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Global metabolomics analysis reveals distinctive tolerance mechanisms in different plant organs of lentil (Lens culinaris) upon salinity stress

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Abstract

Background and Aims

Omic technologies in the past years have provided a variety of data in model plants. In legumes, results οn Lotus japonicus and Medicago truncatula have highlighted the biochemistry which takes place inside cells under a variety of abiotic stresses. Here we conducted metabolomics in the forage legume lentil (Lens culinaris) upon salinity stress on acclimated and non-acclimated plants and compared results from leaf and root analyses.

Methods

We used two lentil varieties, originated from different geographical locations and studied differences in their global metabolite profile i) using gradual or initial application of salt stress, ii) between leaves and roots, and iii) between the varieties.

Results

Most important differences were noted in salinity induced diminished abundance of organic acids in both varieties’ leaves and roots, accumulation of sugars and polyols in leaves, and accumulation of other key-metabolites, such as L-asparagine, D-trehalose, allantoin and urea in the roots. We also demonstrated the driver of deleterious Cl accumulation in leaves for potential compartmentalization in the vacuole, a defensive mechanism for withstanding salinity stress in plants. Finally, a model is suggested of how legumes upregulate a metabolic pathway, which involves purines catabolism in order to assimilate carbon and nitrogen, which are limited during salinity stress.

Conclusions

Future omics works with lentil can help understanding the regulation of the biochemical “arsenal” against abiotic stresses such as salinity and render the selection of better crops.

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Abbreviations

GA:

Gradual Application

IA:

Initial Application

References

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biol 55:373–399

    Article  CAS  Google Scholar 

  • Aslam M, Huffaker RC, Rains DW (1984) Early effects of salinity on nitrate assimilation in barley seedlings. Plant Physiol 76(2):321–325

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bandeoglu E, Eyidogan F, Yucel M, Oktem HA (2004) Antioxidant responses of shoots and roots of lentil to NaCl-salinity stress. Plant Growth Regul 42:69–77

    Article  CAS  Google Scholar 

  • Bartels D, Sunkar R (2005) Drought and Salt Tolerance in Plants. Crit Rev Plant Sci 24(1):23–58

    Article  CAS  Google Scholar 

  • Basu PS, Ali M, Chaturvedi SK (2007) Osmotic adjustment increases water uptake, remobilization of assimilates and maintains photosynthesis in chickpea under drought. Indian J Exp Biol 45:261–267

    PubMed  CAS  Google Scholar 

  • Becker BF (1993) Towards the physiological function of uric acid. Free Radic Biol Med 14:615–631

    Article  PubMed  CAS  Google Scholar 

  • Bhardwaj KKR (1975) Survival and symbiotic characteristics of rhizobium in saline-alkali soils. Plant Soil 43:377–385

    Article  Google Scholar 

  • Broughton JW, Dilworth JM (1971) Control of leghaemoglobin synthesis in snake beans. Biochem J 125(4):1075–1080

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cañas RA, Quilleré I, Lea PJ, Hirel B (2010) Analysis of amino acid metabolism in the ear of maize mutants deficient in two cytosolic glutamine synthetase isoenzymes highlights the importance of asparagine for nitrogen translocation within sink organs. Plant Biotechnol J 8:966–978

    Article  PubMed  CAS  Google Scholar 

  • Cao Y, Wang Y, Dai B, Wang B, Zhang H, Zhu Z, Xu Y, Cao Y, Jiang Y, Zhang G (2008) Trehalose is an important mediator of Cap1p oxidative stress response in Candida albicans. Biol Pharm Bull 31(3):421–425

    Article  PubMed  CAS  Google Scholar 

  • Carillo P, Annunziata MG, Pontecorvo G, Fuggi A, Woodrow P (2011) Salinity Stress and Salt Tolerance, In: Shanker A (ed) Abiotic Stress in Plants - Mechanisms and Adaptations Edition. InTech, Croatia, Rijeka, pp 21-38

  • Cernusak LA, Winter K, Turner BL (2009) Plant d15N Correlates with the Transpiration Efficiency of Nitrogen Acquisition in Tropical Trees. Plant Physiol 151:1667–1676

