, Volume 249, Issue 5, pp 1417–1433 | Cite as

Distinctive phytohormonal and metabolic profiles of Arabidopsis thaliana and Eutrema salsugineum under similar soil drying

  • Carla PinheiroEmail author
  • Elizabeth Dickinson
  • Andrew Marriott
  • Isa C. Ribeiro
  • Marta Pintó-Marijuan
  • Carla António
  • Olfa Zarrouk
  • Maria Manuela Chaves
  • Ian C. Dodd
  • Sergi Munné-Bosch
  • Jane Thomas-Oates
  • Julie WilsonEmail author
Original Article


Main conclusions

Arabidopsis and Eutrema show similar stomatal sensitivity to drying soil. In Arabidopsis, larger metabolic adjustments than in Eutrema occurred, with considerable differences in the phytohormonal responses of the two species.

Although plants respond to soil drying via a series of concurrent physiological and molecular events, drought tolerance differs greatly within the plant kingdom. While Eutrema salsugineum (formerly Thellungiella salsuginea) is regarded as more stress tolerant than its close relative Arabidopsis thaliana, their responses to soil water deficit have not previously been directly compared. To ensure a similar rate of soil drying for the two species, daily soil water depletion was controlled to 5–10% of the soil water content. While partial stomatal closure occurred earlier in Arabidopsis (Day 4) than Eutrema (from Day 6 onwards), thereafter both species showed similar stomatal sensitivity to drying soil. However, both targeted and untargeted metabolite analysis revealed greater response to drought in Arabidopsis than Eutrema. Early peaks in foliar phytohormone concentrations and different sugar profiles between species were accompanied by opposing patterns in the bioactive cytokinin profiles. Untargeted analysis showed greater metabolic adjustment in Arabidopsis with more statistically significant changes in both early and severe drought stress. The distinct metabolic responses of each species during early drought, which occurred prior to leaf water status declining, seemed independent of later stomatal closure in response to drought. The two species also showed distinct water usage, with earlier reduction in water consumption in Eutrema (Day 3) than Arabidopsis (Day 6), likely reflecting temporal differences in growth responses. We propose Arabidopsis as a promising model to evaluate the mechanisms responsible for stress-induced growth inhibition under the mild/moderate soil drying that crop plants are typically exposed to.


Bioactive cytokinins Drought resilience Metabolite profiles Redox state Rewatering Stomatal conductance Unsupervised multivariate analysis 



2-Isopentenyl adenine


1-Amino-cyclopropane-1-carboxyic acid


Ascorbate (reduced)








Isopentenyl adenosine


Jasmonic acid


Principal component analysis




Trans-zeatin riboside


Relative water content


Salicylic acid


Soil water content



Eutrema seeds were kindly donated by Arie Altman (The Hebrew University of Jerusalem). Annie Storther, Catarina Bicho and Mafalda Rodrigues are acknowledged for their valuable assistance with sampling. The York Centre of Excellence in Mass Spectrometry was created thanks to a major capital investment through Science City York, supported by Yorkshire Forward with funds from the Northern Way Initiative, and subsequently received additional support from the EPSRC (EP/K039660/1; EP/M028127/1). CP acknowledges Cândido Pinto Ricardo continuous support. ASM’s studentship was funded by the Biotechnology and Biological Sciences Research Council. ED thanks the Daphne Jackson Trust for a Fellowship funded by the Royal Society of Chemistry and the Biotechnology and Biological Sciences Research Council. CA gratefully acknowledges support from Fundação para a Ciência e a Tecnologia (FCT, Portugal) through the FCT Investigator Programme (IF/00376/2012/CP0165/CT0003). OZ was supported by postdoctoral fellowship from FCT (SFRH/BPD/111693/2015). This work was supported by the ITQB NOVA R&D GREEN-it ‘Bioresources for sustainability’ (UID/Multi/04551/2013).

