Abstract
Aims
Maize is exposed to the combined stresses of water deficiency and soil salinity within its natural habitat, particularly in irrigated and dry land agricultural areas. Hence, the effect of these combined stresses on the metabolic response of maize plants was determined to improve understanding of stress tolerance mechanisms of maize in the field.
Methods
Maize plants were either singly or simultaneously exposed to soil water deficiency and high salinity for 7 d. Physiological characteristics were analyzed and metabolic changes were quantified by conducting 1H NMR-based analysis of polar and non-polar fractions of maize leaf extracts.
Results
The response of maize plants to the combined stresses was distinct from that of plants subjected to either drought stress or salt stress alone at both the metabolic and physiological level. Maize plants showed a new pattern of metabolic response to the combined stresses. Some metabolites specifically responded to combined stresses and differed from those caused by each stress applied individually. The global metabolic response of maize to the combined stresses was related to the physiological processes.
Conclusions
Our results provide valuable insights into the response of maize to combined drought and salt stress by linking stress-related physiological responses to changes in metabolites.
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References
Alla MMN, Khedr AHA, Serag MM, Abu-Alnaga AZ, Nada RM (2012) Regulation of metabolomics in Atriplex halimus growth under salt and drought stress. Plant Growth Regul 67:281–304. doi:10.1007/s10725-012-9687-1
Ansari MI, Lee R-H, Chen S-CG (2005) A novel senescence associated gene encoding γ-aminobutyric acid (GABA): pyruvate transaminase is upregulated during rice leaf senescence. Physiol Plant 123:1–8. doi:10.1111/j.1399-3054.2004.00430.x
Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399. doi:10.1146/annurev.arplant.55.031903.141701
Araújo WL, Ishizaki K, Nunes-Nesi A, Larson TR, Tohge T, Krahnert I, Witt S, Obata T, Schauer N, Graham IA, Leaver CJ, Fernie AR (2010) Identification of the 2-Hydroxyglutarate and isovaleryl-CoA dehydrogenases as alternative electron donors linking lysine catabolism to the electron transport chain of Arabidopsis mitochondria. Plant Cell 22:1549–1563. doi:10.1105/tpc.110.075630
Ashraf M, McNeally T (1990) Improvement of salt tolerance in maize for selection and breeding. Plant Breed 104:101–107. doi:10.1111/j.1439-0523.1990.tb00410.x
Bentley R (1990) The shikimate pathway- a metabolic tree with many branches. Crit Rev Biochem Mol Biol 25:307–384. doi:10.3109/10409239009090615
Bouché N, Fromm H (2004) GABA in plants: just a metabolite? Trends Plant Sci 9:110–115. doi:10.1016/j.tplants.2004.01.006
Boyer JS (1982) Plant productivity and environment. Sci 218:443–448. doi:10.1126/science.218.4571.443
Carreno-Quintero N, Bouwmeester HJ, Keurentjes JJB (2013) Genetic analysis of metabolome- phenotype interactions: from model to crop species. Trends Genet 29:41–50. doi:10.1016/j.tig.2012.09.006
Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 103:551–560. doi:10.1093/aob/mcn125
Chaves MM, Oliveira MM (2004) Mechanisms underlying plant resilience to water deficits: prospects for water-saving agriculture. J Exp Bot 55:2365–2384. doi:10.1093/jxb/erh269
Cheeseman JM (1988) Mechanisms of salinity tolerance in plants. Plant Physiol 87:547–550. doi:10.1104/pp. 87.3.547
Chen THH, Murata N (2011) Glycinebetaine protects plants against abiotic stress: mechanisms and biotechnological applications. Plant Cell Environ 34:1–20. doi:10.1111/j.1365-3040.2010.02232.x
