Abstract
Metabolomics offers opportunities for studying the systematic response of an organism to a genetic and/or an environmental change. Here, the metabolic consequences of drought stress were characterized in the highly drought tolerant plant Caragana korshinskii. The time-of-flight mass spectrometry platform employed identified several hundred metabolites in extracts of the leaf, stem, root collar, and root of plants which had been either subjected to drought stress or were well-watered. Each of the four organs harbored a number of potential metabolite markers for the drought response. An increased abundance of various small carbohydrates and soluble amino acids in each of the four organs was induced by the stress; these compounds may act as compatible solutes or antioxidants. Across the whole plant, there was a fall in the content of several Krebs cycle and glycolysis intermediates, as well as in that of the amino acids glutamic acid and aspartic acid. Pathway analysis suggested that most of the potential metabolite markers were involved in energy metabolism and amino-acid metabolism. The implication was that energy metabolism and photosynthesis are compromised during the adaptation of C. korshinskii to drought stress. Given the different spectrum of metabolites associated with the drought response in the four organs, it was concluded that each organ employs a distinct strategy to cope with drought stress.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Angelcheva L, Mishra Y, Antti H, Kjellsen TD, Funk C, Strimbeck RG, Schroder WP (2014) Metabolomic analysis of extreme freezing tolerance in Siberian spruce (Picea obovata). New Phytol 204:545–555. doi:10.1111/nph.12950
Barrs H, Weatherley P (1962) A re-examination of the relative turgidity technique for estimating water defi-cits in leaves. Aust J Biol Sci 15:413–428. doi:10.1071/BI9620413
Blackman SA, Obendorf RL, Leopold AC (1992) Maturation proteins and sugars in desiccation tolerance of developing soybean seeds. Plant Physiol 100:225–230. doi:10.1104/pp.100.1.225
Boudet AM (2007) Evolution and current status of research in phenolic compounds. Phytochemistry 68(22–24):2722–2735. doi:10.1016/j.phytochem.2007.06.012
Brenac P, Horbowicz M, Downer SM, Dickermn AM, Smith ME, Obendorf RL (1997) Raffinose accumulation related to desiccation tolerance during maize (Zea mays L.) seed development and maturation. J Plant Physiol 150:481–488. doi:10.1016/S0176-1617(97)80102-2
de Miguel M, Guevara MA, Sanchez-Gomez D, de Maria N, Diaz LM, Mancha JA, de Simon BF, Cadahía E, Desai N, Aranda I, Cervera MT (2016) Organ-specific metabolic responses to drought in Pinus pinaster Ait. Plant Physiol Biochem 102:17–26. doi:10.1016/j.plaphy.2016.02.013
Erxleben A, Gessler A, Vervliet-Scheebaum M, Reski R (2012) Metabolite profiling of the moss Physcomitrella patens reveals evolutionary conservation of osmoprotective substances. Plant Cell Rep 31:427–436. doi:10.1007/s00299-011-1177-9
Fang X, Li Y, Xu D, Yang X, Wang G (2006) Activities of starch hydrolytic enzymes and starch mobilization in roots of Caragana korshinskii following above-ground partial shoot removal. Trees 21:93–100. doi:10.1007/s00468-006-0100-4
Fang X, Li J, Xiong Y, Xu D, Fan X, Li F (2007) Responses of Caragana korshinskii Kom. to shoot removal: mechanisms underlying regrowth. Ecol Res 23:863–871. doi:10.1007/s11284-007-0449-x
Fang XW, Turner NC, Li FM, Li WJ, Guo XS (2011) Caragana korshinskii seedlings maintain positive photosynthesis during short-term, severe drought stress. Photosynthetica 49:603–609. doi:10.1007/s11099-011-0067-2
Gargallo-Garriga A, Sardans J, Perez-Trujillo M, Rivas-Ubach A, Oravec M, Vecerova K, Penuelas J (2014) Opposite metabolic responses of shoots and roots to drought. Sci Rep 4:6829. doi:10.1038/srep06829
