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

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Abstract

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.

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Abbreviations

2-iP:

2-Isopentenyl adenine

ACC:

1-Amino-cyclopropane-1-carboxyic acid

AscA:

Ascorbate (reduced)

CK:

Cytokinin

DHA:

Dehydroascorbate

GA:

Gibberellin

IPA:

Isopentenyl adenosine

JA:

Jasmonic acid

PCA:

Principal component analysis

Z:

Trans-zeatin

ZR:

Trans-zeatin riboside

RWC:

Relative water content

SA:

Salicylic acid

SWC:

Soil water content

References

  • 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 1187:111–118

    CAS  PubMed  Google Scholar 

  • Arbona V, Argamasilla R, Gómez-Cadenas A (2010) Common and divergent physiological, hormonal and metabolic responses of Arabidopsis thaliana and Thellungiella halophila to water and salt stress. J Plant Physiol 167:1342–1350

    CAS  PubMed  Google Scholar 

  • Bechtold U, Penfold CA, Jenkins DJ et al (2016) Time-series transcriptomics reveals that AGAMOUS-LIKE22 affects primary metabolism and developmental processes in drought-stressed Arabidopsis. Plant Cell 28:345–366

    CAS  PubMed  PubMed Central  Google 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 57:289–300

    Google Scholar 

  • Chaves MMM, Costa JMM, Zarrouk O, Pinheiro C, Lopes CMM, Pereira JSS (2016) Controlling stomatal aperture in semi-arid regions—the dilemma of saving water or being cool? Plant Sci 251:54–64

    CAS  PubMed  Google Scholar 

  • Clauw P, Coppens F, Korte A et al (2016) Leaf growth response to mild drought: natural variation in Arabidopsis sheds light on trait architecture. Plant Cell 28:2417–2434

    CAS  PubMed  PubMed Central  Google Scholar 

  • Core Team R (2016) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Davies WJ, Mansfield TA, Hetherington AM (1990) Sensing of soil water status and the regulation of plant growth and development. Plant Cell Environ 13:709–719

    Google Scholar 

  • de Ollas C, Dodd IC (2016) Physiological impacts of ABA–JA interactions under water-limitation. Plant Mol Biol 91:641–650

    PubMed  PubMed Central  Google Scholar 

  • Dedrick J (2007) Physiological and biochemical responses of Yukon and Shandong Thellungiella to water deficits. MSc Thesis (McMaster University)

  • Dinakar C, Bartels B (2013) Desiccation tolerance in resurrection plants: new insights from transcriptome, proteome, and metabolome analysis. Front Plant Sci 4:482

    PubMed  PubMed Central  Google Scholar 

  • Farber M, Attia Z, Weiss D (2016) Cytokinin activity increases stomatal density and transpiration rate in tomato. J Exp Bot 67:6351–6362

    CAS  PubMed  PubMed Central  Google Scholar 

  • Foyer C, Rowell J, Walker D (1983) Measurement of the ascorbate content of spinach leaf protoplasts and chloroplasts during illumination. Planta 157:239–244

    CAS  PubMed  Google Scholar 

  • Gilliham M, Able JA, Roy SJ (2017) Translating knowledge about abiotic stress tolerance to breeding programmes. Plant J 90:898–917

    CAS  PubMed  Google Scholar 

  • Golldack D, Li C, Mohan H, Probst N (2014) Tolerance to drought and salt stress in plants: unraveling the signaling networks. Front Plant Sci 5:151

    PubMed  PubMed Central  Google Scholar 

  • Gong Q, Li P, Ma S, Indu Rupassara S, Bohnert HJ (2005) Salinity stress adaptation competence in the extremophile Thellungiella halophila in comparison with its relative Arabidopsis thaliana. Plant J 44:826–839

    CAS  PubMed  Google Scholar 

  • Granda E, Camarero JJ (2017) Drought reduces growth and stimulates sugar accumulation: new evidence of environmentally driven non-structural carbohydrate use. Tree Physiol 37:997–1000

