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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.
Strigolactone levels in dicot roots are determined by an ancestral symbiosis-regulated clade of the PHYTOENE SYNTHASE gene family
Stauder, Ron ; Welsch, Ralf ; Camagna, Maurizio ; Kohlen, Wouter ; Balcke, Gerd U. ; Tissier, Alain ; Walter, Michael H. - \ 2018
Frontiers in Plant Science 9 (2018). - ISSN 1664-462X
Apocarotenoids - Arbuscular mycorrhiza - Carotenoids - Medicago truncatula - Solanum lycopersicum - Strigolactones - Symbiosis
Strigolactones (SLs) are apocarotenoid phytohormones synthesized from carotenoid precursors. They are produced most abundantly in roots for exudation into the rhizosphere to cope with mineral nutrient starvation through support of root symbionts. Abscisic acid (ABA) is another apocarotenoid phytohormone synthesized in roots, which is involved in responses to abiotic stress. Typically low carotenoid levels in roots raise the issue of precursor supply for the biosynthesis of these two apocarotenoids in this organ. Increased ABA levels upon abiotic stress in Poaceae roots are known to be supported by a particular isoform of phytoene synthase (PSY), catalyzing the rate-limiting step in carotenogenesis. Here we report on novel PSY3 isogenes from Medicago truncatula (MtPSY3) and Solanum lycopersicum (SlPSY3) strongly expressed exclusively upon root interaction with symbiotic arbuscular mycorrhizal (AM) fungi and moderately in response to phosphate starvation. They belong to a widespread clade of conserved PSYs restricted to dicots (dPSY3) distinct from the Poaceae-PSY3s involved in ABA formation. An ancient origin of dPSY3s and a potential co-evolution with the AM symbiosis is discussed in the context of PSY evolution. Knockdown of MtPSY3 in hairy roots of M. truncatula strongly reduced SL and AM-induced C13 α-ionol/C14 mycorradicin apocarotenoids. Inhibition of the reaction subsequent to phytoene synthesis revealed strongly elevated levels of phytoene indicating induced flux through the carotenoid pathway in roots upon mycorrhization. dPSY3 isogenes are coregulated with upstream isogenes and downstream carotenoid cleavage steps toward SLs (D27, CCD7, CCD8) suggesting a combined carotenoid/apocarotenoid pathway, which provides “just in time”-delivery of precursors for apocarotenoid formation.
Short-term salt stress strongly affects dynamic photosynthesis, but not steady-state photosynthesis, in tomato (Solanum lycopersicum)
Zhang, Yuqi ; Kaiser, Elias ; Zhang, Yating ; Yang, Qichang ; Li, Tao - \ 2018
Environmental and Experimental Botany 149 (2018). - ISSN 0098-8472 - p. 109 - 119.
Dynamic photosynthesis - Fluctuating light - Salt stress - Solanum lycopersicum - Stomatal conductance - Tomato
Salt stress occurs worldwide due to widespread soil salinization. Also, plants are often subjected to rapidly alternating periods of sun and shade (sunflecks). Despite this combined occurrence of salt stress and sunflecks, dynamic photosynthetic responses to sunflecks under salt stress remain unknown. This study addresses this discrepancy by exploring photosynthetic gas exchange and chlorophyll fluorescence, both after dark-light transitions and during artificial light fluctuations (lightflecks and shadeflecks), in salt stressed leaves. Three weeks old growth-chamber grown tomato (Solanum lycopersicum Mill ‘Beijing Cherry Tomato’) plants were exposed to 0, 70 or 140 mM of sodium chloride (NaCl), for 7–9 days. Photosynthetic induction after dark-light transitions was strongly inhibited in salt-stressed leaves, due to increased transient stomatal limitation and slower apparent Rubisco activation. During photosynthetic induction, non-photochemical quenching (NPQ) and intrinsic water use efficiency (WUEi) were positively correlated with [NaCl]. Under periods of low light (shadeflecks), the longer the shadefleck lasted, the more strongly photosynthesis after re-illumination was downregulated by salt stress, and this downregulation in photosynthesis was positively correlated with the severity of salt stress. Under regularly applied lightflecks, salt stress decreased photosynthesis by 12–42%, which was mainly caused by decreased stomatal conductance. Salt-stressed leaves also displayed significantly lower stomatal pore area and stomatal index. Crucially, salt stress did not affect steady-state photosynthetic capacity as indicated by similar light and CO2 response curves of photosynthesis. We conclude that a short-term salt stress strongly affects dynamic leaf photosynthesis in tomato while its effect on steady state photosynthesis is negligible.
