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• W2000512853 abstract "Dear Editor, Phytohormones have been described as essential regulators of various processes throughout plant life, forming a strong interactive network. Because of this important function, they are central and integrative modulators forming a physiological key interface between plant responses and primary parameters such as genotype, environmental conditions, and developmental status. Consequently, the determination of the phytohormone signature as a key physiological parameter is necessary to understand the correlations between genotype and phenotype, as well as the influence of exogenous modulations on the phenotype (Yin et al., 2004Yin X. Struik P.C. Kropff M.J Role of crop physiology in predicting gene-to-phenotype relationships.Trends Plant Sci. 2004; 9: 426-432Abstract Full Text Full Text PDF PubMed Scopus (186) Google Scholar). Thus, evaluation of the phytohormone signature has to be considered for physiological phenotyping, especially for the improvement of crops or developing strategies for plant protection. This includes the important trait plant immunity, which is determined also by distinct and fine-tuned modulations of phytohormones (Robert-Seilaniantz et al., 2011Robert-Seilaniantz A. Grant M. Jones J.D.G Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism.Annu. Rev. Phytopathol. 2011; 49: 317-343Crossref PubMed Scopus (1261) Google Scholar). Ethylene, jasmonic (JA), and salicylic acid (SA) are well established as central stress signals to regulate defense responses. Other classic phytohormones such as abscisic acid (ABA) or auxin were only later recognized to interact with the central defense signaling backbone as additional regulators (Robert-Seilaniantz et al., 2011Robert-Seilaniantz A. Grant M. Jones J.D.G Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism.Annu. Rev. Phytopathol. 2011; 49: 317-343Crossref PubMed Scopus (1261) Google Scholar). Recently, we identified an important and novel role of cytokinins (CKs) to induce resistance against Pseudomonas syringae in tobacco (Großkinsky et al., 2011Großkinsky D.K. Naseem M. Abdelmohsen U.R. Plickert N. Engelke T. Griebel T. Zeier J. Novák O. Strnad M. Pfeifhofer H. et al.Cytokinins mediate resistance against Pseudomonas syringae in tobacco through increased antimicrobial phytoalexin synthesis independent of salicylic acid signaling.Plant Physiol. 2011; 157: 815-830Crossref PubMed Scopus (129) Google Scholar, Großkinsky et al., 2013Großkinsky D.K. Edelsbrunner K. Pfeifhofer H. van der Graaff E. Roitsch T. Cis- and trans-zeatin differentially modulate plant immunity.Plant Signal. Behav. 2013; 8: e24798Crossref PubMed Scopus (46) Google Scholar). The investigated CKs showed differential action on defense signaling components such as ABA (D.K. Großkinsky and T. Roitsch, unpublished results) and SA as well as on the formation of defense compounds such as phytoalexins (Großkinsky et al., 2011Großkinsky D.K. Naseem M. Abdelmohsen U.R. Plickert N. Engelke T. Griebel T. Zeier J. Novák O. Strnad M. Pfeifhofer H. et al.Cytokinins mediate resistance against Pseudomonas syringae in tobacco through increased antimicrobial phytoalexin synthesis independent of salicylic acid signaling.Plant Physiol. 2011; 157: 815-830Crossref PubMed Scopus (129) Google Scholar, Großkinsky et al., 2012bGroßkinsky D.K. van der Graaff E. Roitsch T. Phytoalexin transgenics in crop protection-fairy tale with a happy end?.Plant Sci. 2012; 195: 54-70Crossref PubMed Scopus (64) Google Scholar, Großkinsky et al., 2013Großkinsky D.K. Edelsbrunner K. Pfeifhofer H. van der Graaff E. Roitsch T. Cis- and trans-zeatin differentially modulate plant immunity.Plant Signal. Behav. 2013; 8: e24798Crossref PubMed Scopus (46) Google Scholar). Similar studies in other plant species regarding CKs as inducers of defense responses or as component of plant–pathogen interactions also indicated crosstalk with other phytohormones such as SA (Choi et al., 2010Choi J. Huh S.U. Kojima M. Sakakibara H. Paek K.