    PubMed  Google Scholar 

  • Ha S, Vankova R, Yamaguchi-Shinozaki K, Shinozaki K, Tran L-SP (2012) Cytokinins: metabolism and function in plant adaptation to environmental stresses. Trends Plant Sci 17:172–179

    CAS  PubMed  Google Scholar 

  • Harris MJ, Outlaw WH (1991) Rapid adjustment of guard-cell abscisic acid levels to current leaf-water status. Plant Physiol 95:171–173

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hirose N, Takei K, Kuroha T et al (2008) Regulation of cytokinin biosynthesis, compartmentalization and translocation. J Exp Bot 59:75–83

    CAS  PubMed  Google Scholar 

  • Hummel I, Pantin F, Sulpice R et al (2010) Arabidopsis plants acclimate to water deficit at low cost through changes of carbon usage: an integrated perspective using growth, metabolite, enzyme, and gene expression analysis. Plant Physiol 154:357–372

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kalaji HM, Schansker G, Brestic M et al (2017) Frequently asked questions about chlorophyll fluorescence, the sequel. Photosynth Res 132:13–66

    CAS  Google Scholar 

  • Kieber JJ, Schaller GE (2014) Cytokinins. The Arabidopsis book 12:e0168

    PubMed  Google Scholar 

  • Koffler BE, Luschin-Ebengreuth N, Stabentheiner E, Müller M, Zechmann B (2014) Compartment specific response of antioxidants to drought stress in Arabidopsis. Plant Sci 227:133–144

    CAS  PubMed  PubMed Central  Google Scholar 

  • Koornneef M, Meinke D (2010) The development of Arabidopsis as a model plant. Plant J 61:909–921

    CAS  PubMed  Google Scholar 

  • Kosma DK, Bourdenx B, Bernard A et al (2009) The impact of water deficiency on leaf cuticle lipids of Arabidopsis. Plant Physiol 151:1918–1929

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lee YP, Funk C, Erban A, Kopka J, Köhl KI, Zuther E, Hincha DK (2016) Salt stress responses in a geographically diverse collection of Eutrema/Thellungiella spp. accessions. Funct Plant Biol 43:590–606

    CAS  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-F4.3.8

  • Lü S, Zhao H, Marais DLD et al (2012) Arabidopsis ECERIFERUM9 involvement in cuticle formation and maintenance of plant water status. Plant Physiol 159:930–944

    PubMed  PubMed Central  Google Scholar 

  • MacLeod MJ, Dedrick J, Ashton C, Sung WW, Champigny MJ, Weretilnyk EA (2015) Exposure of two Eutrema salsugineum (Thellungiella salsuginea) accessions to water deficits reveals different coping strategies in response to drought. Physiol Plant 155:267–280

    CAS  PubMed  Google Scholar 

  • Maurel C, Verdoucq L, Rodrigues O (2016) Aquaporins and plant transpiration. Plant Cell Env 39:2580–2587

    CAS  Google Scholar 

  • Meyre D, Leonardi A, Brisson G, Vartanian N (2001) Drought-adaptive mechanisms involved in the escape/tolerance strategies of Arabidopsis Landsberg erecta and Columbia ecotypes and their F1 reciprocal progeny. J Plant Physiol 158:1145–1152

    CAS  Google Scholar 

  • Montesinos-Navarro A, Wig J, Xavier Pico F, Tonsor SJ (2011) Arabidopsis thaliana populations show clinal variation in a climatic gradient associated with altitude. New Phytol 189:282–294

    PubMed  Google Scholar 

  • Müller M, Munné-Bosch S (2011) Rapid and sensitive hormonal profiling of complex plant samples by liquid chromatography coupled to electrospray ionization tandem mass spectrometry. Plant Methods 7:37

