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Effect of drought stress on metabolite contents in barley recombinant inbred line population revealed by untargeted GC–MS profiling

  • Barbara Swarcewicz
  • Aneta Sawikowska
  • Łukasz Marczak
  • Magdalena Łuczak
  • Danuta Ciesiołka
  • Karolina Krystkowiak
  • Anetta Kuczyńska
  • Mariola Piślewska-Bednarek
  • Paweł KrajewskiEmail author
  • Maciej StobieckiEmail author
Original Article

Abstract

Drought stress is perhaps one of the most common abiotic factors which crop plants have to cope with. To survive, plants have to adapt to periods of water deficit that may occur during their vegetation. This can be achieved by triggering various changes in the plant genome, transcriptome, proteome, and metabolome, leading to different physiological and biochemical reactions of plants. We have compared changes in barley leaf and root metabolomes in response to drought in recombinant inbred line (RIL) population derived from hybrids between two spring genotypes: German variety Maresi and Syrian breeding line Cam/B1//CI08887/CI05761. Response of plants to drought of the studied barley lines was rather conservative; most barley genotypes changed their metabolome composition independently in leaf and root. Based on analysis of variance, metabolites were classified with respect to significance of difference between lines, drought effect (understood as the difference between metabolite level in drought and control plants), and line × drought interaction. The revealed changes in accumulation of some metabolites, e.g., proline and other amino acids, carbohydrates or carboxylic acids have been regarded to be a basic plant strategy for acquiring drought stress tolerance. It was possible to draw some general inferences from obtained results: changes of metabolites involved in barley response to drought were rather similar qualitatively but varied quantitatively among the studied RILs. Compatible solutes and osmolytes were the major group of compounds accumulated under drought. We have also observed significant organ specificity between leaf and root response to drought at the metabolome level in all recognized metabolites classes. Moreover, we have found metabolites which differentiated tested genotypes under drought—and these compounds might be considered as potential biomarkers associated with drought tolerance in barley.

Keywords

Abiotic stress Drought Gas chromatography/mass spectrometry Hordeum vulgare Metabolomics Primary and secondary metabolites Recombinant inbred lines 

Notes

Acknowledgements

This work was supported by the European Regional Development Fund through the Innovative Economy Program for Poland 2007–2013, project WND-POIG.01.03.01-00-101/08 POLAPGEN-BD.