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Farquhar GD, Richards RA (1984) Isotopic composition of plant carbon correlates with water-use efficiency of wheat genotypes. Aust J Plant Physiol 11:539–552

    Article  CAS  Google Scholar 

  • Farquhar GD, O’Leary MH, Berry JA (1982) On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. Australian Journal of Plant Physiology 9: 121–137

  • Fiehn O, Barupal DK, Kind T (2011) Extending biochemical databases by metabolomic surveys. J Biol Chem 286(27):23637–23643

  • Flowers TJ, Munns R, Colmer TD (2014) Sodium chloride toxicity and the cellular basis of salt tolerance in halophytes. Ann Bot 115(3):419–431

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fougère F, Le Rudulier D, Streeter GJ (1991) Effects of Salt Stress on Amino Acid, Organic Acid, and Carbohydrate Composition of Roots, Bacteroids, and Cytosol of Alfalfa (Medicago sativa L.). Plant Physiol 96:1228–1236. https://doi.org/10.1104/pp.96.4.1228

    Article  PubMed  PubMed Central  Google Scholar 

  • Gao Z, Sagi M, Lips HS (1998) Carbohydrate metabolism in leaves and assimilate partitioning in fruits of tomato (Lycopersicon esculentum L.) as affected by salinity. Plant Sci 135:149–159

    Article  CAS  Google Scholar 

  • Garcia AB, Engler J, Iyer S, Gerats T, Van Montagu M, Caplan AB (1997) Effects of osmoprotectants upon NaCl stress in rice. Plant Physiol 115(1):159–169

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Garg AK, Kim JK, Owens TG, Ranwala AP, Choi YD, Kochian LV, Wu RJ (2002) Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses. Proc Natl Acad Sci U S A 99:15898–15903

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gessler A, Duarte H, Franco CA, Lüttge U, de Mattos AE, Nahm M, Scarano RF, Zaluar TLH, Rennenberg H (2005). Ecophysiology of selected tree species in different plant communities at the periphery of the Atlantic Forest of SE - Brazil. II. Spacial and ontogenetic dynamics in Andira legalis, a deciduous legume tree. Trees 19:510–522

  • Ghassemi F, Jakeman AJ, Nix HA (1995). Salinization of Land and Water Resources: Human Causes, Extent, Management and Case Studies. (CAB International)

  • Ghosh G, Drew MC (1991) Comparison of analytical methods for extraction of chloride from plant tissue using 36CL as tracer. Plant Soil 136:265–368

    Article  CAS  Google Scholar 

  • Graham PH, Vance CP (2003) Legumes: Importance and Constraints to Greater Use. Plant Physiol 131:872–877

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Grattan SR, Grieve CM (1999) Salinity-mineral nutrient relations in horticultural crops. Sci Hortic 78:127–157

    Article  CAS  Google Scholar 

  • Gujaria-Verma N, Vail SL, Carrasquilla-Garcia N, Penmetsa RV, Cook DR, Farmer AD, Vandenberg A, Bett KE (2014) Genetic mapping of legume orthologs reveals high conservation of synteny between lentil species and the sequenced genomes of Medicago and chickpea. Front Plant Sci 5:2014. https://doi.org/10.3389/fpls.2014.00676

    Article  Google Scholar 

  • Gupta B, Huang B (2014) Mechanism of Salinity Tolerance in Plants: Physiological. Biochemical, and Molecular Characterization, Int J of Gen. https://doi.org/10.1155/2014/701596

  • Hanson J, Smeekens S (2009) Sugar perception and signaling--an update. Curr Opin Plant Biol 12:562–567

    Article  PubMed  CAS  Google Scholar 

  • Hautala EL, Wulff A, Oksanen J (1992) Effects of deicing salt on visible symptoms, element concentrations and membrane damage in first-year needles of roadside Scots pine (Pinus sylvestris). Ann Bot Fenn 29:179–185

    CAS  Google Scholar 

  • Hinsinger P, Plassard C, Tang C, Jaillard B (2003) Origins of root-mediated pH changes in the rhizosphere and their responses to environmental constraints: A review. Plant Soil 248:43–59

