 - p. 1837 - 1848.
Cell-content feeder - effectors - herbivorous insect - phytohormone signalling - plant defence - specialized metabolites - thrips - virus - volatiles
Plants have developed diverse defence mechanisms to ward off herbivorous pests. However, agriculture still faces estimated crop yield losses ranging from 25% to 40% annually. These losses arise not only because of direct feeding damage, but also because many pests serve as vectors of plant viruses. Herbivorous thrips (Thysanoptera) are important pests of vegetable and ornamental crops worldwide, and encompass virtually all general problems of pests: they are highly polyphagous, hard to control because of their complex lifestyle, and they are vectors of destructive viruses. Currently, control management of thrips mainly relies on the use of chemical pesticides. However, thrips rapidly develop resistance to these pesticides. With the rising demand for more sustainable, safer, and healthier food production systems, we urgently need to pinpoint the gaps in knowledge of plant defences against thrips to enable the future development of novel control methods. In this review, we summarize the current, rather scarce, knowledge of thrips-induced plant responses and the role of phytohormonal signalling and chemical defences in these responses. We describe concrete opportunities for breeding resistance against pests such as thrips as a prototype approach for next-generation resistance breeding.
The correlation between leaf-surface and leaf-tissue secondary metabolites : a case study with pyrrolizidine alkaloids in Jacobaea hybrid plants
Cheng, Dandan ; Mulder, Patrick P.J. ; Meijden, Eddy van der; Klinkhamer, Peter G.L. ; Vrieling, Klaas - \ 2017
Metabolomics 13 (2017)5. - ISSN 1573-3882
Host-plant recognition - Jacobaea aquatica - Jacobaea vulgaris - Oviposition - Secondary metabolites
Introduction: Usually whole plant or whole leaf extracts are analyzed to study the chemical ecology of insect-plant interactions. For herbivore species the contact with the leaf surface enables them to estimate the quality of the plant. The relationship between the leaf-surface and leaf-tissue secondary metabolites (SMs) could offer important new insights in insect-plant interactions mediated by SMs. Pyrrolizidine alkaloids (PAs), typical defense chemicals in Jacobaea species, are repellent for generalist herbivores but are attractive to specialists. Objectives: Explore whether the PAs on the leaf surface are a reliable representation of the PAs in the leaf tissue in PA-containing plants. Method: The concentration of individual PAs present on the leaf surface and in the corresponding leaf tissue from 37 genotypes (one plant from each genotype) of an F2 generation of a cross between Jacobaea vulgaris and Jacobaea aquatica was measured by high performance liquid chromatography coupled to tandem mass spectrometry (LC-MS/MS). PAs were removed from the leaf surface by extraction with a slightly acidic aqueous solution. Results: The total amount of PAs present on the surface of the leaves was only 0.015% (range 0.001–0.163%) of the total amount present in the leaf tissue. Most PAs present in the leaf tissue were also found on the surface, except for jaconine, dehydrojaconine, dehydrojacoline and usaramine N-oxide. Positive correlations between leaf-surface and leaf-tissue concentrations were found for most of the jacobine-like and otosenine-like PAs, but correlations for total PA, senecionine- and erucifoline-like PAs were not significant. Conclusion: These results indicate that PA variation on the leaf surface only partially reflects the PA variation in the leaf tissue. Because most herbivores are affected in a different manner by individual PAs, this result means that the leaf surface does not give a reliable estimate of plant quality to herbivores.
Local adaptation in oviposition choice of a specialist herbivore : The cinnabar moth
Wei, Xianqin ; Vrieling, Klaas ; Mulder, Patrick P.J. ; Klinkhamer, Peter G.L. - \ 2017
Acta Oecologica-International Journal of Ecology 79 (2017). - ISSN 1146-609X - p. 1 - 7.
