Reduction of photosynthetic sensitivity in response to abiotic stress in tomato is mediated by a new generation plant activator
© Wargent et al.; licensee BioMed Central Ltd. 2013
Received: 9 December 2012
Accepted: 18 July 2013
Published: 30 July 2013
Yield losses as a result of abiotic stress factors present a significant challenge for the future of global food production. While breeding technologies provide potential to combat negative stress-mediated outcomes over time, interventions which act to prime plant tolerance to stress, via the use of phytohormone-based elicitors for example, could act as a valuable tool for crop protection. However, the translation of fundamental biology into functioning solution is often constrained by knowledge-gaps.
Photosynthetic and transcriptomic responses were characterised in young tomato (Solanum lycopersicum L.) seedlings in response to pre-treatment with a new plant health activator technology, ‘Alethea’, followed by a subsequent 100 mM salinity stress. Alethea is a novel proprietary technology composed of three key constituent compounds; the hitherto unexplored compound potassium dihydrojasmonate, an analogue of jasmonic acid; sodium benzoate, a carboxylic acid precursor to salicylic acid, and the α-amino acid L-arginine. Salinity treatment led to a maximal 47% reduction in net photosynthetic rate 8 d following NaCl treatment, yet in Alethea pre-treated seedlings, sensitivity to salinity stress was markedly reduced during the experimental period. Microarray analysis of leaf transcriptional responses showed that while salinity stress and Alethea individually impacted on largely non-overlapping, distinct groups of genes, Alethea pre-treatment substantially modified the response to salinity. Alethea affected the expression of genes related to biotic stress, ethylene signalling, cell wall synthesis, redox signalling and photosynthetic processes. Since Alethea had clear effects on photosynthesis/chloroplastic function at the physiological and molecular levels, we also investigated the ability of Alethea to protect various crop species against methyl viologen, a potent generator of oxidative stress in chloroplasts. Alethea pre-treatment produced dramatic reductions in visible foliar necrosis caused by methyl viologen compared with non-primed controls.
‘Alethea’ technology mediates positive recovery of abiotic stress-induced photosynthetic and foliar loss of performance, which is accompanied by altered transcriptional responses to stress.
KeywordsPhotosynthesis Abiotic stress Priming Tomato Transcriptomics Potassium dihydrojasmonate Sodium benzoate L-arginine
Plants are necessarily exposed to a variety of stresses throughout growth, many of which have a detrimental effect on growth and development. As a consequence, plants have evolved an equally wide variety of defence systems to minimise the negative impacts of stress. The development of technologies that exploit natural plant stress responses has never been of greater importance, as efforts are made to strengthen food crop provision for a growing global population in the face of current and future food supply insecurities [1, 2]. Threats to plant productivity are routinely imposed by biotic stresses such as herbivory and pathogenic disease [3, 4], but abiotic factors, such as temperature, drought and salinity stress, pose the greatest restriction on crop production . Although new genotypes provided by both conventional breeding and genetic modification technologies offer key steps forward, practical challenges still remain regarding the uptake and provision of breeding technologies . Enhancing our mechanistic understanding of plant responses to environmental stimuli in order to augment existing grower practices is therefore one important route to closing the perceived yield gap of global food crop production. Although active intervention to buffer consequential yield losses due to stress has always been an explicit component of food crop cultivation practice (e.g. the use of applied agro-chemical compounds), over time more sustainable approaches directly exploiting fundamental plant responses in crop species have been developed. These include, for example, the use of partial root-zone irrigation strategies to increase water use efficiency in crops such as maize and tomato [7, 8], or the early stage exposure of leafy vegetable crops to solar ultraviolet radiation to drive enhanced photoprotection and photosynthetic productivity .
