Salt-stress induced alterations in the root lipidome of two barley genotypes with contrasting responses to salinity
Siria H. A. Natera A D , Camilla B. Hill B C , Thusitha W. T. Rupasinghe A and Ute Roessner A B
+ Author Affiliations
- Author Affiliations
A Metabolomics Australia, School of BioSciences, BioSciences 2, Parkville, Vic. 3010, Australia.
B School of BioSciences, BioSciences 2, Parkville, Vic. 3010, Australia.
C Present address: Western Barley Genetics Alliance, Western Australian State Agricultural Biotechnology Centre, School of Veterinary and Life Sciences, Murdoch University, 90 South Street, Murdoch, WA 6150, Australia.
D Corresponding author. Email: s.natera@unimelb.edu.au
Functional Plant Biology 43(2) 207-219 https://doi.org/10.1071/FP15253
Submitted: 21 August 2015 Accepted: 12 November 2015 Published: 4 January 2016
Abstract
Changes in lipid metabolism and composition as well as in distinct lipid species have been linked with altered plant growth, development and responses to environmental stresses including salinity. However, there is little information available in the literature focusing on lipids in roots under soil-related stresses such as salinity. Barley (Hordeum vulgare L.) is a major cereal grain and, as a glycophyte, suffers substantial yield loss when grown under saline conditions. Relatively little is understood of adaptation and tolerance mechanisms involving lipids and lipid metabolism in barley roots during development and under exposure to salinity stress. In this study we investigated the lipid composition of barley roots of Clipper and Sahara – two genotypes with contrasting responses to salinity – before and after salinity stress using a combination of three lipidomics techniques: Fatty acid compositional analysis, untargeted lipid profiling, and targeted analysis to profile quantitatively the individual molecular species of key plant lipid classes. Our results provide new insight into the effect of salinity on fatty acid profiles and key lipid classes within barley roots of two different genotypes, which is discussed in the context of current knowledge of the root metabolic responses of cereal crops to salinity stress.
Additional keywords: Hordeum vulgare, lipid metabolism, lipidomics, mass spectrometry, salinity.
References
Adem GD, Roy SJ, Zhou M, Bowman JP, Shabala S (2014) Evaluating contribution of ionic, osmotic and oxidative stress components towards salinity tolerance in barley. BMC Plant Biology 14, 113| Evaluating contribution of ionic, osmotic and oxidative stress components towards salinity tolerance in barley.Crossref | GoogleScholarGoogle Scholar | 24774965PubMed |
Blanksby SJ, Mitchell TW (2010) Advances in mass spectrometry for lipidomics. Annual Review of Analytical Chemistry (Palo Alto, Calif.) 3, 433–465.
| Advances in mass spectrometry for lipidomics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVOlsr3J&md5=96caf8d353af1d37af5877281ca01c6dCAS |
Brown DJ, DuPont FM (1989) Lipid composition of plasma membranes and endomembranes prepared from roots of barley (Hordeum vulgare L.): effects of salt. Plant Physiology 90, 955–961.
| Lipid composition of plasma membranes and endomembranes prepared from roots of barley (Hordeum vulgare L.): effects of salt.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXlvFWntbg%3D&md5=cb30989d0e32ab56936eef66646a6f83CAS | 16666904PubMed |
Carruthers A, Melchior DJ (1986) How bilayer lipids affect membrane protein activity. Trends in Biochemical Sciences 11, 331–335.
| How bilayer lipids affect membrane protein activity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28Xls1Kqsbg%3D&md5=f844da252b347f57796764ec006648eaCAS |
Chalbi N, Martínez-Ballesta MC, Youssef NB, Carvajal M (2015) Intrinsic stability of Brassicaceae plasma membrane in relation to changes in proteins and lipids as a response to salinity. Journal of Plant Physiology 175, 148–156.
| Intrinsic stability of Brassicaceae plasma membrane in relation to changes in proteins and lipids as a response to salinity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXislKjuw%3D%3D&md5=2df407c71eed7cf8e26599a53802e614CAS | 25544590PubMed |
Cooke DT, Burden RS (1990) Lipid modulation of plasma membrane-bound ATPases. Physiologia Plantarum 78, 153–159.