Batch size - Defoliation - Egg batch - Jacobaea plants - Plant size - Tyria jacobaeae
Specialist herbivores feed on a restricted number of related plant species and may suffer food shortage if overexploitation leads to periodic defoliation of their food plants. The density, size and quality of food plants are important factors that determine the host plant choice of specialist herbivores. To explore how all these factors influence their oviposition behaviour, we used the cinnabar moth Tyria jacobaeae and the hybrids of a cross between Jacobaea vulgaris and J. aquatica as a study system. While defoliation by the cinnabar moth is common in the coastal area of The Netherlands, it is relatively rare in inland ragwort population. Ragworts contain pyrrolizidine alkaloids (PAs) and those that are found in coastal areas are rich in jacobine-like PAs while those that occur inland are rich in erucifoline-like PAs. We tested how the oviposition preference was influenced by plant size, nitrogen and water content and PA composition. We used cinnabar moth populations from a regularly defoliated area, Meijendel, and Bertogne, a rarely defoliated area. Our results revealed no effects of nitrogen or water content on oviposition preference. Moths from both populations laid larger egg batches on the plants rich in jacobine-like PAs. Moths from Meijendel preferred larger plants and spread their eggs over more egg batches that were, on average, smaller than those of Bertogne moths. These results suggest that Meijendel moths adopted a oviposition strategy to cope with potential defoliation.
Are effects of common ragwort in the Ames test caused by pyrrolizidine alkaloids?
Bovee, T.F.H. ; Helsdingen, R.J.R. ; Hoogenboom, R.L.A.P. ; Nijs, M.W.C.M. de; Liu, Xiaojie ; Vrieling, Klaas ; Klinkhamer, P.G.L. ; Peijnenburg, A.A.C.M. ; Mulder, P.P.J. - \ 2015
Mutation Research. Fundamental and Molecular Mechanisms of Mutagenesis 778 (2015). - ISSN 0027-5107 - p. 1 - 10.
Ames test - LC-MS/MS - Pyrrolizidine alkaloids - Quercetin - Ragwort
It has previously been demonstrated by others that acetone extracts of Senecio jacobaea (syn. Jacobaea vulgaris, common or tansy ragwort) test positive in the Salmonella/microsome mutagenicity test (Ames test). Pyrrolizidine alkaloids (PAs) are thought to be responsible for these mutagenic effects. However, it was also observed that the major PA present in common ragwort, jacobine, produced a negative response (with and without the addition of rat liver S9) in Salmonella test strains TA98, TA100, TA1535 and TA1537. To investigate which compounds in the plant extracts were responsible for the positive outcome, the present study investigated the contents and mutagenic effects of methanol and acetone extracts prepared from dried ground S. jacobaea and Senecio inaequidens (narrow-leafed ragwort). Subsequently, a fractionation approach was set up in combination with LC-MS/MS analysis of the fractions. It was shown that the positive Ames test outcomes of S. jacobaea extracts are unlikely to be caused by PAs, but rather by the flavonoid quercetin. This study also demonstrates the importance of identifying compounds responsible for positive test results in bioassays.
Testing the Generalist-Specialist Dilemma: The Role of Pyrrolizidine Alkaloids in Resistance to Invertebrate Herbivores in Jacobaea Species
Wei, X. ; Vrieling, K. ; Mulder, P.P.J. ; Klinkhamer, P.G.L. - \ 2015
Journal of Chemical Ecology 41 (2015). - ISSN 0098-0331 - p. 159 - 167.
longitarsus flea beetles - senecio-jacobaea - secondary metabolites - natural-selection - chemical defense - ipomopsis-aggregata - plant defense - scarlet-gilia - host plants - hybridization
Plants produce a diversity of secondary metabolites (SMs) to protect them from generalist herbivores. On the other hand, specialist herbivores use SMs for host plant recognition, feeding and oviposition cues, and even sequester SMs for their own defense. Therefore, plants are assumed to face an evolutionary dilemma stemming from the contrasting effects of generalist and specialist herbivores on SMs. To test this hypothesis, bioassays were performed with F2 hybrids from Jacobaea species segregating for their pyrrolizidine alkaloids (PAs), using a specialist flea beetle (Longitarsus jacobaeae) and a generalist slug (Deroceras invadens). Our study demonstrated that while slug feeding damage was negatively correlated with the concentration of total PAs and that of senecionine-like PAs, flea beetle feeding damage was not affected by PAs. It was positively correlated though, with leaf fresh weight. The generalist slug was deterred by senecionine-like PAs but the specialist flea beetle was adapted to PAs in its host plant. Testing other herbivores in the same plant system, it was observed that the egg number of the specialist cinnabar moth was positively correlated with jacobine-like PAs, while the silver damage of generalist thrips was negatively correlated with senecionine- and jacobine-like PAs, and the pupae number of generalist leaf miner was negatively correlated with otosenine-like PAs. Therefore, while the specialist herbivores showed no correlation whatsoever with PA concentration, the generalist herbivores all showed a negative correlation with at least one type of PA. We concluded that the generalist herbivores were deterred by different structural groups of PAs while the specialist herbivores were attracted or adapted to PAs in its host plants.