-H. Hwang I. The cytokinin-activated transcription factor ARR2 promotes plant immunity via TGA/NPR1-dependent salicylic acid signaling in Arabidopsis.Dev. Cell. 2010; 19: 284-295Abstract Full Text Full Text PDF PubMed Scopus (290) Google Scholar; Argueso et al., 2012Argueso C.T. Ferreira F.J. Epple P. To J.P.C. Hutchison C.E. Schaller G.E. Dangl J.L. Kieber J.J Two-component elements mediate interactions between cytokinin and salicylic acid in plant immunity.PLoS Genet. 2012; 8: e1002448Crossref PubMed Scopus (156) Google Scholar; Jiang et al., 2013Jiang C.J. Shimono M. Sugano S. Kojima M. Liu X. Inoue H. Sakakibara H. Takatsuji H. Cytokinins act synergistically with salicylic acid to activate defense gene expression in rice.Mol. Plant Microbe Interact. 2013; 26: 287-296Crossref PubMed Scopus (114) Google Scholar). Thus, the complete network of phytohormones, notably including CKs, has to be considered to identify all regulatory mechanisms for spatiotemporal dynamics of defense reactions. Therefore, we developed an easy method for rapid phytohormone profiling that includes the following hormones and derivatives: ABA, indole-3-acetic acid (IAA), JA, SA, and the CKs cis-zeatin (cZ), dihydrozeatin (DHZ), dihydrozeatinriboside (DHZR), isopentenyladenine (iP), trans-zeatin (tZ), trans-zeatin-O-glucoside (tZOG), trans-zeatinriboside (tZR), and trans-zeatinriboside-O-glucoside (tZROG). Additionally, this method enabled the determination of certain phytoalexins (camalexin and scopoletin) in Arabidopsis thaliana and Nicotiana tabacum in the same extract. Because the importance of the inter-regulatory phytohormone network also becomes increasingly evident for other processes, we transferred this method to additional (crop) plant species and cell suspension cultures. This method enables establishment of the phytohormone signature and, thus, is a valuable tool for efficient physiological phenotyping allowing direct correlations between the determined phytohormone levels within one extract. The method set-up was based on previously published methods (Dobrev and Kamínek, 2002Dobrev P.I. Kamínek M. Fast and efficient separation of cytokinins from auxin and abscisic acid and their purification using mixed-mode solid-phase extraction.J. Chromatogr. A. 2002; 950: 21-29Crossref PubMed Scopus (477) Google Scholar; Albacete et al., 2008Albacete A. Ghanem M.E. Martínez-Andújar C. Acosta M. Sánchez-Bravo J. Martínez V. Lutts S. Dodd I.C. Pérez-Alfocea F. Hormonal changes in relation to biomass partitioning and shoot growth impairment in salinized tomato (Solanum lycopersicum L.) plants.J. Exp. Bot. 2008; 59: 4119-4131Crossref PubMed Scopus (334) Google Scholar; Forcat et al., 2008Forcat S. Bennett M.H. Mansfield J.W. Grant M.R A rapid and robust method for simultaneously measuring changes in the phytohormones ABA, JA and SA in plants following biotic and abiotic stress.Plant Methods. 2008; 4: 16Crossref PubMed Scopus (175) Google Scholar; Novák et al., 2008Novák O. Hauserová E. Amakorová P. Doležal K. Strnad M. Cytokinin profiling in plant tissues using ultra-performance liquid chromatography–electrospray tandem mass spectrometry.Phytochemistry. 2008; 69: 2214-2224Crossref PubMed Scopus (192) Google Scholar) with some modifications (Figure 1A): up to 250mg (FW) ground plant or cell culture material were mixed with 1.25ml 80% methanol. For phytohormone determination, 4 μl of internal standard (IS) mix (5 μg ml–1 in 80% methanol) composed of deuterium-labeled hormones (Supplemental Material and Methods) were added. To determine phytoalexins, 250 μl 6-fluoroindole-3-carboxyaldehyde (200 μg ml–1 in 80% methanol; Sigma-Aldrich, Steinheim/Germany) for camalexin (Loeffler et al., 2005Loeffler C. Berger S. Guy A. Durand T. Bringmann G. Dreyer M. von Rad U. Durner J. Mueller M.J B1-phytoprostanes trigger plant defense and detoxification responses.Plant Physiol. 