    PubMed  PubMed Central  Google Scholar 

  • Müller M, Munné-Bosch S (2015) Ethylene response factors: a key regulatory hub in hormone and stress signaling. Plant Physiol 169:32–41

    PubMed  PubMed Central  Google Scholar 

  • Munné-Bosch S, Müller M (2013) Hormonal cross-talk in plant development and stress responses. Front Plant Sci 4:529

    PubMed  PubMed Central  Google Scholar 

  • Nguyen KH, Ha CV, Nishiyama R et al (2016) Arabidopsis type B cytokinin response regulators ARR1, ARR10, and ARR12 negatively regulate plant responses to drought. Proc Natl Acad Sci USA 113:3090–3095

    CAS  PubMed  Google 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 23:2169–2183

    CAS  PubMed  PubMed Central  Google Scholar 

  • Noctor G, Mhamdi A, Foyer CH (2014) The roles of reactive oxygen metabolism in drought: not so cut and dried. Plant Physiol 164:1636–1648

    CAS  PubMed  PubMed Central  Google Scholar 

  • Orsini F, D’Urzo MP, Inan G, Serra S et al (2010) A comparative study of salt tolerance parameters in 11 wild relatives of Arabidopsis thaliana. J Exp Bot 61:3787–3798

    CAS  PubMed  PubMed Central  Google Scholar 

  • Osakabe Y, Osakabe K, Shinozaki K, Tran L-SP (2014) Response of plants to water stress. Front Plant Sci 5:86

    PubMed  PubMed Central  Google Scholar 

  • Peters S, Mundree SG, Thomson JA, Farrant JM, Keller F (2007) Protection mechanisms in the resurrection plant Xerophyta viscosa (Baker): both sucrose and raffinose family oligosaccharides (RFOs) accumulate in leaves in response to water deficit. J Exp Bot 58:1947–1956

    CAS  PubMed  Google 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 7:1179

    PubMed  PubMed Central  Google Scholar 

  • Pinheiro C, Chaves MM (2011) Photosynthesis and drought: can we make metabolic connections from available data? J Exp Bot 62:869–882

    CAS  PubMed  Google Scholar 

  • Pinheiro C, Chaves MM, Ricardo CP (2001) Alterations in carbon and nitrogen metabolism induced by water deficit in the stems and leaves of Lupinus albus L. J Exp Bot 52:1063–1070

    CAS  PubMed  Google Scholar 

  • Pinheiro C, Passarinho JA, Ricardo CP (2004) Effect of drought and rewatering on the metabolism of Lupinus albus organs. J Plant Physiol 161:1203–1210

    CAS  PubMed  Google 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 62:4965–4974

    CAS  PubMed  Google Scholar 

  • Piquerez SJM, Harvey SE, Beynon JL, Ntoukakis V (2014) Improving crop disease resistance: lessons from research on Arabidopsis and tomato. Front Plant Sci 5:671

    PubMed  PubMed Central  Google Scholar 

  • Queval G, Noctor G (2007) A plate reader method for the measurement of NAD, NADP, glutathione, and ascorbate in tissue extracts: application to redox profiling during Arabidopsis rosette development. Anal Biochem 363:58–69

    CAS  PubMed  Google Scholar 

  • Rivas-San Vicente M, Plasencia J (2011) Salicylic acid beyond defence: its role in plant growth and development. J Exp Bot 62:3321–3338

    CAS  PubMed  Google Scholar 

  • Rivero RM, Kojima M, Gepstein A et al (2007) Delayed leaf senescence induces extreme drought tolerance in a flowering plant. Proc Natl Acad Sci USA 104:19631–19636

    CAS  PubMed  Google Scholar 

  • Ruan YL (2014) Sucrose metabolism: gateway to diverse carbon use and sugar signaling. Annu Rev Plant Biol 65:33–67

    CAS  PubMed  Google Scholar 

  • Rusilowicz M, Dickinson M, Charlton A, O’Keefe S, Wilson J (2016) A batch correction method for liquid chromatography–mass spectrometry data that does not depend on quality control samples. Metabolomics 12:56