| Lipid modulation of plasma membrane-bound ATPases.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXhsFCjtr4%3D&md5=f3df1130846434c3fd6e5ad087ddbc0cCAS |
Devaiah SP, Roth MR, Baughman E, Li M, Tamura P, Jeannotte R, Welti R, Wang X (2006) Quantitative profiling of polar glycerolipid species from organs of wild-type Arabidopsis and a PHOSPHOLIPASE Dα1 knockout mutant. Phytochemistry 67, 1907–1924.
| Quantitative profiling of polar glycerolipid species from organs of wild-type Arabidopsis and a PHOSPHOLIPASE Dα1 knockout mutant.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XovVSisbo%3D&md5=ecb0320647dd7e9bfec6e1815f6b649cCAS | 16843506PubMed |
DuPont FM, Tanaka CK, Hurkman WJ (1988) Separation and immunological characterization of membrane fractions from barley roots. Plant Physiology 86, 717–724.
| Separation and immunological characterization of membrane fractions from barley roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXitVSgs7g%3D&md5=c2d27433126dbee6f0d7cfe38b135a22CAS | 16665976PubMed |
Fahy E, Cotter D, Byrnes R, Sud M, Maer A, Li J, Nadeau D, Zhau Y, Subramaniam S (2007a). Bioinformatics for lipidomics. In ‘Methods in enzymology’. (Ed. HA Brown) pp. 247–273. (Academic Press: New York)
Fahy E, Sud M, Cotter D, Subramaniam S (2007b) LIPID MAPS online tools for lipid research. Nucleic Acids Research 35, W606–W612.
| LIPID MAPS online tools for lipid research.Crossref | GoogleScholarGoogle Scholar | 17584797PubMed |
Fahy E, Subramaniam S, Murphy R, Nishijima M, Raetz C, Shimizu T, Spener F, van Meer G, Wakelam M, Dennis EA (2009) Update of the LIPID MAPS comprehensive classification system for lipids. Journal of Lipid Research 50, S9–S14.
| Update of the LIPID MAPS comprehensive classification system for lipids.Crossref | GoogleScholarGoogle Scholar | 19098281PubMed |
FAO (2012) Food and Agriculture Organization of the United Nations (FAO) statistical databases. Available at http://faostat.fao.org [Verified 20 August 2015]
Flowers TJ, Munns R, Colmer TD (2015) Sodium chloride toxicity and the cellular basis of salt tolerance in halophytes. Annals of Botany 115, 419–431.
| Sodium chloride toxicity and the cellular basis of salt tolerance in halophytes.Crossref | GoogleScholarGoogle Scholar | 25466549PubMed |
Genc Y, McDonald GK, Tester M (2007) Reassessment of tissue Na+ concentration as a criterion for salinity tolerance in bread wheat. Plant, Cell & Environment 30, 1486–1498.
| Reassessment of tissue Na+ concentration as a criterion for salinity tolerance in bread wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1yhsrbE&md5=0defca1b02c8884e3c38b24c4840f436CAS |
Greenway H, Munns R (1980) Mechanisms of salt tolerance in Nonhalophytes. Annual Review of Plant Physiology 31, 149–190.
| Mechanisms of salt tolerance in Nonhalophytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXksVWntb4%3D&md5=61cb9bcc484c17fdb79bcc6025e26374CAS |
Hill CB, Bacic A, Roessner U (2014) LC-MS profiling to link metabolic and phenotypic diversity in plant mapping populations. In ‘Mass spectrometry in metabolomics’. pp. 29–41. (Springer: New York)
Horn PJ, Chapman KD (2011) Organellar lipidomics. Plant Signaling & Behavior 6, 1594–1596.
| Organellar lipidomics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XjsVGhsbs%3D&md5=1056457a015fadb7beca2e0946a970cfCAS |
Horn PJ, Chapman KD (2012) High-resolution measurements in plant biology: lipidomics in tissues, cells and subcellular compartments. The Plant Journal 70, 69–80.