Supplementary material

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References

  1. Agati G, Matteini P, Goti A, Tattini M (2007) Chloroplast-located flavonoids can scavenge singlet oxygen. New Phytol 174:77–89CrossRefPubMedGoogle Scholar
  2. Ashraf M (2010) Inducing drought tolerance in plants: recent advances. Biotechnol Adv 28:169–183CrossRefPubMedGoogle Scholar
  3. Barchet GLH, Dauwe R, Guy RD, Schroeder WR, Soolanayakanahally RY, Campbell MM, Mansfield SD (2014) Investigating the drought-stress response of hybrid poplar genotypes by metabolite profiling. Tree Physiol 34:1203–1219CrossRefPubMedGoogle Scholar
  4. Bartels D, Sunkar R (2005) Drought and salt tolerance in plants. Crit Rev Plant Sci 24:23–58CrossRefGoogle Scholar
  5. Bascuñán-Godoy L, Reguera M, Abdel-Tawab YM, Blumwald E (2016) Water deficit stress-induced changes in carbon and nitrogen partitioning in Chenopodium quinoa Willd. Planta 243:591–603CrossRefPubMedGoogle Scholar
  6. Bennet-Clark A (1933) The role of the organic acids in plant metabolism. New Phytol 32:37–71CrossRefGoogle Scholar
  7. Bhargava S, Sawant K (2013) Drought stress adaptation: metabolic adjustment and regulation of gene expression (R Tuberosa, Ed.). Plant Breeding 132:21–32CrossRefGoogle Scholar
  8. Bollina V, Kumaraswamy GK, Kushalappa AC, Choo TM, Dion Y, Rioux S, Faubert D, Hamzehzarghani H (2010) Mass spectrometry-based metabolomics application to identify quantitative resistance-related metabolites in barley against Fusarium head blight. Mol Plant Pathol 11:769–782PubMedGoogle Scholar
  9. Bowne JB, Erwin TA, Juttner J, Schnurbusch T, Langridge P, Bacic A, Roessner U (2012) Drought responses of leaf tissues from wheat cultivars of differing drought tolerance at the metabolite level. Mol Plant 5:418–429CrossRefPubMedGoogle Scholar
  10. Bunzel M (2010) Chemistry and occurrence of hydroxycinnamate oligomers. Phytochem Rev 9:47–64CrossRefGoogle Scholar
  11. Chen Z, Cuin TA, Zhou M, Twomey A, Naidu BP, Shabala S (2007) Compatible solute accumulation and stress-mitigating effects in barley genotypes contrasting in their salt tolerance. J Exp Bot 58:4245–4255CrossRefPubMedGoogle Scholar
  12. Chmielewska K, Rodziewicz P, Swarcewicz B. Sawikowska A, Krajewski P, Marczak Ł, Ciesiołka D, Kuczyńska A, Mikołajczak K, Ogrodowicz P, Krystkowiak K, Surma M, Adamski T, Bednarek P, Stobiecki M (2016) Analysis of drought-induced proteomic and metabolomic changes in barley (Hordeum vulgare L.) leaves and roots unravels some aspects of biochemical mechanisms involved in drought tolerance. Front Plant Sci 7, Article no 1108Google Scholar
  13. Choi YH, van Spronsen J, Dai Y, Verberne M, Hollmann F, Arends WCEI, Witkamp G-J, Verpoorte R (2011) Are natural deep eutectic solvents the missing link in understanding cellular metabolism and physiology? Plant Physiol 156:1701–1705CrossRefPubMedPubMedCentralGoogle Scholar
  14. Cuadros-Inostroza Á, Caldana C, Redestig H, Kusano M, Lisec J, Peña-Cortés H, Willmitzer L, Hannah MA (2009) TargetSearch: a Bioconductor package for the efficient preprocessing of GC-MS metabolite profiling data. BMC Bioinform 10:428CrossRefGoogle Scholar
  15. Cullis BR, Smith AB, Coombes NE (2006) On the design of early generation variety trials with correlated data. J Agr Biol Environ Stat 11:381–393CrossRefGoogle Scholar
  16. Degenkolbe T, Do PT, Kopka J, Zuther E, Hincha DK, Köhl KI (2013) Identification of drought tolerance markers in a diverse population of rice cultivars by expression and metabolite profiling (GK Pandey, Ed.). PLoS One 8:e63637CrossRefPubMedPubMedCentralGoogle Scholar
  17. Dixon RA, Strack D (2003) Phytochemistry meets genome analysis, and beyond. Phytochemistry 62:815–816CrossRefPubMedGoogle Scholar
  18. Do PT, Prudent M, Sulpice R, Causse M, Fernie AR (2010) The influence of fruit load on the tomato pericarp metabolome in a Solanum chmielewskii introgression line population. Plant Physiol 154:1128–1142CrossRefPubMedPubMedCentralGoogle Scholar
  19. Fernie AR, Schauer N (2009) Metabolomics-assisted breeding: a viable option for crop improvement? Trends Genet 25:39–48CrossRefPubMedGoogle Scholar
  20. Fry SC (2004) Primary cell wall metabolism: tracking the careers of wall polymers in living plant cells. New Phytol 161:641–675CrossRefGoogle Scholar
  21. Goldschmidt EE, Huber SC (1992) Regulation of photosynthesis by end-product accumulation in leaves of plants storing starch, sucrose, and hexose sugars. Plant Physiol 99:1443–1448CrossRefPubMedPubMedCentralGoogle Scholar