New insights into domestication of carrot from root transcriptome analyses
Rong, J. ; Lammers, Y. ; Strasburg, J.L. ; Schidlo, N.S. ; Ariyurek, Y. ; Jong, T.J. de; Klinkhamer, P.G.L. ; Smulders, M.J.M. ; Vrieling, K. - \ 2014
BMC Genomics 15 (2014). - ISSN 1471-2164 - 15 p.
daucus-carota l. - nucleotide polymorphism - wild - populations - inference - sativus - genome - diversity - sequences - selection
Background - Understanding the molecular basis of domestication can provide insights into the processes of rapid evolution and crop improvement. Here we demonstrated the processes of carrot domestication and identified genes under selection based on transcriptome analyses. Results - The root transcriptomes of widely differing cultivated and wild carrots were sequenced. A method accounting for sequencing errors was introduced to optimize SNP (single nucleotide polymorphism) discovery. 11,369 SNPs were identified. Of these, 622 (out of 1000 tested SNPs) were validated and used to genotype a large set of cultivated carrot, wild carrot and other wild Daucus carota subspecies, primarily of European origin. Phylogenetic analysis indicated that eastern carrot may originate from Western Asia and western carrot may be selected from eastern carrot. Different wild D. carota subspecies may have contributed to the domestication of cultivated carrot. Genetic diversity was significantly reduced in western cultivars, probably through bottlenecks and selection. However, a high proportion of genetic diversity (more than 85% of the genetic diversity in wild populations) is currently retained in western cultivars. Model simulation indicated high and asymmetric gene flow from wild to cultivated carrots, spontaneously and/or by introgression breeding. Nevertheless, high genetic differentiation exists between cultivated and wild carrots (Fst =0.295) showing the strong effects of selection. Expression patterns differed radically for some genes between cultivated and wild carrot roots which may be related to changes in root traits. The up-regulation of water-channel-protein gene expression in cultivars might be involved in changing water content and transport in roots. The activated expression of carotenoid-binding-protein genes in cultivars could be related to the high carotenoid accumulation in roots. The silencing of allergen-protein-like genes in cultivated carrot roots suggested strong human selection to reduce allergy. These results suggest that regulatory changes of gene expressions may have played a predominant role in domestication. Conclusions - Western carrots may originate from eastern carrots. The reduction in genetic diversity in western cultivars due to domestication bottleneck/selection may have been offset by introgression from wild carrot. Differential gene expression patterns between cultivated and wild carrot roots may be a signature of strong selection for favorable cultivation traits.
Toxicity of Pyrrolizidine Alkaloids to Spodoptera exigua Using Insect Cell Lines and Injection Bioassays
Nuringtyas, T.R. ; Verpoorte, R. ; Klinkhamer, P.G.L. ; Oers, M.M. van; Leiss, K.A. - \ 2014
Journal of Chemical Ecology 40 (2014)6. - ISSN 0098-0331 - p. 609 - 616.
tertiary amine - n-oxides - performance - herbivores - resistance - asteraceae - vulgaris - hybrids - plants
Pyrrolizidine alkaloids (PAs) are feeding deterrents and toxic compounds to generalist herbivores. Among the PAs of Jacobaea vulgaris Gaertn, jacobine and erucifoline are the most effective against insect herbivores as indicated by correlative studies. Because little is known about the effect of jacobine and erucifoline as individual PAs, we isolated these compounds from their respective Jacobaea chemotypes. These PAs and other commercially available senecionine-like PAs, including senecionine, seneciphylline, retrorsine, and senkirkine, were tested as free base and N-oxide forms at a range of 0–70 ppm. Feeding bioassays using live insects are closer to the natural pattern but require relatively large amounts of test compounds. We, therefore, compared the toxicity of PAs using both Spodoptera exigua cell line and larval injection bioassays. Both bioassays led to similar results in the order of PA toxicity, indicating that the cell lines are a valuable tool for a first toxicity screen. Testing individual PAs, jacobine and erucifoline were the most toxic PAs, suggesting their major role in plant defense against generalist herbivores. Senkirkine and seneciphylline were less toxic than jacobine and erucifoline but more toxic than retrorsine. Senecionine was not toxic at the tested concentrations. For all toxic PAs, the free base form was more toxic than the N-oxide form. Our results demonstrate that structural variation of PAs influences their effectiveness in plant defense.