Chinnusamy V, Schumaker K, Zhu JK (2004) Molecular genetic perspectives on cross-talk and specificity in abiotic stress signalling in plants. J Exp Bot 55:225–236. doi:10.1093/jxb/erh005
Choi YH, Tapias EC, Kim HK, Lefeber AWM, Erkelens C, Verhoeven JT, Brzin J, Zel J, Verpoorte R (2004) Metabolic discrimination of Catharanthus roseus leaves infected by phytoplasma using 1H-NMR spectroscopy and multivariate data analysis. Plant Physiol 135:2398–2410. doi:10.1104/pp. 104.041012
Cramer G, Ergűl A, Grimplet J, Tillett R, Tattersall E, Bohlman M, Vincent D, Sonderegger J, Evans J, Osborne C, Quilici D, Schlauch K, Schooley D, Cushman J (2007) Water and salinity stress in grapevines: early and late changes in transcript and metabolite profiles. Funct Integr Genomic 7:111–134. doi:10.1007/s10142-006-0039-y
Dakhma WS, Zarrouk M, Cherif A (1995) Effects of drought-stress on lipids in rape leaves. Phytochem 40:1383–1386. doi:10.1016/0031-9422(95)00459-K
Ding D, Zhang L, Wang H, Liu Z, Zhang Z, Zheng Y (2009) Differential expression of miRNAs in response to salt stress in maize roots. Ann Bot 103:29–38. doi:10.1093/aob/mcn205
Ericsson T (1995) Growth and shoot:root ratio of seedlings in relation to nutrient availability. Plant Soil 168:205–214. doi:10.1007/BF00029330
Fan TWM (1996) Metabolite profiling by one- and two-dimensional NMR analysis of complex mixtures. Prog Nucl Magn Reson Spectrosc 28:161–219
Fiehn O (2002) Metabolomics-the link between genotypes and phenotypes. Plant Mol Biol 48:155–171. doi:10.1007/978-94-010-0448-0_11
Flowers TJ (2004) Improving crop salt tolerance. J Exp Bot 55:307–319. doi:10.1093/jxb/erh003
Gavaghan CL, Li JV, Hadfield ST, Hole S, Nicholson Je K, Wilson ID, Howe PWA, Stanley PD, Holmes E (2011) Application of NMR-based metabolomics to the investigation of salt stress in maize (Zea mays). Phytochem Anal 22:214–224. doi:10.1002/pca.1268
Gigon A, Matos AR, Laffray D, Zuily-Fodil Y, Pham-Thi AT (2004) Effect of drought stress on lipid metabolism in the leaves of Arabidopsis thaliana (Ecotype Columbia). Ann Bot 94:345–351. doi:10.1093/aob/mch150
Glass ADM, Britto DT, Kaiser BN, Kinghorn JR, Kronzucker HJ, Kumar A, Okamoto M, Rawat S, Siddiqi MY, Unkles SE, Vidmar JJ (2002) The regulation of nitrate and ammonium transport systems in plants. J Exp Bot 53:855–864. doi:10.1093/jexbot/53.370.855
Gomez-Merino FC, Arana-Ceballos FA, Trejo-Tellez LI, Skirycz A, Brearley CA, Dormann P, Mueller-Roeber B (2005) Arabidopsis AtDGK7, the smallest member of plant diacylglycerol kinases (DGKs), displays unique biochemical features and saturates at low substrate concentration: the DGK inhibitor R59022 differentially affects AtDGK2 and AtDGK7 activity in vitro and alters plant growth and development. J Biol Chem 280:34888–34899. doi:10.1074/jbc.M506859200
Guevara DR, Champigny MJ, Tattersall A, Dedrick J, Wong CE, Li Y, Labbe A, Ping CL, Wang Y, Nuin P, Golding GB, McCarry BE, Summers PS, Moffatt BA, Weretilnyk EA (2012) Transcriptomic and metabolomic analysis of Yukon Thellungiella plants grown in cabinets and their natural habitat show phenotypic plasticity. BMC Plant Biol 12:175-192. doi:10.1186/1471-2229-12-175
Gupta AK, Kaur N (2005) Sugar signalling and gene expression in relation to carbohydrate metabolism under abiotic stresses in plants. J Biosci 30:761–776. doi:10.1007/BF02703574
Hanson J, Smeekens S (2009) Sugar perception and signaling - an update. Curr Opin Plant Biol 12:562–567. doi:10.1016/j.pbi.2009.07.014
