Distinctive phytohormonal and metabolic profiles of Arabidopsis thaliana and Eutrema salsugineum under similar soil drying
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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.
KeywordsBioactive cytokinins Drought resilience Metabolite profiles Redox state Rewatering Stomatal conductance Unsupervised multivariate analysis
Principal component analysis
Relative water content
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).
- Antonio C, Pinheiro C, Chaves MM, Ricardo CP, Ortuño MF, Thomas-Oates J (2008) Analysis of carbohydrates in Lupinus albus stems on imposition of water deficit, using porous graphitic carbon liquid chromatography-electrospray ionization mass spectrometry. J Chromatogr A 1187:111–118CrossRefPubMedGoogle Scholar
- Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Series B Methodol 57:289–300Google Scholar
- Core Team R (2016) R: A language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
- Dedrick J (2007) Physiological and biochemical responses of Yukon and Shandong Thellungiella to water deficits. MSc Thesis (McMaster University)Google Scholar
- Lichtenthaler HK, Buschmann C (2001) Chlorophylls and carotenoids: measurement and characterization by UV–VIS Spectroscopy. Curr Protocols Food Anal Chem F4.3.1-F4.3.8Google Scholar
- Nishiyama R, Watanabe Y, Fujita Y, Le DT et al (2011) Analysis of cytokinin mutants and regulation of cytokinin metabolic genes reveals important regulatory roles of cytokinins in drought, salt and abscisic acid responses, and abscisic acid biosynthesis. Plant Cell 23:2169–2183CrossRefPubMedPubMedCentralGoogle Scholar
- Pilarska M, Wiciarz M, Ivan Jajić I et al (2016) A different pattern of production and scavenging of reactive oxygen species in halophytic Eutrema salsugineum (Thellungiella salsuginea) plants in comparison to Arabidopsis thaliana and its relation to salt stress signaling. Front Plant Sci 7:1179CrossRefPubMedPubMedCentralGoogle Scholar
- Pinheiro C, Antonio C, Ortuno MF, Dobrev PI, Hartung W, Thomas-Oates J, Ricardo CP, Vankova R, Chaves MM, Wilson JC (2011) Initial water deficit effects on Lupinus albus photosynthetic performance, carbon metabolism, and hormonal balance: metabolic reorganization prior to early stress responses. J Exp Bot 62:4965–4974CrossRefPubMedGoogle Scholar
- Tran LSP, Urao T, Qin F, Maruyama K, Kakimoto T, Shinozaki K, Yamaguchi-Shinozaki K (2007) Functional analysis of AHK1/ATHK1 and cytokinin receptor histidine kinases in response to abscisic acid, drought, and salt stress in Arabidopsis. Proc Natl Acad Sci USA 104:20623–20628CrossRefPubMedGoogle Scholar