    Article  CAS  Google Scholar 

  • Hu Y, Burucs Z, Tucher S, Schmidhalter U (2007) Short-term effects of drought and salinity on mineral nutrient distribution along growing leaves of maize seedlings. Env and Exp Botany 60(2):268–275

    Article  CAS  Google Scholar 

  • Hu B, Simon J, Kuster MT, Rennenberg H (2013) Drought and air warming affect the levels of stress related metabolites in leaves of oak trees on acidic and calcareous soil. Tree Physiol 33:489–504

    Article  PubMed  CAS  Google Scholar 

  • Hu B, Zhou M, Dannenmann M, Saiz G, Simon J, Bilela S, Liu X, Hou L, Chen H, Zhang S, Butterbach-Bahl K, Rennenberg H (2017) Comparison of nitrogen nutrition and soil carbon status of afforestation stands established in degraded soil of the Loess Plateau, China. Forest Ecol Management 389:46–58

    Article  Google Scholar 

  • Ialicicco M, Viscosi V, Arena S, Scaloni A, Trupiano D, Rocco M, Chiatante D, Scippa GS (2012) Lens culinaris Medik. seed proteome: Analysis to identify landrace markers. Plant Sci 197:1–9

    Article  PubMed  CAS  Google Scholar 

  • Idrissi O, Udupa SM, De Keyser E, McGee RJ, Coyne CJ, Saha GC, Muehlbauer FJ, Van Damme P, De Riek J (2016) Identification of Quantitative Trait Loci Controlling Root and Shoot Traits Associated with Drought Tolerance in a Lentil (Lens culinaris Medik.) Recombinant Inbred Line Population. Front Plant Sci 7:1174. https://doi.org/10.3389/fpls.2016.01174

    Article  PubMed  PubMed Central  Google Scholar 

  • Kanani H, Dutta B, Klapa MI (2010) Individual vs. combinatorial effect of elevated CO2 conditions and salinity stress on Arabidopsis thaliana liquid cultures: comparing the early molecular response using time-series transcriptomic and metabolomic analyses. BMC Syst Biol 4:177

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Katerji N, Van Hoorn JW, Hamdy A, Mastrorilli M (2003). Salinity effect on crop development and yield, analysis of salt tolerance according to several classification methods. Agric. Water Manag 62:37–66

  • Kozlowski TT (1997) Responses of woody plants to flooding and salinity. Tree Physiol 1:13–21

    Google Scholar 

  • Lam HM, Coschigano KT, Oliveira IC, Melo-Oliveira R, Coruzzi GM (1996) The molecular-genetics of nitrogen assimilation into amino acids in higher plants. Annu Rev Plant Physiol Plant Mol Biol 47:569–593

    Article  PubMed  CAS  Google Scholar 

  • Li D, Su Z, Dong J, Wang T (2009) An expression database for roots of the model legume Medicago truncatula under salt stress. BMC Genomics 10:517

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lichtenthaler HK (1996) Vegetation Stress: An Introduction to the Stress Concept in Plants. Plant Physiol 148:4–14

    Article  CAS  Google Scholar 

  • Liu J, Ishitani M, Halfter U, Kim CS, Zhu JK (2000) The Arabidopsis thaliana SOS2 gene encodes a protein kinase that is required for salt tolerance. Proc Natl Acad Sci U S A 97:3730–3734

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444(2):139–158

    Article  PubMed  CAS  Google Scholar 

  • Miflin JB, Habash ZD (2002) The role of glutamine synthetase and glutamate dehydrogenase in nitrogen assimilation and possibilities for improvement in the nitrogen utilization of crops. J Exp Bot 53(370):979–987. https://doi.org/10.1093/jexbot/53.370.979

    Article  PubMed  CAS  Google Scholar 

  • Miller E, Mrowicka M, Malinowska K, Zolynski K, Józef K (2010) Effects of the whole-body cryotherapy on a total anti- oxidative status and activities of some antioxidative enzymes in blood of patients with multiple sclerosis- preliminary study. J Med Investig 57:168–173