Pyrrolizidine Alkaloid Composition Influences Cinnabar Moth Oviposition Preferences in Jacobaea Hybrids
Cheng, D. ; Meijden, E. van der; Mulder, P.P.J. ; Vrieling, K. ; Klinkhamer, P.G.L. - \ 2013
Journal of Chemical Ecology 39 (2013)3. - ISSN 0098-0331 - p. 430 - 437.
host-plant choice - senecio-jacobaea - specialist herbivore - generalist herbivores - tyria-jacobaeae - chemical defense - evolution - hybridization - populations - performance
Plants produce a variety of secondary metabolites (PSMs) that may be selective against herbivores. Yet, specialist herbivores may use PSMs as cues for host recognition, oviposition, and feeding stimulation, or for their own defense against parasites and predators. This summarizes a dual role of PSMs: deter generalists but attract specialists. It is not clear yet whether specialist herbivores are a selective force in the evolution of PSM diversity. A prerequisite for such a selective force would be that the preference and/or performance of specialists is influenced by PSMs. To investigate these questions, we conducted an oviposition experiment with cinnabar moths (Tyria jacobaeae) and plants from an artificial hybrid family of Jacobaea vulgaris and Jacobaea aquatica. The cinnabar moth is a specialist herbivore of J. vulgaris and is adapted to pyrrolizidine alkaloids (PAs), defensive PSMs of these plants. The number of eggs and egg batches oviposited by the moths were dependent on plant genotype and positively correlated to concentrations of tertiary amines of jacobine-like PAs and some otosenine-like PAs. The other PAs did not correlate with oviposition preference. Results suggest that host plant PAs influence cinnabar moth oviposition preference, and that this insect is a potential selective factor against a high concentration of some individual PAs, especially those that are also involved in resistance against generalist herbivores
Cinnabar moth uses pyrrolizidine alkaloid composition and concentration as a cue for oviposition
Cheng, D. ; Meijden, E. van der; Mulder, P.P.J. ; Vrieling, K. ; Klinkhamer, P.G.L. - \ 2011
Leaf surface chemistry: the interface between herbivores and plants
Vrieling, K. ; Cheng, D. ; Mulder, P.P.J. ; Klinkhamer, P.G.L. - \ 2011
The genotype dependent presence of pyrrolizidine alkaloids as tertiary amine in jacobaea vulgaris
Joosten, L. ; Cheng, D. ; Mulder, P.P.J. ; Vrieling, K. ; Veen, J.A. van; Klinkhamer, P.G.L. - \ 2011
Phytochemistry 72 (2011)2-3. - ISSN 0031-9422 - p. 214 - 222.
senecio-jacobaea - n-oxides - root cultures - plants - insects - hybridization - biosynthesis - metabolism - herbivores - transport
Secondary metabolites such as pyrrolizidine alkaloids (PAs) play a crucial part in plant defense. PAs can occur in plants in two forms: tertiary amine (free base) and N-oxide. PA extraction and detection are of great importance for the understanding of the role of PAs as plant defense compounds, as the tertiary PA form is known for its stronger influence on several generalist insects, whereas the N-oxide form is claimed to be less deterrent. We measured PA N-oxides and their reduced tertiary amines by liquid chromatography–tandem mass spectrometry (LC-MS/MS). We show that the occurrence of tertiary PAs is not an artifact of the extraction and detection method. We found up to 50% of tertiary PAs in shoots of Jacobine – chemotype plants of Jacobaea vulgaris. Jacobine and its derivatives (jacoline, jaconine, jacozine and dehydrojaconine) may occur for more than 20% in reduced form in the shoots and more than 10% in the roots. For 22 PAs detected in F2 hybrids (J. vulgaris × Jacobaea aquatica), we calculate the tertiary amine percentage (TA% = the tertiary amine concentration/(tertiary amine concentration + the corresponding N-oxide concentration) × 100). We found that the TA% for various PAs was genotype-dependent. Furthermore, TA% for the different PAs were correlated and the highest correlations occurred between PAs which share high structural similarity. --------------------------------------------------------------------------------
The Relationship between Structurally Different Pyrrolizidine Alkaloids and Western Flower Thrips Resistance in F2 Hybrids of Jacobaea vulgaros and Jacobaea aquatica
Cheng, D. ; Kirk, H. ; Vrieling, K. ; Mulder, P.P.J. ; Klinkhamer, P.G.L. - \ 2011
Journal of Chemical Ecology 37 (2011)10. - ISSN 0098-0331 - p. 1071 - 1080.