Equally, there is currently marked opportunity to exploit those increasingly well-defined plant signalling responses to biotic stress in order to enhance plant tolerance. For example, the exploitation of non-pathogenic rhizobacteria for induced resistance against the necrotroph Botrytis cinerea has been successfully demonstrated in grapevine using mutant strains of Pseudomonas fluorescens and P. aeruginosa. Considering potential limitations in the application of a biotic agent to induce a desired state of enhanced plant stress protection, the use of chemical elicitors to mediate tolerance or resistance to biotic stress is increasingly receiving attention . For example, it is now well established that applications of the non-protein amino acid beta-aminobutyric acid (BABA) can enhance stress responses to a variety of stimuli including drought stress and disease infection [12, 13]. Despite such advances, large scale applications of ‘activator’ compounds often do not represent an economically viable option. ‘Alethea’ is a novel proprietary technology composed of three key constituent compounds; the hitherto unexplored compound potassium dihydrojasmonate (PDJ), an analogue of jasmonic acid (JA); sodium benzoate (SB), a carboxylic acid precursor to salicylic acid (SA), and the α-amino acid L-arginine (Arg) (Additional file 1). The roles of the jasmonate and salicylate groups of phytohormones have been the subject of extensive focus to date, principally with regard to cellular biosynthesis, transport and perception [14, 15], and particularly, the involvement of both groups in plant defence; [16–18]. Alethea is categorised as a ‘plant health regulator’ in the alleviation of abiotic plant stress, yet has not been the focus of any published studies to date. Knowledge of the capability of technologies such as Alethea in limiting the impact of abiotic stress, and elucidation of the mechanistic nature of any induced resistance to stress, might represent a step forward in the development of plant additives which could help reduce crop losses. In order to characterise the effects of Alethea on plant biology, we focussed first on stress caused by salinity. It has been estimated that around 8% of the world’s food crop productivity could be affected by elevated Na+ levels , via an often temporally separated combination of osmotic (rapid) and ionic (acute) effects on plant growth, including reductions in stomatal aperture and net photosynthetic rate , in addition to longer term consequences for shoot growth . The managed induction of enhanced plant tolerance to salinity has received some attention to date. For example, Jakab and colleagues  demonstrated reduced sensitivity to both salinity and drought stress following treatment of Arabidopsis seedlings with BABA, demonstrating an abscisic acid (ABA)-dependent response mediating protective effects. In addition, colonisation of Populus canescens with the ectomycorrhizal fungus Paxillus involutus led to increased accumulation of both ABA and SA under salinity stress , and previous studies have raised the possibility that JA-dependent processes may confer enhanced plant tolerance to salt-mediated effects .
Here, we investigated the impact of Alethea treatment in tomato plants under salinity stress. Photosynthetic and related plant gas exchange variables demonstrated a clear protective effect of Alethea, and our subsequent transcriptomics approach identified a number of genes responsive to Alethea application plus a modification of the salt stress response in the presence of Alethea. On the basis of the results, we extended our investigation to evaluate the protective effects of Alethea in response to another model photosynthetic stress, the reactive oxygen species-generating methyl viologen (paraquat). Alethea dramatically reduced the extent of necrosis in a number of key crop species following application of methyl viologen, indicating a general protection against oxidative stress by Alethea. This study provides further knowledge regarding responses to salinity stress at the transcriptome level, and confirms the potential for the use of a novel plant activator-based approach to crop protection.