| High-resolution measurements in plant biology: lipidomics in tissues, cells and subcellular compartments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XmtVKnu7Y%3D&md5=9fb8c947550dfce59371bb3838289055CAS | 22117762PubMed |
Hu CH, van Dommelen J, van der Heijden R, Spijksma G, Reijmers TH, Wang M, Slee E, Lu X, Xu G, van der Greef J, Hankemeier T (2008) RPLC-Ion-Trap-FTMS method for lipid profiling of plasma: method validation and application to p53 mutant mouse model. Journal of Proteome Research 7, 4982–4991.
| RPLC-Ion-Trap-FTMS method for lipid profiling of plasma: method validation and application to p53 mutant mouse model.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1WjsrzF&md5=dce41e6cd574b94a39b12fcbc54af4f5CAS |
Karakousis A, Barr AR, Kretschmer JM, Manning S, Jefferies SP, Chalmers KJ, Islam AKM, Langridge P (2003) Mapping and QTL analysis of the barley population Clipper× Sahara. Crop and Pasture Science 54, 1137–1140.
| Mapping and QTL analysis of the barley population Clipper× Sahara.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpvV2mtLs%3D&md5=6cc6e68bcb8a07602f05970863778019CAS |
Lee AG (2004) How lipids affect the activities of integral membrane proteins. Biochimica et Biophysica Acta (BBA) – Biomembranes 1666, 62–87.
| How lipids affect the activities of integral membrane proteins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXptFOktLw%3D&md5=64368fed44716e4f5c1e66401ae1573bCAS |
Lee YJ, Perdian DC, Song Z, Yeung ES, Nikolau BJ (2012) Use of mass spectrometry for imaging metabolites in plants. The Plant Journal 70, 81–95.
| Use of mass spectrometry for imaging metabolites in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XmtVKmsr4%3D&md5=bb6642b6f1ac783e36c4b7770ce30171CAS | 22449044PubMed |
Mansour MMF (2013) Plasma membrane permeability as an indicator of salt tolerance in plants. Biologia Plantarum 57, 1–10.
| Plasma membrane permeability as an indicator of salt tolerance in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXnt12ksrw%3D&md5=955cd8366508ccd3f7ecb580e441f08aCAS |
Meijer HJ, Munnik T (2003) Phospholipid-based signaling in plants. Annual Review of Plant Biology 54, 265–306.
| Phospholipid-based signaling in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXntFSgu7g%3D&md5=066ed27d3369a2502174e04e708cf140CAS | 14502992PubMed |
Mittler R (2006) Abiotic stress, the field environment and stress combination. Trends in Plant Science 11, 15–19.
| Abiotic stress, the field environment and stress combination.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjvVKjsw%3D%3D&md5=4c94697f7fe05499ac12ded3c5b6d58aCAS | 16359910PubMed |
Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annual Review of Plant Biology 59, 651–681.
| Mechanisms of salinity tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXntFaqtrw%3D&md5=dd68a82a6d2c6414e1266213f98edac3CAS | 18444910PubMed |
Narasimhan R, Wang G, Li M, Roth M, Welti R, Wang X (2013) Differential changes in galactolipid and phospholipid species in soybean leaves and roots under nitrogen deficiency and after nodulation. Phytochemistry 96, 81–91.
| Differential changes in galactolipid and phospholipid species in soybean leaves and roots under nitrogen deficiency and after nodulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhs1CqsL7O&md5=e1a08c94e44dd57f3e5a30edb29f8820CAS | 24139145PubMed |
Okazaki Y, Saito K (2014) Roles of lipids as signaling molecules and mitigators during stress response in plants. The Plant Journal 79, 584–596.
| Roles of lipids as signaling molecules and mitigators during stress response in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtlaktb3K&md5=73dcc2fa8c6018c3466307b206f63b1dCAS | 24844563PubMed |
Okazaki Y, Kamide Y, Hirai MY, Saito K (2013) Plant lipidomics based on hydrophilic interaction chromatography coupled to ion trap time-of-flight mass spectrometry. Metabolomics 9, 121–131.
| Plant lipidomics based on hydrophilic interaction chromatography coupled to ion trap time-of-flight mass spectrometry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjtFSgsLg%3D&md5=72dac9ae0c5e70779f8f7ab92515610bCAS | 23463370PubMed |
Olmstead ILD, Hill DRA, Dias DA, Jayasinghe NS, Callahan DL, Kentish SE, Scales PJ, Martin GJO (2013) A quantitative analysis of microalgal lipids for optimization of biodiesel and omega-3 production. Biotechnology and Bioengineering 110, 2096–2104.