    Article  Google Scholar 

  • Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250

    Article  PubMed  CAS  Google Scholar 

  • Munns R (2005) Genes and salt tolerance: Bringing them together. New Phytol 167:645–663

    Article  PubMed  CAS  Google Scholar 

  • O’Brien JΕ (1962) Automatic Analysis of Chlorides in Sewage. Wastes Eng 33:670–672

    Google Scholar 

  • Orcutt DM, Nilsen ET (2000) The Physiology of Plant Under Stress: Soil and Biotic Factors. Wiley

  • Pajuelo E, Stougaard J (2005) Lotus japonicus as a model system. Springer Netherlands, Dordrecht

    Google Scholar 

  • Polacco CJ, Holland AM (1993) Roles of Urease in plant cells. Intern rev of cytol 145

  • Patnaik P (2010) Handbook of environmental analysis: Chemical Pollutants in Air, Water, Soil, and Solid Wastes, Second edn. CRC Press, USA, FL, Boca Raton

  • Purvis JE, Yomano LP, Ingram LO (2005) Enhanced trehalose production improves growth of Escherichia coli under osmotic stress. Appl Environ Microbiol 71(7):3761–3769

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ramel F, Sulmon C, Gouesbet G, Couée I (2009) Natural variation reveals relationships between pre-stress carbohydrate nutritional status and subsequent responses to xenobiotic and oxidative stress in Arabidopsis thaliana. Ann Bot 104(7):1323–1337

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rao KR, Gnanam A (1990) Inhibition of nitrate and nitrite reductase activities by salinity stress in Sorghum vulgare. Phytochemistry 29:1047–1049

    Article  CAS  Google Scholar 

  • Rivero RM, Mestre TC, Mittler R, Rubio F, Garcia-Sanchez F, Martinez V (2014) The combined effect of salinity and heat reveals a specific physiological, biochemical and molecular response in tomato plants. Plant Cell Enviro 37:1059–1073

    Article  CAS  Google Scholar 

  • Sanchez DH, Lippold F, Redestig H, Hannah AM, Erban A, Kramer U, Kopka J, Udvardi KM (2008) Integrative functional genomics of salt acclimatization in the model legume Lotus japonicus. Plant J 53:973–987

    Article  PubMed  CAS  Google Scholar 

  • Sanchez DH, Pieckenstain F, Escaray F, Erban A, Kraemer U, Udvardi KM, Kopka J (2011a) Comparative ionomics and metabolomics in extremophile and glycophytic Lotus species under salt stress challenge the metabolic pre-adaptation hypothesis. Plant Cell Environ 34:605–617

    Article  PubMed  CAS  Google Scholar 

  • Sanchez DH, Pieckenstain F, Szymanski J, Erban A, Bromke M, Hannah AM, Kraemer U, Kopka J, Udvardi KM (2011b) Comparative functional genomics of salt stress in related model and cultivated plants identifies and overcomes limitations to translational genomics. PLoS One 6:14–19

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Sanchez DH, Szymanski J, Erban A, Udvardi MK, Kopka J (2010) Mining for robust transcriptional and metabolic responses to long-term salt stress: A case study on the model legume Lotus japonicus. Plant Cell Environ 33:468–480

    Article  PubMed  CAS  Google Scholar 

  • Schauer N, Steinhauser D, Strelkov S et al (2005) GC-MS libraries for the rapid identification of metabolites in complex biological samples. FEBS Lett 579:1332–1337

    Article  PubMed  CAS  Google Scholar 

  • Sirko A, Brodzik R (2000) Plant ureases: Roles and regulation. Acta Biochim Pol 47:1189–1195

    PubMed  CAS  Google Scholar 

  • Szabados L, Savouré A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15(2):89–97

    Article  PubMed  CAS  Google Scholar 

  • Tasic-Kostov M, Pavlovic D, Lukic M, Jaksic I, Arsic I, Savic S (2012) Lactobionic acid as antioxidant and moisturizing active in alkyl polyglucoside-based topical emulsions: The colloidal structure, stability and efficacy evaluation. Int J Cosmet Sci 34:424–434