2005; 137: 328-340Crossref PubMed Scopus (108) Google Scholar) and/or 50 μl 4-methylumbelliferone (40 μM in 75% ethanol; Sigma-Aldrich) for scopoletin (Sharan et al., 1998Sharan M. Taguchi G. Gonda K. Jouke T. Shimosaka M. Hayashida N. Okazaki M. Effects of methyl jasmonate and elicitor on the activation of phenylalanine ammonia-lyase and the accumulation of scopoletin and scopolin in tobacco cell cultures.Plant Sci. 1998; 132: 13-19Crossref Scopus (84) Google Scholar) were added as IS. Samples were thoroughly vortexed, incubated for 30min at 4°C, and centrifuged (20000 g, 4°C, 15min). Supernatants were passed through 80% methanol pre-equilibrated Chromafix C18 columns (Macherey-Nagel, Düren/Germany) and filtrates were collected on ice. Extraction was repeated with 1.25ml 80% methanol; second extracts were passed through the same columns. The combined extracts were concentrated to complete dryness using the Integrated SpeedVac® Concentrator System AES1000 (Savant Instruments Inc., Holbrook/USA). The residues were resolved in 500 or 1000 μl 20% methanol, sonicated for 8min, and passed through 0.2-μm syringe filters (Chromafil PES-20/25 or 0.45-μm Chromafil RC-45/25 filters in case of camalexin determination; Macherey-Nagel). Samples were collected in HPLC vials for analysis, and optionally stored at –80°C. Phytohormone analyses were performed using a UHPLC–MS/MS system consisting of a Thermo ACCELA pump (Thermo Scientific, Waltham/USA) coupled to a tempered HTC-PAL autosampler (CTC Analytics, Zwingen/Switzerland), and connected to a Thermo TSQ Quantum Access Max Mass Spectrometer (Thermo Scientific) with a heated electrospray ionization (HESI) interface. Single hormone standards (0.5, 0.1, 0.05, 0.01, 0.005 μg ml–1) and the IS mix (0.02 μg ml–1) were prepared in 80% methanol. 10 μl of each standard (for calibration) or sample were injected onto a Nucleoshell-PFP column (2.7 μm, 100×2mm; Macherey-Nagel) and eluted at a flow rate of 250 μl min–1. Mobile phases A consisting of water/methanol/acetic acid (89.5/10/0.5) and B consisting of methanol/acetic acid (99.5/0.5) were used for chromatographic separation. The elution consisted of 4min of 100% A and a linear gradient from 0% to 95% of B in 6min. 95% B was maintained for 6min, and afterwards the column was equilibrated with the starting composition (100% A) for 8min prior to each analytical run. The mass spectrometer was operated in the positive mode for all hormones analyzed, except ABA, JA, and SA (negative mode). Capillary spray voltage was set to 4000V, sheath gas pressure to 60 arbitrary units, auxiliary gas pressure to 20 arbitrary units, vaporizer temperature to 250°C, capillary temperature to 270°C, and the cycle time was 0.5 s. The chromatograms (for representative chromatograms, see Supplemental Figures 1 and 2) of each hormone (from standards and samples) were extracted and the peak area was quantified using the Thermo Xcalibur software (version 2.1.0). Analysis of the different substances via multiple reaction monitoring of ion pairs of IS and endogenous phytohormones was based on the specific mass transitions (Supplemental Material and Methods). General limits of detection (LOD) according to linear regression calculations (Shrivastava and Gupta, 2011Shrivastava A. Gupta V.B Methods for the determination of limit of detection and limit of quantification of the analytical methods.Chron. Young Sci. 2011; 2: 21-25Crossref Google Scholar) of two-fold dilution series (5–0.04ng ml–1) for the different phytohormone standards have been determined in the range of 0.02 for DZR and tZR, and 0.18ng ml–1 for IAA (Supplemental Figure 3 and Supplemental Table 1). LODs of individual samples however strongly depend on specific parameters (e.g. matrix) of the analyzed material. For all phytohormones, the linear range covers three to four orders of magnitude, determined by an extended two-fold dilutions series ranging from 160 to 0.001ng ml–1. Average recovery rates of phytohormones in a representative sample set ranged from 44.22% for IAA to 95.77% for tZROG (Supplemental Table 1). Phytoalexin analyses were performed using the HPLC system Ultimate 3000 (Dionex, Sunnyvale/USA) including a tempered autosampler unit (8°C). Camalexin (excitation of 318nm, emission of 370nm), scopoletin, and 4-methylumbelliferone (excitation of 350nm, emission of 430nm) were analyzed using a fluorescence detector, 6-fluoroindole-3-carboxyaldehyde (absorption at 280nm) via a UV detector. 