    PubMed  PubMed Central  Google Scholar 

  • Sack L, John GP, Buckley TN (2018) ABA accumulation in dehydrating leaves is associated with decline in cell volume not turgor pressure. Plant Physiol 176:489–495

    CAS  PubMed  Google Scholar 

  • Skirycz A, Vandenbroucke K, Clauw P et al (2011) Survival and growth of Arabidopsis plants given limited water are not equal. Nat Biotechnol 29:212–214

    CAS  PubMed  Google Scholar 

  • Sun X, Luo X, Sun M et al (2014) A Glycine soja 14-3-3 protein GsGF140 participates in stomatal and root hair development and drought tolerance in Arabidopsis thaliana. Plant Cell Physiol 55:99–118

    CAS  PubMed  Google Scholar 

  • Taji T, Seki M, Satou M, Sakurai T et al (2004) Comparative genomics in salt tolerance between Arabidopsis and Arabidopsis-related halophyte salt cress using Arabidopsis microarray. Plant Physiol 135:1697–1709

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tardieu F (2012) Any trait or trait-related allele can confer drought tolerance: just design the right drought scenario. J Exp Bot 63:25–31

    CAS  PubMed  Google Scholar 

  • Tardieu F, Parent B, Simonneau T (2010) Control of leaf growth by abscisic acid: hydraulic or non-hydraulic processes? Plant, Cell Environ 33:636–647

    Google 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 104:20623–20628

    CAS  PubMed  Google Scholar 

  • Turner NC, Abbo S, Berger JD, Chaturvedi SK, French RJ, Ludwig C et al (2007) Osmotic adjustment in chickpea (Cicer arietinum L.) results in no yield benefit under terminal drought. J Exp Bot 58:187–194

    CAS  PubMed  Google Scholar 

  • Urano K, Maruyama K, Jikumaru Y, Kamiya Y, Yamaguchi-Shinozaki K, Shinozaki K (2017) Analysis of plant hormone profiles in response to moderate dehydration stress. Plant J 90:17–36

    CAS  PubMed  Google Scholar 

  • Wehrens R, Hageman JA, van Eeuwijk F, Kooke R et al (2016) Improved batch correction in untargeted MS-based metabolomics. Metabolomics 12:88

    PubMed  PubMed Central  Google Scholar 

  • Xu X, Feng J, Lü S, Lohrey GT, An H, Zhou Y, Jenks MA (2014) Leaf cuticular lipids on the Shandong and Yukon ecotypes of saltwater cress, Eutrema salsugineum, and their response to water deficiency and impact on cuticle permeability. Physiol Plant 151:446–458

    CAS  PubMed  Google Scholar 

  • Xu Y, Burgess P, Huang B (2017) Transcriptional regulation of hormone-synthesis and signaling pathways by overexpressing cytokinin-synthesis contributes to improved drought tolerance in creeping bentgrass. Physiol Plant 161:235–256

    CAS  PubMed  Google Scholar 

  • Zhao Y, Chan Z, Gao J et al (2016) ABA receptor PYL9 promotes drought resistance and leaf senescence. Proc Natl Acad Sci USA 113:1949–1954

    CAS  PubMed  Google Scholar 

  • Zhu J-K (2015) The next top models: extreme farming. Cell 163:18–20

    Google Scholar 

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Acknowledgements

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).

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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)

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)

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)

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)

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)

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)

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)

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)

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)

Suppl. Fig. S8

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)

Suppl. Fig. S9

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)

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Pinheiro, C., Dickinson, E., Marriott, A. et al. Distinctive phytohormonal and metabolic profiles of Arabidopsis thaliana and Eutrema salsugineum under similar soil drying. Planta 249, 1417–1433 (2019). https://doi.org/10.1007/s00425-019-03095-5

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