    Article  PubMed  CAS  Google Scholar 

  • Tester M, Davenport R (2003) Na+ tolerance and Na+ transport in higher plants. Ann Bot 91:503–527

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tsikou D, Kalloniati C, Fotelli MN, Nikolopoulos D, Katinakis P, Udvardi MK, Rennenberg H, Flemetakis E (2013) Cessation of photosynthesis in Lotus japonicus leaves leads to reprogramming of nodule metabolism. J Exp Bot 64:1317–1332

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Van Hoorn JW, Katerji N, Hamdy A, Mastrorilli M (2001). Effect of salinity on yield and nitrogen uptake of four grain legumes and on biological nitrogen contribution from the soil. Agric Water Manag 51:87–98

  • Verbruggen N, Hermans C (2008) Proline accumulation in plants: a review. Amino Acids 35(4):753–759

    Article  PubMed  CAS  Google Scholar 

  • Vinocur B, Altman A (2005) Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. Cur Opin in Biotechn 16(2):123–132

    Article  CAS  Google Scholar 

  • Wang H, Liu D, Sun J, Zhang A (2005) Asparagine synthetase gene TaASN1 from wheat is up-regulated by salt stress, osmotic stress and ABA. J Plant Physiol 162:81–89

    Article  PubMed  CAS  Google Scholar 

  • Waterhouse RN, Smyth AJ, Massonneau A, Prosser IM, Clarkson DT (1996) Molecular cloning and characterisation of asparagine synthetase from Lotus japonicus: dynamics of asparagine synthesis in N-sufficient conditions. Plant Mol Biol 30:883–897

    Article  PubMed  CAS  Google Scholar 

  • Wu D, Cai S, Chen M, Ye L, Chen Z, Zhang H, Dai F, Wu F, Zhang G (2013) Tissue Metabolic Responses to Salt Stress in Wild and Cultivated Barley. PLoS One 8(1):e55431. https://doi.org/10.1371/journal.pone.0055431

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yousfi S, Serret MD, Márquez AJ, Voltas J, Araus JL (2012) Combined use of δ13C, δ18O and δ15N tracks nitrogen metabolism and genotypic adaptation of durum wheat to salinity and water deficit. New Phytol 194:230–244. https://doi.org/10.1111/j.1469-8137.2011.04036.x

    Article  PubMed  CAS  Google Scholar 

  • Zahaf O, Blanchet S, Zélicourt A, Alunni B, Plet J, Laffont C, Lorenzo L, Imbeaud S, Ichanté JL, Diet A, Badri M, Ana Zabalza A, Esther M, González EM, Delacroix H, Gruber V, Frugier F, Crespi M (2012) Comparative transcriptomic analysis of salt adaptation in roots of contrasting medicago truncatula genotypes. Mol Plant 5:1068–1081

    Article  PubMed  CAS  Google Scholar 

  • Zall DM, Fisher D, Garner MQ (1956) Photometric Determination of Chlorides in Water. Anal Chem 28:1665–1668

    Article  CAS  Google Scholar 

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Acknowledgements

The authors extend their sincere appreciation to the Deanship of Scientific Research at King Saud University for funding this Prolific Research Group (PRG-1436-24).

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EF and DS conceived the study and designed the research. DS, CK, GK and HR performed experimental work. DS and CK performed bioinformatics work. DS, CK and GK analyzed the data. EF, DS and CK wrote the draft manuscript. HR and GNS critical revised the draft manuscript and all the authors commented on the manuscript.

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Correspondence to Emmanouil Flemetakis.

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Responsible Editor: Wieland Fricke.

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Table S1

Average relative content of metabolites for variety F-56 and LC-960254 and their respective roots and leaves upon control and salinity treatments. (XLS 556 kb)

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Skliros, D., Kalloniati, C., Karalias, G. et al. Global metabolomics analysis reveals distinctive tolerance mechanisms in different plant organs of lentil (Lens culinaris) upon salinity stress. Plant Soil 429, 451–468 (2018). https://doi.org/10.1007/s11104-018-3691-9

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