10 μl of standard solutions and samples were loaded onto a Dionex Acclaim® 120 C18 reversed-phase column (5 μm, 4.6×250mm) and eluted at a flow rate of 1ml min–1. For camalexin analysis, mobile phases A consisting of methanol/water/acetic acid (50/49.9/0.1) and B consisting of methanol/acetic acid (99.9/0.1) were used for chromatographic separation. The elution consisted of a linear gradient from 0% to 100% of B in 15min. 100% B was maintained for 5min, and the column was equilibrated afterwards with 100% A for 9min prior to each analytical run. Under these conditions, the retention time of camalexin was around 11min and around 7.5min for 6-fluoroindole-3-carboxyaldehyde. For scopoletin analysis, mobile phases A consisting of water/acetonitrile/acetic acid (89.9/10/0.1) and B consisting of acetonitrile/acetic acid (99.9/0.1) were used for chromatographic separation. The elution consisted of a linear gradient from 10% to 50% of B in 20min. 50% B was maintained for 5min and the column was equilibrated afterwards with 90% A for 9min prior to each analytical run. Under these conditions, the retention time of scopoletin was around 10min and around 12min for 4-methylumbelliferone. Chromatograms were extracted, and the peak area was quantified using the Dionex Chromeleon® software (version 6.80). The combined determination of phytohormones and phytoalexins within the same extract was successfully applied to leaf material of A. thaliana and N. tabacum infected with virulent P. syringae pv. tomato DC3000 or pv. tabaci, respectively, as reported before (Supplemental Material and Methods; Großkinsky et al., 2012aGroßkinsky D.K. Koffler B.E. Roitsch T. Maier R. Zechmann B. Compartment specific antioxidative defense in Arabidopsis thaliana against virulent and avirulent Pseudomonas syringae.Phytopathology. 2012; 102: 662-673Crossref PubMed Scopus (37) Google Scholar). This clearly showed the expected pathogen-dependent/triggered accumulation of phytoalexins (Großkinsky et al., 2012bGroßkinsky D.K. van der Graaff E. Roitsch T. Phytoalexin transgenics in crop protection-fairy tale with a happy end?.Plant Sci. 2012; 195: 54-70Crossref PubMed Scopus (64) Google Scholar) as well as species specific differences in the accumulation of the different compounds (Figure 1B). Additionally, this method was successfully employed for physiological phenotyping in several plant species (A. thaliana, Beta vulgaris, Brassica napus, N. tabacum, and Solanum lycopersicum) and cultured cells (heterotrophic N. tabacum BY2 and S. lycopersicum, and mixotrophic A. thaliana). Results clearly indicate source (species) specific differences in the accumulation of the phytohormones analyzed (Figure 1C) as well as differences in phytohormone levels (e.g. SA) determined in infected tissue of A. thaliana and N. tabacum (Figure 1B). These data illustrate that this adapted method allows the parallel quantification of 12 phytohormones in one extract, is applicable to various plant materials (species, organs) generated under different conditions, and has potential to reveal biological effects such as the described impact of infections. Thus, the presented method enables direct correlations within the determined phytohormone spectrum as physiological key interface to modulate plant responses and relation to the examined process, which makes it a valuable tool for efficient physiological phenotyping. Supplementary Data are available at Molecular Plant Online. This work was supported by funding from the Society for the Advancement of Plant Sciences (Vienna, Austria) to D.K.G." @default.
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• W2000512853 title "A Rapid Phytohormone and Phytoalexin Screening Method for Physiological Phenotyping" @default.
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