Hill CB, Taylor JD, Edwards J, Mather D, Bacic A, Langridge P, Roessner U (2013) Whole-genome mapping of agronomic and metabolic traits to identify novel quantitative trait loci in bread wheat grown in a water-limited environment. Plant Physiol 162:1266–1281. doi:10.1104/pp. 113.217851
Iyer S, Caplan A (1998) Products of proline catabolism can induce osmotically regulated genes in rice. Plant Physiol 116:203–211. doi:10.1104/pp. 116.1.203
Jacob J, Lawlor DW (1991) Stomatal and mesophyll limitations of photosynthesis in phosphate deficient sunflower, maize and wheat plants. J Exp Bot 42:1003–1011. doi:10.1093/jxb/42.8.1003
Joshi V, Joung JG, Fei Z, Jander G (2010) Interdependence of threonine, methionine and isoleucine metabolism in plants: accumulation and transcriptional regulation under abiotic stress. Amino Acids 39:933–947. doi:10.1007/s00726-010-0505-7
Kim HK, Choi YH, Verpoorte R (2010) NMR-based metabolomic analysis of plants. Nat Protoc 5:536–549. doi:10.1038/nprot.2009.237
Kim JK, Bamba T, Harada K, Fukusaki E, Kobayashi A (2007) Time-course metabolic profiling in Arabidopsis thaliana cell cultures after salt stress treatment. J Exp Bot 58:415–424. doi:10.1093/jxb/erl216
Krasensky J, Jonak C (2012) Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. J Exp Bot 63:1593–1608. doi:10.1093/jxb/err460
Krishnan P, Kruger NJ, Ratcliffe RG (2005) Metabolite fingerprinting and profiling in plants using NMR. J Exp Bot 56:255–265. doi:10.1093/jxb/eri010
Lawlor DW (2002) Carbon and nitrogen assimilation in relation to yield: mechanisms are the key to understanding production systems. J Exp Bot 53:773–787. doi:10.1093/jexbot/53.370.773
Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: An overview. Arch Biochem Biophys 444:139–158. doi:10.1016/j.abb.2005.10.018
Martin BA, Schoper JB, Whinne R (1986) Change in soybean (Glycin max [L.] Merr.) glycerolipids in response to water stress. Plant Physiol 81:798–801. doi:10.1104/pp. 81.3.798
Martínez JP, Kinet JM, Bajji M, Lutts S (2005) NaCl alleviates polyethylene glycol induced water stress in the halophyte species Atriplex halimus L. J Exp Bot 56:2421–2131. doi:10.1093/jxb/eri235
Mattoo AK, Sobolev AP, Neelam A, Goyal RK, Handa AK, Segre AL (2006) Nuclear magnetic resonance spectroscopy-based metabolite profiling of transgenic tomato fruit engineered to accumulate spermidine and spermine reveals enhanced anabolic and nitrogen-carbon interactions. Plant Physiol 142:1759–1770. doi:10.1104/pp. 106.084400
McNeil SD, Nuccio ML, Ziemak MJ, Hanson AD (2001) Enhanced synthesis of choline and glycine betaine in transgenic tobacco plants that overexpress phosphoethanolamine N-methyltransferase. Proc Natl Acad Sci U S A 98:10001–10005. doi:10.1073/pnas.171228998
Mittler R (2006) Abiotic stress, the field environment and stress combination. Trends Plant Sci 11:15–19. doi:10.1016/j.tplants.2005.11.002
Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250. doi:10.1046/j.0016-8025.2001.00808.x
Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681. doi:10.1146/annurev.arplant.59.032607.092911
Nunes-Nesi A, Fernie AR, Stitt M (2010) Metabolic and signaling aspects underpinning the regulation of plant carbon nitrogen interactions. Mol Plant 3:973–996. doi:10.1093/mp/ssq049
Obata T, Fernie AR (2012) The use of metabolomics to dissect plant responses to abiotic stresses. Cell Mol Life Sci 69:3225–3243. doi:10.1007/s00018-012-1091-5
Oki T, Kanae S (2006) Global hydrological cycles and world water resources. Sci 313:1068–1072. doi:10.1126/science.1128845
Opitz N, Paschold A, Marcon C, Malik WA, Lanz C, Piepho HP, Hochholdinger F (2014) Transcriptomic complexity in young maize primary roots in response to low water potentials. BMC Genomics 15:741–754. doi:10.1186/1471-2164-15-741
Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environ Saf 60:324–349. doi:10.1016/j.ecoenv.2004.06.010
Pérez-Pérez JG, Syvertsen JP, Botía P, García-Sánchez F (2007) Leaf water relations and net gas exchange responses of salinized Carrizo citrange seedlings during drought stress and recovery. Ann Bot 100:335–345. doi:10.1093/aob/mcm113
Pinheiro C, Chaves MM (2011) Photosynthesis and drought: can we make metabolic connections from available data? J Exp Bot 62:869–882. doi:10.1093/jxb/erq340
Rabbani MA, Maruyama K, Abe H, Khan MA, Katsura K, Ito Y, Yoshiwara K, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Monitoring expression profiles of rice genes under cold, crought, and high-salinity stresses and abscisic acid application using cDNA microarray and RNA gel-blot analyses. Plant Physiol 133:1755–1767. doi:10.1104/pp. 103.025742
Ramel F, Sulmon C, Gouesbet G, Couee 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 104:1323–1337. doi:10.1093/aob/mcp243
Rivas-Ubacha A, Sardansa J, Pérez-Trujillob M, Estiartea M, Peñuelasa J (2012) Strong relationship between elemental stoichiometry and metabolome in plants. PNAS 109:4181–4186. doi:10.1073/pnas.1116092109
Rizhsky L, Liang H, Shuman J, Shulaev V, Davletova S, Mittler R (2004) When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiol 134:1683–1696. doi:10.1104/pp. 103.033431
Rolland F, Baena-Gonzalez E, Sheen J (2006) Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu Rev Plant Biol 57:675–709. doi:10.1146/annurev.arplant.57.032905.105441
Rozema J, Flowers T (2008) Ecology: crops for a salinized world. Sci 322:1478–1480. doi:10.1126/science.1168572
Sanchez DH, Pieckenstain FL, Escaray F, Erban A, Kraemer U, Udvardi MK, Kopka J (2011) 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. doi:10.1111/j.1365-3040.2010.02266.x
Sato S, Yanagisawa S (2014) Characterization of metabolic states of Arabidopsis thaliana under diverse carbon and nitrogen nutrient conditions via targeted metabolomic analysis. Plant Cell Physiol 55:306–319. doi:10.1093/pcp/pct192
Schlüter U, Colmsee C, Scholz U, Bräutigam A, Weber APM, Zellerhoff N, Bucher M, Fahnenstich H, Sonnewald U (2013) Adaptation of maize source leaf metabolism to stress related disturbances in carbon, nitrogen and phosphorus balance. BMC Genomics 14:442–467. doi:10.1186/1471-2164-14-442
Seebauer JR, Moose SP, Fabbri BJ, Crossland LD, Below FE (2004) Amino acid metabolism in young maize earshoots: implications for assimilate movement and nitrogen signaling. Plant Physiol 136:4326–4334. doi:10.1104/pp. 104.043778
Shalhevet J (1994) Using water of marginal quality for crop production: major issues. Agric Water Manag 25:233–269. doi:10.1016/0378-3774(94)90063-9
Shani U, Dudley LM (2001) Field studies of crop response to water and salt stress. Soil Sci Soc Am J 65:1522–1528. doi:10.2136/sssaj2001.6551522x
Shelp BJ, Bown AW, McLean MD (1999) The metabolism and functions of gamma aminobutyric acid. Trends Plant Sci 4:446–452. doi:10.1016/S1360-1385(99)01486-7
Shulaev V, Cortes D, Miller G, Mittler R (2008) Metabolomics for plant stress response. Plant Physiol 132:199–208. doi:10.1111/j.1399-3054.2007.01025.x
Sidhu OP, Annarao S, Chatterjee S, Tuli R, Roy R, Khetrapal CL (2011) Metabolic alterations of Withania somnifera (L.) dunal fruits at different developmental stages by NMR spectroscopy. Phytochem Anal 22:492–502. doi:10.1002/pca.1307