| A quantitative analysis of microalgal lipids for optimization of biodiesel and omega-3 production.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXit1Kqt7o%3D&md5=15a27fd8b53972278faeec7aad52ac57CAS |
Pluskal T, Castillo S, Villar-Briones A, Orešič M (2010) MZmine 2: Modular framework for processing, visualizing, and analyzing mass spectrometry-based molecular profile data. BMC Bioinformatics 11, 395
| MZmine 2: Modular framework for processing, visualizing, and analyzing mass spectrometry-based molecular profile data.Crossref | GoogleScholarGoogle Scholar | 20650010PubMed |
Ren M, Phoon CKL, Schlame M (2014) Metabolism and function of mitochondrial cardiolipin. Progress in Lipid Research 55, 1–16.
| Metabolism and function of mitochondrial cardiolipin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtlCjtr7J&md5=f9c009ab5ea20c54640ab4298b556bf2CAS | 24769127PubMed |
Samarakoon T, Shiva S, Lowe K, Tamura P, Roth MR, Welti R (2012) Arabidopsis thaliana membrane lipid molecular species and their mass spectral analysis. High-Throughput Phenotyping in Plants: Methods and Protocols 918, 179–268.
Shelden MC, Roessner U, Sharp RE, Tester M, Bacic A (2013) Genetic variation in the root growth response of barley genotypes to salinity stress. Functional Plant Biology 40, 516–530.
| Genetic variation in the root growth response of barley genotypes to salinity stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXnsFSnsrs%3D&md5=d29698330935b35b5253a57f8dbf7a21CAS |
Shi BJ, Sutton T, Collins NC, Pallotta M, Langridge P (2010) Construction of a barley bacterial artificial chromosome library suitable for cloning genes for boron tolerance, sodium exclusion and high grain zinc content. Plant Breeding 129, 291–296.
| Construction of a barley bacterial artificial chromosome library suitable for cloning genes for boron tolerance, sodium exclusion and high grain zinc content.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXot1eqsr0%3D&md5=b61252fd7badabceea31be1c8dbad457CAS |
Shiva S, Vu HS, Roth MR, Zhou Z, Marepally SR, Nune DS, Lushington GH, Visvanathan M, Welti R (2013) Lipidomic analysis of plant membrane lipids by direct infusion tandem mass spectrometry. Plant Lipid Signaling Protocols 1009, 79–91.
Sommer B (2013) Membrane packing problems: a short review on computational membrane modeling methods and tools. Computational and Structural Biotechnology Journal 5, 1–13.
| Membrane packing problems: a short review on computational membrane modeling methods and tools.Crossref | GoogleScholarGoogle Scholar |
Spychalla JP, Desborough SL (1990) Fatty acids, membrane permeability, and sugars of stored potato tubers. Plant Physiology 94, 1207–1213.
| Fatty acids, membrane permeability, and sugars of stored potato tubers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXit1Kmtg%3D%3D&md5=f0b6236c79be963c144d1ccfa39edcbdCAS | 16667818PubMed |
Surjus A, Durand M (1996) Lipid changes in soybean root membranes in response to salt treatment. Journal of Experimental Botany 47, 17–23.
| Lipid changes in soybean root membranes in response to salt treatment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XhtlajtL8%3D&md5=463a8cc06d1a23e7284500bcce370363CAS |
Tavakkoli E, Rengasamy P, McDonald GK (2010) High concentrations of Na+ and Cl– ions in soil solution have simultaneous detrimental effects on growth of faba bean under salinity stress. Journal of Experimental Botany 61, 4449–4459.
| High concentrations of Na+ and Cl– ions in soil solution have simultaneous detrimental effects on growth of faba bean under salinity stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlShtLbK&md5=f330ab73e11836de0a9a328121db4bceCAS | 20713463PubMed |
Upchurch RG (2008) Fatty acid unsaturation, mobilization, and regulation in the response of plants to stress. Biotechnology Letters 30, 967–977.