senecio-jacobaea - n-oxide - hybridization - evolution - plants - asteraceae - biosynthesis - herbivores - responses - ecology
Segregating plant hybrids often have more ecological and molecular variability compared to parental species, and are therefore useful for studying relationships between different traits, and the adaptive significance of trait variation. Hybrid systems have been used to study the relationship between the expression of plant defense compounds and herbivore susceptibility. We conducted a western flower thrips (WFT) bioassay using a hybrid family and investigated the relationship between WFT resistance and pyrrolizidine alkaloid (PA) variation. The hybrid family consisted of two parental (Jacobaea vulgaris and Jacobaea aquatica) genotypes, two F1 genotypes, and 94 F2 hybrid lines. The J. aquatica genotype was more susceptible to thrips attack than the J. vulgaris genotype, the two F1 hybrids were as susceptible as J. aquatica, and susceptibility to WFT differed among F2 hybrid lines: 69 F2 lines were equally susceptible compared to J. aquatica, 10 F2 lines were more susceptible than J. aquatica and 15 F2 lines were as resistant as J. vulgaris or were intermediate to the two parental genotypes. Among 37 individual PAs that were derived from four structural groups (senecionine-, jacobine-, erucifoline- and otosenine-like PAs), the N-oxides of jacobine, jaconine, and jacoline were negatively correlated with feeding damage caused by WFT, and the tertiary amines of jacobine, jaconine, jacoline, and other PAs did not relate to feeding damage. Total PA concentration was negatively correlated with feeding damage. Among the four PA groups, only the total concentration of the jacobine-like PAs was negatively correlated with feeding damage. Multiple regression tests suggested that jacobine-like PAs play a greater role in WFT resistance than PAs from other structural groups. We found no evidence for synergistic effects of different PAs on WFT resistance. The relationship between PA variation and WFT feeding damage in the Jacobaea hybrids suggests a role for PAs in resistance to generalist insects.
Pyrrolizidine alkaloid variation in shoots and roots of segregating hybrids between Jacobaea vulgaris and Jacobaea aquatica
Cheng, D. ; Kirk, H. ; Mulder, P.P.J. ; Vrieling, K. ; Klinkhamer, P.G.L. - \ 2011
New Phytologist 192 (2011)4. - ISSN 0028-646X - p. 1010 - 1023.
senecionine n-oxide - british-isles - natural hybridization - plant hybridization - chemical diversity - tyria-jacobaeae - asteraceae - speciation - evolution - translocation
Hybridization can lead to novel qualitative or quantitative variation of secondary metabolite (SM) expression that can have ecological and evolutionary consequences.•We measured pyrrolizidine alkaloid (PA) expression in the shoots and roots of a family including one Jacobaea vulgaris genotype and one Jacobaea aquatica genotype (parental genotypes), two F1 hybrid genotypes, and 102 F2 hybrid genotypes using liquid chromatography–tandem mass spectrometry (LC-MS/MS).•We detected 37 PAs in the roots and shoots of J. vulgaris, J. aquatica and the hybrids. PA concentrations and compositions differed between genotypes, and between roots and shoots. Three otosenine-like PAs that only occurred in the shoots of parental genotypes were present in the roots of F2 hybrids; PA compositions were sometimes novel in F2 hybrids compared with parental genotypes, and in some cases transgressive PA expression occurred. We also found that PAs from within structural groups covaried both in the roots and in the shoots, and that PA expression was correlated between shoots and roots.•Considerable and novel variation present among F2 hybrids indicates that hybridization has a potential role in the evolution of PA diversity in the genus Jacobaea, and this hybrid system is useful for studying the genetic control of PA expression