Metabolomic analysis of tomato seed germination
Kazmi, Rashid H. ; Willems, Leo A.J. ; Joosen, Ronny V.L. ; Khan, Noorullah ; Ligterink, Wilco ; Hilhorst, Henk W.M. - \ 2017
Metabolomics 13 (2017)12. - ISSN 1573-3882 - 17 p.
Canonical correlation analysis (CCA) - GC-TOF/MS - Generalized genetical genomics (GGG) - Metabolomics - mQTL analysis - Seed performance - Solanum lycopersicum - Solanum pimpinellifolium - Tomato
Introduction: Seed germination is inherently related to seed metabolism, which changes throughout its maturation, desiccation and germination processes. The metabolite content of a seed and its ability to germinate are determined by underlying genetic architecture and environmental effects during development. Objective: This study aimed to assess an integrative approach to explore genetics modulating seed metabolism in different developmental stages and the link between seed metabolic- and germination traits. Methods: We have utilized gas chromatography-time-of-flight/mass spectrometry (GC-TOF/MS) metabolite profiling to characterize tomato seeds during dry and imbibed stages. We describe, for the first time in tomato, the use of a so-called generalized genetical genomics (GGG) model to study the interaction between genetics, environment and seed metabolism using 100 tomato recombinant inbred lines (RILs) derived from a cross between Solanum lycopersicum and Solanum pimpinellifolium. Results: QTLs were found for over two-thirds of the metabolites within several QTL hotspots. The transition from dry to 6 h imbibed seeds was associated with programmed metabolic switches. Significant correlations varied among individual metabolites and the obtained clusters were significantly enriched for metabolites involved in specific biochemical pathways. Conclusions: Extensive genetic variation in metabolite abundance was uncovered. Numerous identified genetic regions that coordinate groups of metabolites were detected and these will contain plausible candidate genes. The combined analysis of germination phenotypes and metabolite profiles provides a strong indication for the hypothesis that metabolic composition is related to germination phenotypes and thus to seed performance.
Parameter estimation in tree graph metabolic networks
Astola, Laura ; Stigter, Hans ; Gomez Roldan, Maria Victoria ; Eeuwijk, Fred van; Hall, Robert D. ; Groenenboom, Marian ; Molenaar, Jaap J. - \ 2016
PeerJ 2016 (2016)9. - ISSN 2167-8359
Glycosylation - Kinetic models - Metabolic networks - Network inference - Solanum lycopersicum - Systems biology
We study the glycosylation processes that convert initially toxic substrates to nu- tritionally valuable metabolites in the flavonoid biosynthesis pathway of tomato (Solanum lycopersicum) seedlings. To estimate the reaction rates we use ordinary differential equations (ODEs) to model the enzyme kinetics. A popular choice is to use a system of linear ODEs with constant kinetic rates or to use Michaelis-Menten kinetics. In reality, the catalytic rates, which are affected among other factors by kinetic constants and enzyme concentrations, are changing in time and with the approaches just mentioned, this phenomenon cannot be described. Another problem is that, in general these kinetic coefficients are not always identifiable. A third problem is that, it is not precisely known which enzymes are catalyzing the observed glycosylation processes. With several hundred potential gene candidates, experimental validation using purified target proteins is expensive and time consuming. We aim at reducing this task via mathematical modeling to allow for the pre-selection of most potential gene candidates. In this article we discuss a fast and relatively simple approach to estimate time varying kinetic rates, with three favorable properties: firstly, it allows for identifiable estimation of time dependent parameters in networks with a tree- like structure. Secondly, it is relatively fast compared to usually applied methods that estimate the model derivatives together with the network parameters. Thirdly, by combining the metabolite concentration data with a corresponding microarray data, it can help in detecting the genes related to the enzymatic processes. By comparing the estimated time dynamics of the catalytic rates with time series gene expression data we may assess potential candidate genes behind enzymatic reactions. As an example, we show how to apply this method to select prominent glycosyltransferase genes in tomato seedlings.