  22. Gong L, Chen W, Gao Y, Liu X, Zhang H, Xu C, Yu S, Zhang Q, Luo J (2013) Genetic analysis of the metabolome exemplified using a rice population. Proc Natl Acad Sci 110:20320–20325CrossRefPubMedPubMedCentralGoogle Scholar
  23. Górny AG (2001) Variation in utilization efficiency and tolerance to reduced water and nitrogen supply among wild and cultivated barleys. Euphytica 117:59–66CrossRefGoogle Scholar
  24. Haupt-Herting S, Fock HP (2002) Oxygen exchange in relation to carbon assimilation in water-stressed leaves during photosynthesis. Ann Bot 89 Spec No, 851–9Google Scholar
  25. Huang CY, Roessner U, Eickmeier I, Genc Y, Callahan DL, Shirley N, Langridge P, Bacic A (2008) Metabolite profiling reveals distinct changes in carbon and nitrogen metabolism in phosphate-deficient barley plants (Hordeum vulgare L.). Plant Cell Physiol 49:691–703CrossRefPubMedGoogle Scholar
  26. Jadczyszyn T, Kowalczyk J, Lipiński W (2008) Fertilization recommendations for field crops and permanent grassland. Dissemination Instruction IUNG-PIB 151: p 24Google Scholar
  27. Jones DL, Darrah PR (1994) Role of root derived organic acids in the mobilization of nutrients from the Rhizosphere. Plant Soil 166:247–257CrossRefGoogle Scholar
  28. Jorge TF, Rodrigues JA, Caldana C, Schmidt R, van Dongen JT, Thomas-Oates J, António C (2016) Mass spectrometry-based plant metabolomics: metabolite responses to abiotic stress. Mass Spectrom Rev 35:620–649CrossRefPubMedGoogle Scholar
  29. Keurentjes JJ (2009) Genetical metabolomics: closing in on phenotypes. Curr Opin Plant Biol 12:223–230CrossRefPubMedGoogle Scholar
  30. Kliebenstein DJ, D’Auria JC, Behere AS, Kim JH, Gunderson KL, Breen JN, Lee G, Gershenzon J, Last RL, Jander G (2007) Characterization of seed-specific benzoyloxyglucosinolate mutations in Arabidopsis thaliana. Plant J 51:1062–1076CrossRefPubMedGoogle Scholar
  31. Kopka J (2006) Current challenges and developments in GC–MS based metabolite profiling technology. J Biotechnol 124:312–322CrossRefPubMedGoogle Scholar
  32. Kopka J, Schauer N, Krueger S et al (2005) GMD@CSB.DB: the Golm metabolome database. Bioinformatics 21:1635–1638CrossRefPubMedGoogle Scholar
  33. Kováčik J, Klejdus B, Babula P, Jarošová M (2014) Variation of antioxidants and secondary metabolites in nitrogen-deficient barley plants. J Plant Physiol 171:260–268CrossRefPubMedGoogle Scholar
  34. Kumaraswamy KG, Kushalappa AC, Choo TM, Dion Y, Rioux S (2011) Mass spectrometry based metabolomics to identify potential biomarkers for resistance in barley against fusarium head blight (Fusarium graminearum). J Chem Ecol 37:846–856CrossRefPubMedGoogle Scholar
  35. Langfelder P, Horvath S (2008) WGCNA: an R package for weighted correlation network analysis. BMC Bioinform 9:559CrossRefGoogle Scholar
  36. Lawlor DW, Cornic G (2002) Photosynthetic carbon assimilation and associated metabolism in relation to water deficits in higher plants. Plant Cell Environ 25:275–294CrossRefPubMedGoogle Scholar
  37. Lescano CI, Martini C, González CA, Desimone M (2016) Allantoin accumulation mediated by allantoinase downregulation and transport by Ureide Permease 5 confers salt stress tolerance to Arabidopsis plants. Plant Mol Biol 91:581–595CrossRefPubMedGoogle Scholar
  38. Mazzucotelli E, Tartari A, Cattivelli L, Forlani G (2006) Metabolism of -aminobutyric acid during cold acclimation and freezing and its relationship to frost tolerance in barley and wheat. J Exp Bot 57:3755–3766CrossRefPubMedGoogle Scholar
  39. Mikołajczak K, Ogrodowicz P, Gudyś K et al (2016) Quantitative trait loci for yield and yield-related traits in spring barley populations derived from crosses between European and Syrian cultivars (M Li, Ed.). PLoS One 11(5):e0155938CrossRefPubMedPubMedCentralGoogle Scholar
  40. Mikołajczak K, Kuczyńska A, Krajewski P et al (2017) Quantitative trait loci for plant height in Maresi × CamB barley population and their associations with yield-related traits under different water regimes. J Appl Genet 58:23–35CrossRefPubMedGoogle Scholar
  41. Moco S, Vervoort J, Moco S, Bino RJ, De Vos RCH, Bino R (2007) Metabolomics technologies and metabolite identification. TrAC Trends Anal Chem 26:855–866CrossRefGoogle Scholar
  42. Nakabayashi R, Yonekura-Sakakibara K, Urano K et al (2014) Enhancement of oxidative and drought tolerance in Arabidopsis by overaccumulation of antioxidant flavonoids. Plant J 77:367–379CrossRefPubMedGoogle Scholar
  43. Nishizawa A, Yabuta Y, Shigeoka S (2008) Galactinol and raffinose constitute a novel function to protect plants from oxidative damage. Plant Physiol 147:1251–1263CrossRefPubMedPubMedCentralGoogle Scholar