Supplementary material

425_2019_3095_MOESM1_ESM.xlsx (193 kb)
Suppl. Table S1 Biochemical parameters for both control (WW) and stressed (WD) observations in Arabidopsis. Data are the means ± standard error of 6 biological replicates, except for Day 1 (n = 5). Asterisks in the third row show parameters with a significant difference between WW and WD for a particular day (obtained using Mann-Whitney tests). Asterisks in the final column show days that are significantly different from earlier days (using Tukey’s HSD test) with the specific days given in parentheses. Here, asterisks denote *** P < 0.001, ** P < 0.01 and * P < 0.05. Suppl. Table S2 Biochemical parameters for both control (WW) and stressed (WD) observations in Eutrema. Data are the means ± standard error of 6 biological replicates, except for Day 1 (n = 5). Asterisks in the third row show parameters with a significant difference between WW and WD for a particular day (obtained using Mann-Whitney tests). Asterisks in the final column show days that are significantly different from earlier days (using Tukey’s HSD test) with the specific days given in parentheses. Here, asterisks denote *** P < 0.001, ** P < 0.01 and * P < 0.05 (XLSX 192 kb)
425_2019_3095_MOESM2_ESM.xlsx (172 kb)
Suppl. Table S3 Biochemical parameters for both control (WW) and stressed (WD) observations in Arabidopsis. Samples were control-corrected (see Materials and methods). Data shown are the means ± standard error of 6 biological replicates, except for Day 1 (n = 5). Suppl. Table S4 Biochemical parameters for both control (WW) and stressed (WD) observations in Eutrema. Samples were control corrected (see). Data shown are the means ± standard error of 6 biological replicates, except for Day 1 (n = 5) (XLSX 172 kb)
425_2019_3095_MOESM3_ESM.tiff (6.5 mb)
Suppl. Fig. S1 Preliminary drought assay. a Soil water content (SWC, %) progression during the assay for Eutrema and Arabidopsis. b Leaf stomatal conductance (% of the control gs) as a function of the SWC. For controls, percentage gs was calculated relative to Day 0; for treatments, percentage gs was calculated relative to the control for the same day. The 80 % gs level was achieved on different days: by Day 4 in Arabidopsis and by Day 6 in Eutrema. c Regression line fit % gs vs soil water content. Each point represents a single measurement (TIFF 6688 kb)
425_2019_3095_MOESM4_ESM.tiff (10.9 mb)
Suppl. Fig. S2 PCA plots showing the scores for the first two principal components obtained for the Eutrema data after scaling to unit variance with the observations coloured by batch. a Before batch correction, clustering within batches can be seen and, in particular, batches 7 and 8 cluster separately. b After batch correction, differences between batches are no longer apparent (TIFF 11157 kb)
425_2019_3095_MOESM5_ESM.tiff (4.5 mb)
Suppl. Fig. S3 PCA scores for the first two principal components obtained for the Arabidopsis data after scaling to unit variance. The observations are coloured by data collection batch and no obvious differences between batches can be seen so that batch correction is not necessary (TIFF 4577 kb)
425_2019_3095_MOESM6_ESM.tiff (8.1 mb)
Suppl. Fig. S4 a Leaf stomatal conductance of Arabidopsis and Eutrema after imposing water deficit and on re-watering (shaded area). b Regression line fitting % gs vs soil water content. Each point represents a single measurement and P-values were determined by ANCOVA for each main effect (treatment and species) and their interaction. ns, not significant; *** P < 0.001 (TIFF 8338 kb)
425_2019_3095_MOESM7_ESM.tiff (14.4 mb)
Suppl. Fig. S5 The nine clusters obtained with k-means analysis of the 46 time-series remaining after iterative filtering of the metabolite data. Clusters a–d include several sucrose species. Cluster e includes raffinose and cluster f includes citric acid (TIFF 14769 kb)
425_2019_3095_MOESM8_ESM.tiff (10.5 mb)
Suppl. Fig. S6 Heatmap showing the similarity of the 46 time-series selected by iterative k-means analysis of the metabolite data. Metabolites are labelled as follows: S, sucrose; R, raffinose; St, stachyose; CA, citric acid; U, unassigned hexose disaccharide (TIFF 10747 kb)
425_2019_3095_MOESM9_ESM.tiff (9.7 mb)
Suppl. Fig. S7 PCA plots of the biochemical parameters for both control (WW) and treatment (WD) observations in Arabidopsis and Eutrema after control correction. a Unscaled variables.b Scaled variables (TIFF 9973 kb)
425_2019_3095_MOESM10_ESM.tiff (7.6 mb)
Suppl. Fig. S8 Bar charts showing physiological and biochemical parameters in early- (Days 1, 3 and 5) and late-drought stress and on re-watering (Day 13) after control correction. Error bars show the standard error between observations (n = 6 biological replicates, except for Day 1, n = 5). Arabidopsis, dark grey; Eutrema, light grey. ANOVA results are presented in Table 2 (TIFF 7813 kb)
425_2019_3095_MOESM11_ESM.tiff (7.5 mb)
Suppl. Fig. S9 Line plots showing physiological and biochemical parameters in early-drought stress (Days 1, 3 and 5) after control correction. Error bars show the standard error between observations (n = 6 biological replicates, except for Day 1, n = 5). Arabidopsis, dark grey; Eutrema, light grey. ANOVA results are presented in Table 3 (TIFF 7693 kb)


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Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Carla Pinheiro
    • 1
    • 2
    Email author
  • Elizabeth Dickinson
    • 3
  • Andrew Marriott
    • 3
  • Isa C. Ribeiro
    • 1
  • Marta Pintó-Marijuan
    • 1
    • 5
  • Carla António
    • 1
    • 3
  • Olfa Zarrouk
    • 1
  • Maria Manuela Chaves
    • 1
  • Ian C. Dodd
    • 6
  • Sergi Munné-Bosch
    • 5
  • Jane Thomas-Oates
    • 4
  • Julie Wilson
    • 3
    Email author
  1. 1.Instituto de Tecnologia Química E BiológicaUniversidade NOVA de LisboaOeirasPortugal
  2. 2.DCV-Faculdade de Ciências e TecnologiaUniversidade NOVA de LisboaCaparicaPortugal
  3. 3.Department of MathematicsUniversity of YorkYorkUK
  4. 4.Department of ChemistryUniversity of YorkYorkUK
  5. 5.Department of Evolutionary Biology, Ecology and Environmental Sciences, Facultat de BiologiaUniversitat de BarcelonaBarcelonaSpain
  6. 6.The Lancaster Environment CentreLancaster UniversityLancasterUK

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