| Fatty acid unsaturation, mobilization, and regulation in the response of plants to stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXkvV2rsb0%3D&md5=82e6974b2691ce60d71a2e6939985914CAS | 18227974PubMed |
van Meer G (2005) Cellular lipidomics. EMBO Journal 24, 3159–3165.
| Cellular lipidomics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVajsrjF&md5=8bdf9138b6eb37069608f649b881f302CAS | 16138081PubMed |
van Meer G, Voelker DR, Feigenson GW (2008) Membrane lipids: where they are and how they behave. Nature Reviews. Molecular Cell Biology 9, 112–124.
| Membrane lipids: where they are and how they behave.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXovFOntw%3D%3D&md5=1d950d504a08468a38fefa99fb510e64CAS | 18216768PubMed |
Walia H, Wilson C, Condamine P, Liu X, Ismail AM, Close TJ (2007) Large-scale expression profiling and physiological characterization of jasmonic acid-mediated adaptation of barley to salinity stress. Plant, Cell & Environment 30, 410–421.
| Large-scale expression profiling and physiological characterization of jasmonic acid-mediated adaptation of barley to salinity stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXksVemuro%3D&md5=107f797ec389d2e9f37868c8c0fedb6dCAS |
Wang X (2002) Phospholipase D in hormonal and stress signalling. Current Opinion in Plant Biology 5, 408–414.
| Phospholipase D in hormonal and stress signalling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XmtlGjtLg%3D&md5=b6f82dfb12b3f40ec21d1d426f9bc652CAS | 12183179PubMed |
Weber H (2002) Fatty acid-derived signals in plants. Trends in Plant Science 7, 217–224.
| Fatty acid-derived signals in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xjtl2kt7o%3D&md5=3210e878ee5b44fbb416b2536a59d16fCAS | 11992827PubMed |
Welti R, Wang X (2004) Lipid species profiling: a high-throughput approach to identify lipid compositional changes and determine the function of genes involved in lipid metabolism and signaling. Current Opinion in Plant Biology 7, 337–344.
| Lipid species profiling: a high-throughput approach to identify lipid compositional changes and determine the function of genes involved in lipid metabolism and signaling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjvVamsLY%3D&md5=d5f70444a23763036fd85b45b32d00bbCAS | 15134756PubMed |
Wenk MR (2005) The emerging field of lipidomics. Nature Reviews. Drug Discovery 4, 594–610.
| The emerging field of lipidomics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmsFGjtbs%3D&md5=785f29e7e7f00ed9106aa7616316f3a8CAS | 16052242PubMed |
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. Journal of Experimental Botany 60, 4089–4103.
| Metabolic responses to salt stress of barley (Hordeum vulgare L.) cultivars, Sahara and Clipper, which differ in salinity tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXht1WqtLnF&md5=d48281b2a470d88776d278c5d41e7693CAS | 19666960PubMed |
Wu J, Seliskar DM, Gallagher JL (2005) The response of plasma membrane lipid composition in callus of the halophyte Spartina patens (Poaceae) to salinity stress. American Journal of Botany 92, 852–858.
| The response of plasma membrane lipid composition in callus of the halophyte Spartina patens (Poaceae) to salinity stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXks1WqsLk%3D&md5=3003a18732b3af044814a3448518f628CAS | 21652466PubMed |
Xia J, Sinelnikov IV, Han B, Wishart DS (2015) MetaboAnalyst 3.0 – making metabolomics more meaningful. Nucleic Acids Research 43, W251–W257.
| MetaboAnalyst 3.0 – making metabolomics more meaningful.Crossref | GoogleScholarGoogle Scholar | 25897128PubMed |
Yoon JY, Hamayun M, Lee SK, Lee IJ (2009) Methyl jasmonate alleviated salinity stress in soybean. Journal of Crop Science and Biotechnology 12, 63–68.
| Methyl jasmonate alleviated salinity stress in soybean.Crossref | GoogleScholarGoogle Scholar |
Zhou X-R, Callahan DL, Shrestha P, Liu Q, Petrie JR, Singh SP (2014) Lipidomic analysis of Arabidopsis seed genetically engineered to contain DHA. Frontiers in Plant Science 5, 419
| Lipidomic analysis of Arabidopsis seed genetically engineered to contain DHA.Crossref | GoogleScholarGoogle Scholar | 25225497PubMed |