  44. Piasecka A, Sawikowska A, Krajewski P, Kachlicki P (2015a) Combined mass spectrometric and chromatographic methods for in-depth analysis of phenolic secondary metabolites in barley leaves. J Mass Spectrom 50:513–532CrossRefPubMedGoogle Scholar
  45. Piasecka A, Jedrzejczak-Rey N, Bednarek P (2015b) Secondary metabolites in plant innate immunity: conserved function of divergent chemicals. New Phytol 206:948–964CrossRefPubMedGoogle Scholar
  46. Piasecka A, Sawikowska A, Kuczyńska A, Ogrodowicz P, Mikołajczak K, Krystkowiak K, Gudyś K, Guzy-Wróbelska J, Krajewski P, Kachlicki P (2016) Drought related secondary metabolites of barley (Hordeum vulgare L.) leaves and their mQTLs. Plant J. doi: 10.1111/tpj.13430
  47. Riedelsheimer C, Lisec J, Czedik-Eysenberg A, Sulpice R, Flis A, Grieder C, Altmann T, Stitt M, Willmitzer L, Melchinger AE (2012) Genome-wide association mapping of leaf metabolic profiles for dissecting complex traits in maize. Proc Natl Acad Sci 109:8872–8877CrossRefPubMedPubMedCentralGoogle Scholar
  48. Rizhsky L (2004) When defense pathways collide. The response of arabidopsis to a combination of drought and heat stress. Plant Physiol 134:1683–1696CrossRefPubMedPubMedCentralGoogle Scholar
  49. Roessner U, Patterson JH, Forbes MG, Fincher GB, Langridge P, Bacic A (2006) An investigation of boron toxicity in barley using metabolomics. Plant Physiol 142:1087–1101CrossRefPubMedPubMedCentralGoogle Scholar
  50. Seki M, Umezawa T, Urano K, Shinozaki K (2007) Regulatory metabolic networks in drought stress responses. Curr Opin Plant Biol 10:296–302CrossRefPubMedGoogle Scholar
  51. Shannon P (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504CrossRefPubMedPubMedCentralGoogle Scholar
  52. Sharp RE (2004) Root growth maintenance during water deficits: physiology to functional genomics. J Exp Bot 55:2343–2351CrossRefPubMedGoogle Scholar
  53. Sicher RC, Timlin D, Bailey B (2012) Responses of growth and primary metabolism of water-stressed barley roots to rehydration. J Plant Physiol 169:686–695CrossRefPubMedGoogle Scholar
  54. Taji T, Ohsumi C, Iuchi S, Seki M, Kasuga M, Kobayashi M, Yamaguchi-Shinozaki K, Shinozaki K (2002) Important roles of drought- and cold-inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. Plant J Cell Mol Biol 29:417–426CrossRefGoogle Scholar
  55. Toubiana D, Semel Y, Tohge T, Beleggia R, Cattivelli L, Rosental L, Nikoloski Z, Zamir D, Fernie AR, Fait A (2012) Metabolic profiling of a mapping population exposes new insights in the regulation of seed metabolism and seed, fruit, and plant relations (GP Copenhaver, Ed.). PLoS Genet 8:e1002612CrossRefPubMedPubMedCentralGoogle Scholar
  56. Ullrich SE (2011) Significance, adaptation, production, and trade of barley. Barley. Wiley-Blackwell, Oxford, pp 3–13Google Scholar
  57. Vinocur B, Altman A (2005) Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. Curr Opin Biotechnol 16:123–132CrossRefPubMedGoogle Scholar
  58. VSN International (2013) GenStat for Windows, 16th edn. Hemel Hempstead, UKGoogle Scholar
  59. Wen W, Li D, Li X et al (2014) Metabolome-based genome-wide association study of maize kernel leads to novel biochemical insights. Nature Commun 5:3438Google Scholar
  60. 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 60:4089–4103CrossRefPubMedPubMedCentralGoogle Scholar
  61. Witt S, Galicia L, Lisec J, Cairns J, Tiessen A, Araus JL, Palacios-Rojas N, Fernie AR (2012) Metabolic and phenotypic responses of greenhouse-grown maize hybrids to experimentally controlled drought stress. Mol Plant 5:401–417CrossRefPubMedGoogle Scholar
  62. Wu D, Cai S, Chen M, Ye L, Chen Z, Zhang H, Dai F, Wu F, Zhang G (2013a) Tissue metabolic responses to salt stress in wild and cultivated barley (M Xu, Ed.). PLoS One 8:e55431CrossRefPubMedPubMedCentralGoogle Scholar
  63. Wu D, Shen Q, Cai S, Chen Z-H, Dai F, Zhang G (2013b) Ionomic responses and correlations between elements and metabolites under salt stress in wild and cultivated barley. Plant Cell Physiol 54:1976–1988CrossRefPubMedGoogle Scholar
  64. Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803CrossRefPubMedGoogle Scholar
  65. Zeiger E (1983) The biology of stomatal guard cells. Ann Rev Plant Physiol 34:441–474CrossRefGoogle Scholar

Copyright information

© Franciszek Górski Institute of Plant Physiology, Polish Academy of Sciences, Kraków 2017

Authors and Affiliations

  1. 1.Institute of Bioorganic Chemistry, Polish Academy of SciencesPoznańPoland
  2. 2.Department of Statistical and Mathematical MethodsPoznań University of Life SciencesPoznańPoland
  3. 3.Institute of Plant Genetics Polish Academy of SciencesPoznańPoland

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