Alethea regulates photosynthetic protection against salinity stress
Alethea drives transcriptional reprogramming and modifies the response to salinity
Enriched GO terms from the tomato function, process and component ontologies with P-value < = 0.05 (with permutation correction) for genes up- or down-regulated by salt or Alethea treatment
Gene Ontology term
Protease inhibitor activity
Two-component sensor activity
Acetylornithine deacetylase activity
Response to stimulus
Amino acid catabolic process
Negative regulation of abscisic acid mediated signaling
Nitrogen compound catabolic process
Xyloglucan:xyloglucosyl transferase activity
Structural constituent of cell wall
Delta12-fatty acid dehydrogenase activity
Omega-6 fatty acid desaturase activity
Glucan metabolic process
Cell wall organization
Cellular carbohydrate metabolic process
Acetyl-coA C-acyltransferase activity
Flavonoid 3’,5’-hydroxylase activity
Response to biotic stimulus
Response to stress
MapMan revealed significant effects of salinity over a wider range of processes. In the absence of Alethea, the most significant effect was on protein turnover, with protein synthesis being down-regulated along with a concomitant up-regulation of genes involved in protein degradation. Several classes of transcriptional regulators were also induced, whilst arabinogalactan proteins (AGPs) and cell wall-modifying enzymes were down-regulated. In Alethea-treated plants, the overall response to salinity was broadly similar. However, the responses of several categories of genes appeared to be attenuated, whereas some responses were enhanced. For example, Alethea pre-treatment reduced salt-induced changes in genes involved in protein turnover, whilst changes in cell wall genes were enhanced. Furthermore, some classes of genes appeared to be significantly altered by salinity only in control plants or only following Alethea pre-treatment. For example, salt-induced changes in genes related to lipid metabolism, lignin and wax metabolism, and various transcription factor families were significant only in the absence of Alethea, whereas carotenoid metabolic genes were induced only in Alethea-treated plants. Overall, the main impression is that salinity and Alethea affect different but overlapping patterns of gene expression, and that the salt stress response is substantially reduced following Alethea pre-treatment.
Protection of photosynthetic capability mediated by Alethea is wide-ranging
Alethea provides protection to the photosynthetic apparatus of a range of cultivated species
Foliar damage (% necrosis)
Con + H2O
0.42 ± 0.15a
0.00 ± 0.00a
0.08 ± 0.07a
0.17 ± 0.11a
AL + H2O
0.58 ± 0.15a
0.00 ± 0.00a
0.00 ± 0.00a
0.42 ± 0.15a
Con + MV
62.08 ± 6.38c
75.00 ± 3.20c
70.33 ± 7.90c
74.75 ± 3.95b
AL + MV
23.75 ± 2.05b
12.33 ± 1.79b
34.00 ± 4.16b
4.50 ± 0.81a
Nevertheless, our microarray analysis identifies possible mechanisms underlying the protective effect of Alethea. Firstly, it is clear that rather than acting simply to enhance the existing transcriptional response to salinity, Alethea treatment generated significant changes in transcription prior to the application of salt stress, and some of these may impact on the subsequent ability of the plant to tolerate salinity. Notably, MapMan and GO term enrichment analysis both identified various defence/stress associated processes as being regulated by Alethea, which may contribute to increased tolerance. These include up-regulation of ethylene signalling and stress-associated transcription factors. Ethylene is important in a range of responses to abiotic stress, including salinity . Secondly, it is also clear from the microarray data that the response to salinity is substantially affected by Alethea pre-treatment. For a number of individual genes (Figure 2; clusters 3, 5 and 8), the response to salinity is attenuated by Alethea pre-treatment, whereas for other genes (Figure 2; clusters 2 and 9), there are additive affects of salinity and Alethea which could contribute to enhanced stress tolerance. At the biological process level, as revealed by MapMan analysis, Alethea appears to augment the overall response of cell wall proteins to salt, with a number of arabinogalactan proteins (AGPs), xyloglucan endotransglycosylases (XETs) and expansins being down-regulated, consistent with a reduction in cell expansion and growth. Curiously though, Alethea treatment alone up-regulates expression of several XETs and expansins (Figure 5; cell wall modification). Previous studies have also highlighted the importance of modifications to cell wall structure in the response to salinity [50, 51] and cell wall-related genes were strongly regulated by salt stress in tomato roots . Since some of these classes of cell-wall genes were already altered by Alethea pre-treatment, this along with the enhanced affect upon subsequent salinity treatment may contribute to enhanced tolerance.