Slama I, Ghnaya T, Savouré A, Abdelly C (2008) Combined effects of long-term salinity and soil drying on growth, water relations, nutrient status and proline accumulation of Sesuvium portulacastrum. CR Biol 331:442–451. doi:10.1016/j.crvi.2008.03.006
Sucre B, Suárez N (2011) Effect of salinity and PEG-induced water stress on water status, gas exchange, solute accumulation, and leaf growth in Ipomoea pes-caprae. Environ Exp Bot 70:192–203. doi:10.1016/j.envexpbot.2010.09.004
Tate AR, Damment SJP, Lindon JC (2001) Investigation of the metabolite variation in control rat urine using 1H NMR. Anal Biochem 291:17–26. doi:10.1006/abio.2001.5008
Tavakkoli E, Rengasamy P, McDonald GK (2010) The response of barley to salinity stress differs between hydroponic and soil systems. Funct Plant Biol 37:621–633. doi:10.1071/FP09202
Verslues PE, Juenger TE (2011) Drought, metabolites, and Arabidopsis natural variation: a promising combination for understanding adaptation to water-limited environments. Curr Opin Plant Biol 14:240–245. doi:10.1016/j.pbi.2011.04.006
Ward JL, Baker JM, Beale MH (2007) Recent applications of NMR spectroscopy in plant metabolomics. FEBS J 274:1126–1131. doi:10.1111/j.1742-4658.2007.05675.x
Weih M, Bonosi L, Ghelardini L, Rönnberg-Wästljung AC (2011) Optimizing nitrogen economy under drought: increased leaf nitrogen is an acclimation to water stress in willow (Salix spp.). Ann Bot 108:1347–1353. doi:10.1093/aob/mcr227
Widodo PJH, 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
Wingler A, Roitsch T (2008) Metabolic regulation of leaf senescence: interactions of sugar signalling with biotic and abiotic stress responses. Plant Biol 10:50–62. doi:10.1111/j.1438-8677.2008.00086.x
Wong CE, Li Y, Labbe A, Guevara D, Nuin P, Whitty B, Diaz C, Golding GB, Gray GR, Weretilnyk EA, Griffith M, Moffatt BA (2006) Transcriptional profiling implicates novel interactions between abiotic stress and hormonal responses in Thellungiella, a close relative of Arabidopsis. Plant Physiol 140:1437–1450. doi:10.1104/pp. 105.070508
Wulff-Zottele C, Gatzke N, Kopka J, Orellana A, Hoefgen R, Fisahn J, Hesse H (2010) Photosynthesis and metabolism interact during acclimation of Arabidopsis thaliana to high irradiance and sulphur depletion. Plant Cell Environ 33:1974–1988. doi:10.1111/j.1365-3040.2010.02199.x
Yancey PH (2005) Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses. J Exp Biol 208:2819–2830. doi:10.1242/jeb.01730
Zhang JT, Zhang Y, Du YY, Chen SY, Tang HR (2011) Dynamic metabonomic responses of tobacco (Nicotiana tabacum) plants to salt stress. J Proteome Res 10:1904–1914. doi:10.1021/pr101140n
Zhang W, Han Z, Guo Q, Liu Y, Zheng Y, Wu F, Jinet W (2014) Identification of maize long non-coding RNAs responsive to drought stress. PLoS ONE 9:e98958. doi:10.1371/journal.pone.0098958
Zhao J, Williams CC, Last RL (1998) Induction of Arabidopsis tryptophan pathway enzymes and camalexin by amino acid starvation, oxidative stress, and an abiotic elicitor. Plant Cell 10:359–370. doi:10.1105/tpc.10.3.359
Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273. doi:10.1146/annurev.arplant.53.091401.143329
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This study was financially supported by National Natural Science Foundation of China (No. 31300331) and Fundamental Research Funds for the Central University (N120405008), P. R. of China.
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Sun, C., Gao, X., Fu, J. et al. Metabolic response of maize (Zea mays L.) plants to combined drought and salt stress. Plant Soil 388, 99–117 (2015). https://doi.org/10.1007/s11104-014-2309-0
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DOI: https://doi.org/10.1007/s11104-014-2309-0