Knocking down expression of the auxin-amidohydrolase IAR3 alters defense responses in Solanaceae family plants
Ippolito, Sebastian D'; Vankova, Radomira ; Joosten, Matthieu H.A.J. ; Casalongué, Claudia A. ; Fiol, Diego F. - \ 2016
Plant Science 253 (2016). - ISSN 0168-9452 - p. 31 - 39.
Auxin - Biotic stress - Cladosporium fulvum - Indole-3-acetic acid amido hydrolases - Nicotiana benthamiana - Phytophthora infestans - Solanum lycopersicum
In plants, indole-3-acetic acid (IAA) amido hydrolases (AHs) participate in auxin homeostasis by releasing free IAA from IAA-amino acid conjugates. We investigated the role of IAR3, a member of the IAA amido hydrolase family, in the response of Solanaceous plants challenged by biotrophic and hemi-biotrophic pathogens. By means of genome inspection and phylogenic analysis we firstly identified IAA-AH sequences and putative IAR3 orthologs in Nicotiana benthamiana, tomato and potato. We evaluated the involvement of IAR3 genes in defense responses by using virus-induced gene silencing. We observed that N. benthamiana and tomato plants with knocked-down expression of IAR3 genes contained lower levels of free IAA and presented altered responses to pathogen attack, including enhanced basal defenses and higher tolerance to infection in susceptible plants. We showed that IAR3 genes are consistently up-regulated in N. benthamiana and tomato upon inoculation with Phytophthora infestans and Cladosporium fulvum respectively. However, IAR3 expression decreased significantly when hypersensitive response was triggered in transgenic tomato plants coexpressing the Cf-4 resistance gene and the avirulence factor Avr4. Altogether, our results indicate that changes in IAR3 expression lead to alteration in auxin homeostasis that ultimately affects plant defense responses.
Cladosporium fulvum Effectors : Weapons in the Arms Race with Tomato
Wit, Pierre J.G.M. de - \ 2016
Annual Review of Phytopathology 54 (2016). - ISSN 0066-4286 - p. 1 - 23.
(hemi)biotroph - arms race - avirulence genes - Cf resistance genes - Cladosporium fulvum - Dothideomycetes - effector genes - extracellular pathogens - Solanum lycopersicum
In this review, I recount my personal history. My drive to study host-pathogen interactions was to find alternatives for agrochemicals, which was triggered after reading the book "Silent Spring" by Rachel Carson. I reflect on my research at the Laboratory of Phytopathology at Wageningen University, where I have worked for my entire career on the interaction between Cladosporium fulvum and tomato, and related gene-for-gene pathosystems. I describe different methods used to identify and sequence avirulence (Avr) genes from the pathogen and resistance (R) genes from the host. The major genes involved in classical gene-for-gene interactions have now been identified, and breeders can produce plants with multiple R genes providing durable and environmentally safe protection against pathogens. In some cases, this might require the use of genetically modified plants when R genes cannot be introduced by classical breeding.
The effect of light intensity and duration on Vitamin C concentration in tomato fruits
Verkerke, W. ; Labrie, C. ; Dueck, T. - \ 2015
Acta Horticulturae 1106 (2015). - ISSN 0567-7572 - p. 49 - 53.
Artificial lighting - Ascorbic acid - Fruit quality - Health related phytochemicals secondary metabolites - Led - Solanum lycopersicum
Increasing health related phytochemicals (HRP) in fruits may create an added value for consumers. We are currently developing greenhouse cultivation protocols for growers to fine tune plant growth and create products with higher amounts of HRP. Tomato (Solanum lycopersicum) greenhouse experiments were carried out to investigate the effect of light intensity and light quality on HRP during the growing period. Vitamin C concentration of different tomato cultivars was increased in a model growing system with red and blue light-emitting diodes (LEDs), increasing logarithmically with increasing radiation. At moderate light intensities of 140, 200 and 285 μmol m-2 s-1 and a light sum of 10-30 mol day-1, the Vitamin C concentration increased by 65% in comparison to the controls. The light sum is best applied at low intensity for a longer period (20 h) than at higher intensities for a shorter period (14 h). The total amount of antioxidants, estimated as oxygen radical absorbance capacity (ORAC) values, also increased. With these results, practical cultivation systems can be developed to increase the Vitamin C concentration, enabling growers to give their products an added value.