One of the key impacts of abiotic stress in plants is oxidative stress, resulting from over-reduction of the photosynthetic electron transport system by reduced CO2 availability associated with stomatal closure. Stomatal conductance was reduced by salinity in both control and Alethea-treated plants in our experiments (Figure 1). Under such conditions, photo-oxidative stress is minimised by the utilisation of alternative electron transport systems in chloroplasts. One such mechanism is the reduction of NAD(P)H by the plastidial NDH complex [30–32]. Statistical analysis in MapMan revealed that genes of the light reactions of photosynthesis were significantly affected by Alethea, and close inspection of these genes revealed four NDH subunit genes that were up-regulated by Alethea. NDH activity is increased under a range of stress conditions [30, 32] and Horváth et al.,  found that a loss-of-function NDH mutation in tobacco caused increased photosynthetic depression when CO2 supply was limited by stomatal closure. Hence, increased NDH expression following Alethea treatment may contribute to the protection of photosynthesis upon subsequent salt stress.
While there is a growing body of evidence to indicate the dynamic and complex nature of plant phytohormone interactions in planta, fewer studies to date have provided a feasible application for incorporation of novel fundamental knowledge regarding plant activation for stress tolerance into a likely agronomic solution. Although the ‘Alethea’ technology is composed of several biologically active constituents, the end result mediates positive recovery of abiotic stress-induced photosynthetic and foliar loss of performance, based on an additive and complementary breadth of responses at the transcriptome level. Building fundamental understanding of the interactions between component compounds will be a valuable future step forward, and will further empower the buffering of food crop cultivation against intolerable losses in yield.
Plant propagation and growing conditions
Tomato seed (cv. Ailsa Craig, Moles Seeds Ltd, Colchester, UK) were sown and germinated in Levington M3 compost (Henry Alty Ltd., Preston, UK), prior to individual transplantation into 2 L pots. Seedlings were maintained in glasshouse conditions supplemented with high pressure sodium lighting, supplying a background Photosynthetically Active Radiation (PAR) photon flux density of approximately 500 μmol m-2 s-1, with a photoperiod of 14 h/10 h light/dark, and air temperatures of 22°C/18°C day/night. Plants were arranged randomly according to treatment, and were grown for four weeks prior to establishment of experimental treatments (approximately 6th true leaf stage). For the methyl viologen assays, tomato was propagated as above; wheat (Triticum aestivum L.cv Granary, Quantil Ltd., Lancashire, UK), dwarf French bean (Phaseolus vulgaris cv. Nassau, Moles Seeds Ltd. Essex, UK) and maize (Zea mays cv. F1 Earligold, Moles Seeds Ltd. Essex, UK) seed were pre-germinated in dishes lined with paper towel which had been soaked in water, covered and then placed into the glasshouse under the same conditions as described above. After three days viable seeds were then selected and sown into individual pots. Bean seeds were sown into standard 13 x 14 cm pots whereas the maize and wheat were sown into 11 x 13.5 cm pots all using Levington M3 compost. For Brassica napus (L. cv Expert, Limagrain Ltd., Lincolnshire, UK) several seeds were sown into standard 13 cm pots as above, with seedlings thinned to single plants in each pot following emergence. Wheat, bean, maize and brassica plants were grown for 3.5 weeks before receiving any treatment.
Pre-treatment of tomato plants with Alethea compound and salinity stress
An experimental formula of the ‘Alethea’ technology (Plant Impact PLC, Harpenden, UK) was applied to four-week old tomato seedlings at a concentration of 99:1 v/v (distilled H2O:Alethea) as per manufacturer’s instructions (see Additional file 1 for a detailed description of the Alethea formulation), in addition to an equal quantity of control plants, which were sprayed with distilled H2O. Alethea solution was sprayed onto leaves until run-off using a pressurized airbrush, plants were air-dried and then returned to the glasshouse. 24 h following Alethea application, a salinity treatment of 100 mM NaCl (Sigma-Aldrich Ltd., Dorset, UK) was applied to plants via pot-watering until maximum soil saturation was reached (~ 3 h), with control plants fed with H2O only. Both Alethea and salinity treatments were then repeated exactly as before 5 d following original treatment days (Day 4 = Alethea, Day 5 = salinity), with plants watered with H2O only on all other days in order to replace transpirational losses. For the methyl viologen assays, due to the waxy composition of the brassica leaves and vertical structure of the maize leaves, a wetting agent (Silwet L-77; De Sangosse Ltd., Cambridge, UK), was added (0.025% concentration) to the Alethea solution (and water control) when being applied to the plants, allowing the treatment to be applied evenly across the whole plant.