Gordon WS, Jackson RB (2000) Nutrient concentrations in fine roots. Ecology 81:275–280. doi:10.1890/0012-9658(2000)081
Guo R, Yang Z, Li F, Yan C, Zhong X, Liu Q, Zhao L (2015) Comparative metabolic responses and adaptive strategies of wheat (Triticum aestivum) to salt and alkali stress. BMC Plant Biol 15:1. doi:10.1186/s12870-015-0546-x
Hao P, Zhu J, Gu A, Lv D, Ge P, Chen G, Yan Y (2015) An integrative proteome analysis of different seedling organs in tolerant and sensitive wheat cultivars under drought stress and recovery. Proteomics 15:1544–1563. doi:10.1002/pmic.201400179
He JS, Wang Z, Wang X, Schmid B, Zuo W, Zhou M, Fang J (2006) A test of the generality of leaf trait relationships on the Tibetan Plateau. New Phytol 170:835–848. doi:10.1111/j.1469-8137.2006.01704.x
Jansen K, Du B, Kayler Z, Siegwolf R, Ensminger I, Rennenberg H, Gessler A (2014) Douglas-fir seedlings exhibit metabolic responses to increased temperature and atmospheric drought. PLoS One 9:e114165. doi:10.1371/journal.pone.0114165
Jian S, Zhao C, Fang S, Yu K (2014) Soil water content and water balance simulation of Caragana korshinskii Kom. in the semiarid Chinese Loess Plateau. J Hydrol Hydromech 62:89–96. doi:10.2478/johh-2014-0020
Kind T, Wohlgemuth G, Lee DY, Lu Y, Palazoglu M, Shahbaz S, Fiehn O (2009) FiehnLib: mass spectral and retention index libraries for metabolomics based on quadrupole and time-of-flight gas chromatography/mass spectrometry. Anal Chem 81:10038–10048. doi:10.1021/ac9019522
Kreuzwieser J, Hauberg J, Howell KA, Carroll A, Rennenberg H, Millar AH, Whelan J (2009) Differential response of gray poplar leaves and roots underpins stress adaptation during hypoxia. Plant Physiol 149:461–473. doi:10.1104/pp.108.125989
Li XR, Zhou HY, Wang XP, Zhu YG, O’Conner PJ (2003) The effects of sand stabilization and revegetation on cryptogam species diversity and soil fertility in the Tengger Desert, Northern China. Plant Soil 251:237–245. doi:10.1023/A:1023023702248
Li XR, Ma FY, Xiao HL, Wang XP, Kim KC (2004) Long-term effects of revegetation on soil water content of sand dunes in arid region of Northern China. J Arid Environ 57:1–16. doi:10.1016/S0140-1963(03)00089-2
Li S, Fan C, Li Y, Zhang J, Sun J, Chen Y, Tian C, Su X, Lu M, Liang C, Hu Z (2016) Effects of drought and salt-stresses on gene expression in Caragana korshinskii seedlings revealed by RNA-seq. BMC Genomics 17(1):1. doi:10.1186/s12864-016-2562-0
Lu Y, Lam H, Pi E, Zhan Q, Tsai S, Wang C, Kwan Y, Ngai S (2013) Comparative metabolomics in Glycine max and Glycine soja under salt stress to reveal the phenotypes of their offspring. J Agric Food Chem 61(36):8711–8721. doi:10.1021/jf402043m
Muscolo A, Junker A, Klukas C, Weigelt-Fischer K, Riewe D, Altmann T (2015) Phenotypic and metabolic responses to drought and salinity of four contrasting lentil accessions. J Exp Bot 66(18):5467–5480. doi:10.1093/jxb/erv208
Niinemets U (2016) Uncovering the hidden facets of drought stress: secondary metabolites make the difference. Tree Physiol 36(2):129–132. doi:10.1093/treephys/tpv128
Obata T, Witt S, Lisec J, Palacios-Rojas N, Florez-Sarasa I, Yousfi S, Araus JL, Cairns JE, Fernie AR (2015) Metabolite profiles of maize leaves in drought, heat, and combined stress field trials reveal the relationship between metabolism and grain yield. Plant Physiol 169(4):2665–2683. doi:10.1104/pp.15.01164
Reich PB, Oleksyn J (2004) Global patterns of plant leaf N and P in relation to temperature and latitude. Proc Natl Acad Sci USA 101:11001–11006. doi:10.1073/pnas.0403588101
Sanchez DH, Siahpoosh MR, Roessner U, Udvardi M, Kopka J (2008) Plant metabolomics reveals conserved and divergent metabolic responses to salinity. Physiol Plant 132:209–219. doi:10.1111/j.1399-3054.2007.00993.x
