Global metabolomics analysis reveals distinctive tolerance mechanisms in different plant organs of lentil (Lens culinaris) upon salinity stress
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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.
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.
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.
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.
KeywordsLens culinaris Lentil Metabolomics Abiotic Salinity Stress Purines Legumes
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).
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.
- 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 8:966–978CrossRefPubMedGoogle 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 21-38Google 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: 121–137Google Scholar
- Fiehn O, Barupal DK, Kind T (2011) Extending biochemical databases by metabolomic surveys. J Biol Chem 286(27):23637–23643Google 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 19:510–522Google Scholar
- Ghassemi F, Jakeman AJ, Nix HA (1995). Salinization of Land and Water Resources: Human Causes, Extent, Management and Case Studies. (CAB International)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 CrossRefGoogle 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
- 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 29:179–185Google 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 389:46–58CrossRefGoogle 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 CrossRefPubMedPubMedCentralGoogle 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 4:177CrossRefPubMedPubMedCentralGoogle 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 62:37–66Google Scholar
- Kozlowski TT (1997) Responses of woody plants to flooding and salinity. Tree Physiol 1:13–21Google Scholar
- O’Brien JΕ (1962) Automatic Analysis of Chlorides in Sewage. Wastes Eng 33:670–672Google Scholar
- Orcutt DM, Nilsen ET (2000) The Physiology of Plant Under Stress: Soil and Biotic Factors. WileyGoogle Scholar
- Pajuelo E, Stougaard J (2005) Lotus japonicus as a model system. Springer Netherlands, DordrechtGoogle Scholar
- Polacco CJ, Holland AM (1993) Roles of Urease in plant cells. Intern rev of cytol 145Google Scholar
- Patnaik P (2010) Handbook of environmental analysis: Chemical Pollutants in Air, Water, Soil, and Solid Wastes, Second edn. CRC Press, USA, FL, Boca RatonGoogle 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 6:14–19Google 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 51:87–98Google 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 5:1068–1081CrossRefPubMedGoogle Scholar