Linking 'generativity' to crop properties of indeterminate growing tomatoes by principal component analysis
Scheepens, D. ; Schepers, H.E. ; Kooten, O. Van - \ 2015
Acta Horticulturae 1107 (2015). - ISSN 0567-7572 - p. 181 - 186.
Crop condition - Grower - Multivariate analysis - Plant balance - Solanum lycopersicum
'Generativity' and 'strength' are elusive concepts. They are in the daily vocabulary of growers, but objective determination and quantification is hard. Therefore they are avoided in science. The incorporation of 'generativity' and 'strength' into the vocabulary of science will increase the understandability of scientific results to growers, and open possibilities for applied research questions. Here we propose a multivariate approach. A tomato crop was monitored with observations that are common in tomato cultivation. The measurements included stem diameter, leaf length, length growth of the stem, harvested fruit weight and brix. A principal component analysis was performed on the plant observations to find out whether the principal components can be linked to the crop attributes 'generativity' and 'strength'. To create a difference in 'generativity' two different irrigation regimes and two different leaf pruning regimes were applied. This article presents a proof of principle. We demonstrate that a multivariate analysis can be used to visualize the crop condition in a way that is recognizable for growers. This opens the possibility for quantification of 'generativity' and 'strength'.
Microarray analysis of developing fruits from transgenic lines with increased or reduced SlARF9 mRNA levels in tomato.
Jong, Maaike de; Wolters-Arts, Mieke ; Schimmel, Bernardus C. ; Stultiens, Catharina L. ; Groot, Peter F. de; Powers, Stephen J. ; Tikunov, Yury ; Bovy, Arnaud ; Mariani, Celestina ; Vriezen, Wim H. ; Rieu, Ivo - \ 2014
Solanum lycopersicum - GSE63637 - PRJNA268511
The transformation of the ovary into a fruit after successful completion of pollination and fertilization has been associated with many changes at transcriptomic level. These changes are part of a dynamic and complex regulatory network that is controlled by phytohormones, with a major role for auxin. One of the auxin-related genes differentially expressed upon fruit set and early tomato fruit development is Solanum lycopersicum ARF9 (SlARF9). To explore the physiological role of SlARF9 in tomato fruit set and development, we generated transgenic tomato lines in which the gene was overexpressed or silenced, and used microarray analysis to identify possible transcriptomic changes associated with the fruit developmental phenotypes observed in the transgenic lines.
Gene expression in three stages of ripening tomato fruit
Maagd, R.A. de; Bovy, A.G. - \ 2013
Solanum lycopersicum - GSE42783 - PRJNA183126
Gene expression in three stages of ripening tomato fruit (variety Ailsa Craig) was determined with the EUTOM3 Affymetrix array in order to compare with degradrome sequencing data from study GSE42661, treated as RNAseq.
Identification of microRNA targets in tomato fruit development using high-throughput sequencing and degradome analysis
Maagd, R.A. de; Karlova, R.B. ; Haarst, J.C. van - \ 2013
Solanum lycopersicum - GSE42661 - PRJNA182523
By using parallel analysis of RNA ends (PARE) for global identification of miRNA targets and comparing four different stages of tomato fruit development we identified a large number of target genes of miRNAs. PARE libraries were produced, one each, for tomato fruits at 5 days after pollination, mature green fruit, Breaker fruit, and 7 days after Breaker stge fruits
Comparison of tomato fruit gene expression data obtained by microarray analysis and by treatment of degradome sequencing data as an RNAseq experiment
Maagd, R.A. de - \ 2013
Solanum lycopersicum - GSE42784 - PRJNA183125
Non-coding RNA profiling by high throughput sequencing Expression profiling by array
Comparison of gene expression between wild type and FUL1/2 knockdown tomato fruits
Bemer, M. ; Karlova, R.B. ; Maagd, R.A. de - \ 2012
Solanum lycopersicum - GSE41560 - PRJNA177429
We compared gene expression by microarray analysis between wild type and transgenic sibling progeny from two primary transgenic lines containing a construct for knocking down expression of both tomato fruitfull orthologs, FUL1/TDR4 and FUL2/MBP7.