Sanchez DH, Schwabe F, Erban A, Udvardi MK, Kopka J (2012) Comparative metabolomics of drought acclimation in model and forage legumes. Plant Cell Environ 35(1):136–149. doi:10.1111/j.1365-3040.2011.02423.x
Sanchez-Martin J, Heald J, Kingston-Smith A, Winters A, Rubiales D, Sanz M, Mur LAJ, Prats E (2014) A metabolomic study in oats (Avena sativa) highlights a drought tolerance mechanism based upon salicylate signalling pathways and the modulation of carbon, antioxidant and photo-oxidative metabolism. Plant Cell Environ. doi:10.1111/pce.12501
Satou M, Enoki H, Oikawa A, Ohta D, Saito K, Hachiya T, Motohashi R (2014) Integrated analysis of transcriptome and metabolome of Arabidopsis albino or pale green mutants with disrupted nuclear-encoded chloroplast proteins. Plant Mol Biol 85:411–428. doi:10.1007/s11103-014-0194-9
Takahashi H, Imamura T, Konno N, Takeda T, Fujita K, Konishi T, Nishihara M, Uchimiya H (2014) The gentio-oligosaccharide gentiobiose functions in the modulation of bud dormancy in the herbaceous perennial Gentiana. Plant Cell 26(10):3949–3963. doi:10.1105/tpc.114.131631
Van den Ende W (2013) Multifunctional fructans and raffinose family oligosaccharides. Front Plant Sci 4:247. doi:10.3389/fpls.2013.00247
Van der Graaff E, Schwacke R, Schneider A, Desimone M, Kunze R (2006) Transcription analysis of Arabidopsis membrane transporters and hormone pathways during developmental and induced leaf senescence. Plant Physiol 141:776–792. doi:10.1104/pp.106.079293
Wang XP, Brown-Mitic CM, Kang ES, Zhang JG, Li XR (2004) Evapotranspiration of Caragana korshinskii communities in a revegetated desert area: tengger desert, China. Hydrol Process 18:3293–3303. doi:10.1002/hyp.5661
Wang Z, Gao HW, Wu YQ, Han JG (2007) Genetic diversity and Population structure of Caragana korshinskii revealed by AFLP. Crop Sci 47:1737–1743. doi:10.2135/cropsci2006.09.0562
Watanabe M, Balazadeh S, Tohge T, Erban A, Giavalisco P, Kopka J (2013) Comprehensive dissection of spatiotemporal metabolic shifts in primary, secondary, and lipid metabolism during developmental senescence in Arabidopsis. Plant Physiol 162:1290–1310. doi:10.1104/pp.113.217380
Widodo-Patterson JH, Newbigin E, Tester M, Bacic A, Roessner U (2009) Metabolic responses to salt stress of barley (Hordeum vulgare L.) cultivars, Sahara and Clipper, which differ in salinity tolerance. J Exp Bot 60:4089–4103. doi:10.1093/jxb/erp243
Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Villar R (2004) The worldwide leaf economics spectrum. Nature 428:821–827
Xu DH, Fang XW, Su PX, Wang G (2012) Ecophysiological responses of Caragana korshinskii Kom. under extreme drought stress: leaf abscission and stem survives. Photosynthetica 50:541–548. doi:10.1007/s11099-012-0060-4
Zhang ZS, Li XR, Liu LC, Jia RL, Zhang JG, Wang T (2009) Distribution, biomass, and dynamics of roots in a revegetated stand of Caragana korshinskii in the tengger desert, northwestern China. J Plant Res 122:109–119. doi:10.1007/s10265-008-0196-2
Acknowledgement
This work was supported by the National Basic Research Program of China (973 Program, 2013CB429904), The Science Fund for Creative Research Groups (41621001), China, and National Natural Science Foundation of China (No. 31560120).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by H. Peng.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Zhang, J., Chen, G., Zhao, P. et al. The abundance of certain metabolites responds to drought stress in the highly drought tolerant plant Caragana korshinskii . Acta Physiol Plant 39, 116 (2017). https://doi.org/10.1007/s11738-017-2412-y
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11738-017-2412-y