Measurement of gas exchange parameters
Net photosynthesis and related gas exchange variables were measured using a portable infrared gas analysis system (CIRAS-2; PP systems, Hitchin, UK) with cuvette conditions set to PAR: 500 mmol m-2 s-1, 60% relative humidity and 380 ppm CO2, with leaves left to equilibrate for 5 min prior to measurement. Measurements were made using 3rd true leaves and were taken daily prior to and during initial Alethea and salinity treatments, and every 48 h thereafter. Ten plants were measured per treatment in a single experiment.
24 h following salinity treatment (48 h following Alethea treatment), 3rd true leaves of plants were snap frozen in liquid N2. Leaves were sampled from three plants per treatment, and the experiment was carried out on three separate occasions. RNA was then extracted using a scaled-up version of the method described by  and purified using the Qiagen RNeasy kit, as per manufacturers’ instructions (Qiagen; http://www.qiagen.com). Labelling and hybridization to the Affymetrix GeneChip® Tomato Genome Array were performed at the Nottingham Arabidopsis Stock Centre (University of Nottingham, UK; http://www.arabidopsis.info).
Microarray data analysis and bioinformatics
Raw data were normalised using GCRMA  and the data were filtered to eliminate probe sets for which the mean signal from the three replicate arrays did not exceed a value of 10 (log2 = 3.2) for at least one treatment. This resulted in the inclusion of 7,799 probe sets for further analysis from the original 10,209 probe sets on the array. Differentially-expressed genes were identified using the Rank Product algorithm  implemented in the Multiple Experiment Viewer package . We used 2-class paired comparisons with P-values calculated using 1000 random permutations of the data, and false detection rate of 0.05 used as a cut-off. Hiercarchical clustering  was performed in the D-Chip package using the correlation distance metric and average linkage . For analysis using MapMan , mean log2 fold-change values for all 7,799 probe sets included in our original analysis were used for display and statistical testing using the Wilcoxon rank sum test. The Benjamini and Hochberg correction was applied to statistical tests in MapMan to take account of multiple hypothesis testing. Probe annotation and gene ontology (GO) term enrichment analysis were performed using the tools provided by the Tomato Functional Genomics Database . P-values were corrected using the permutation algorithm within the analysis tool. Annotation files were the January 2010 versions.
Gene expression analysis by RT-PCR
Following RNA extraction as outlined above and prior to cDNA synthesis, 10 μg RNA was treated with DNaseI (Invitrogen; http://www.invitrogen.com). cDNA was synthesized using SuperScript II reverse transcriptase (Invitrogen) using the primer GGCCACGCGTCGACTAGTAC(T)16VN. 30 cycles of PCR were carried out using Taq DNA polymerase (REDTaq; Sigma-Aldrich).
Methyl viologen assay
Alethea pre-treatment was applied to tomato plants at 4.5 weeks, and wheat, maize, bean and brassica plants at 3.5 weeks (as detailed above) 24 h prior to the application of 500 μM methyl viologen (Sigma-Aldrich Ltd., Dorset, UK). MV was applied using a pressurized airbrush, and Silwet L-77 (De Sangosse Ltd., Cambridge, UK), a wetting agent, was added when applying the herbicide to maize and brassica plants to provide even application across the leaves. Control plants were treated with 0 μM MV (water) using the same method, and brassica and maize control plants received 0 μM MV (water) plus Silwet L-77 (0.025%). Once sprayed, plants were returned to the glasshouse and supplementary lighting switched off until the treatments had dried onto the leaves. 3 d after MV application, necrosis on the leaf surfaces was estimated visually as a percentage of the whole plant. Each species was subject to a minimum of two separate MV experiments, with the exception of tomato, which was assayed in four separate experiments.
We are grateful to Plant Impact PLC for funding this work with a research grant to NP and MR, and to the Biotechnology and Biological Sciences Research Council (UK) for a CASE studentship awarded to DP.
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