Abstract
Barley (Hordeum vulgare L.) is well known for its relatively high salt tolerance among cereal crops. However, the genetic variation of cultivated barley becomes narrower due to continuous artificial selection and breeding processes. Compared with cultivated barley, wild barley contains wider genetic variation and abundant sources for abiotic stress tolerance, considering as an elite resource for mechanism study on salt tolerance. In this study, Tibetan wild barley accession XZ113 identified with high salt tolerance, was used to investigate ionic responses and to identify proteins involved in salt tolerance in roots and shoots at early stage of salt stress, during 48 h. Exposed to salinity, shoot growth is more sensitive than root growth. Conversely, K/Na ratio in the shoots was larger than that in the roots, and both were above 1.0. Steady-state K+ flux experiment showed XZ113 had a strong K+-retaining ability under salt stress, maybe contributing to its good performance of the absolute growth rate. Proteomic results suggested that monodehydroascorbate reductase and peroxidases related to reactive oxygen species scavenging in the roots and phosphoglycerate kinase, triosephosphate isomerase and sedoheptulose-1,7-bisphosphatase associated with photosynthesis and metabolisms in the shoots, played important roles in salt tolerance at early stage of salinity in wild barley.
Similar content being viewed by others
Abbreviations
- ATP:
-
Adenosine triphosphate
- BPB:
-
Bromophenol blue
- DTT:
-
Dithiothreitol
- DW:
-
Dried weight
- FW:
-
Fresh weight
- GR:
-
Growth rate
- ICP–OES:
-
Inductively coupled plasma–optical emission spectrometer
- IEF:
-
Isoelectric focusing electrophoresis
- IPG:
-
Immobilized pH gradient
- MALDI-TOF/TOF MS:
-
Matrix-assisted laser desorption/ionization time of flight mass
- MIFE:
-
Microelectrode ion flux estimation
- PM:
-
Plasma membrane
- PIPs:
-
Plasma membrane intrinsic proteins
- ROS:
-
Reactive oxygen species
- RWC:
-
Relative water content
- SDS-PAGE:
-
Sodium dodecyl sulfate polyacrylamide gel electrophoresis
- SBPase:
-
Sedoheptulose-1,7-bisphosphatase
- 2-DE:
-
Two-dimensional gel electrophoresis
- TCA:
-
Tricarboxylic acid cycle
- VDAC:
-
Voltage-dependent anion channel
References
Blumwald E (2000) Sodium transport and salt tolerance in plants. Curr Opin Cell Biol 12(4):431–434
Chen ZH, Newman I, Zhou MX, Mendham N, Zhang GP, Shabala S (2005) Screening plants for salt tolerance by measuring K+ flux: a case study for barley. Plant Cell Environ 28(10):1230–1246
Chen ZH, Pottosin II, Cuin TA, Fuglsang AT, Tester M, Jha D, Zepeda-Jazo I, Zhou MX, Palmgren MG, Newman IA, Shabala S (2007) Root plasma membrane transporters controlling K+/Na+ homeostasis in salt-stressed barley. Plant Physiol 145(4):1714–1725
Cheng YW, Qi YC, Zhu Q, Chen X, Wang N, Zhao X, Chen HY, Cui XJ, Xu LL, Zhang W (2009) New changes in the plasma-membrane-associated proteome of rice roots under salt stress. Proteomics 9(11):3100–3114
Dai F, Nevo E, Wu DZ, Comadran J, Zhou MX, Qiu L, Chen ZH, Beiles A, Chen GX, Zhang GP (2012) Tibet is one of the centers of domestication of cultivated barley. Proc Natl Acad Sci USA 109:16969–16973
Deinlein U, Stephan AB, Horie T, Luo W, Xu GH, Schroeder JI (2014) Plant salt-tolerance mechanisms. Trends Plant Sci 19(6):371–379
Ellis RP, Forster BP, Robinson D, Handley LL, Gordon DC, Russell JR, Powell W (2000) Wild barley: a source of genes for crop improvement in the 21st century? J Exp Bot 51(342):9–17
Ellouzi H, Ben Hamed K, Hernandez I, Cela J, Muller M, Magne C, Abdelly C, Munne-Bosch S (2014) A comparative study of the early osmotic, ionic, redox and hormonal signaling response in leaves and roots of two halophytes and a glycophyte to salinity. Planta 240(6):1299–1317
Geiger TR, Keith CS, Muszynski MG, Newton KJ (1999) Sequences of three maize cDNAs encoding mitochondrial voltage-dependent anion channel (VDAC) proteins (accession nos. AF178950, AF178951, and AF178952) (PGR 99-156). Plant Physiol 121(2):686
Glenn EP, Brown JJ, Blumwald E (1999) Salt tolerance and crop potential of halophytes. Crit Rev Plant Sci 18(2):27–255
Gorham J, Wyn Jones RG, Bristol A (1990) Partial characterization of the trait for enhanced K+–Na+ discrimination in the D genome of wheat. Planta 180:590–597
Guo L, Wang ZY, Cui WE, Chen J, Liu MH, Chen ZL, Qu LJ, Gu HY (2006) Expression and functional analysis of the rice plasma-membrane intrinsic protein gene family. Cell Res 16(3):277–286
Han Y, Yin SY, Huang L (2015) Towards plant salinity tolerance-implications from ion transporters and biochemical regulation. Plant Growth Regul 76(1):13–23
Horie T, Karahara I, Katsuhara M (2012) Salinity tolerance mechanisms in glycophytes: an overview with the central focus on rice plants. Rice 5:11
Kohzuma K, Dal Bosco C, Meurer J, Kramer DM (2013) Light- and metabolism-related regulation of the chloroplast ATP synthase has distinct mechanisms and functions. J Biol Chem 288(18):13156–13163
Kosová K, Vítámvás P, Prášil IT, Renaut J (2011) Plant proteome changes under abiotic stress—contribution of proteomics studies to understanding plant stress response. J Proteomics 74:1301–1322
Kosová K, Vítámvás P, Urban MO, Prášil IT (2013a) Plant proteome responses to salinity stress—comparison of glycophytes and halophytes. Funct Plant Biol 40:775–786
Kosová K, Prášil IT, Vítámvás P (2013b) Protein contribution to plant salinity response and tolerance acquisition. Int J Mol Sci 14:6757–6789
Maathuis FJM, Amtmann A (1999) K+ nutrition and Na+ toxicity: the basis of cellular K+/Na+ ratios. Ann Bot 84(2):123–133
Maurel C, Verdoucq L, Luu DT, Santoni V (2008) Plant aquaporins: membrane channels with multiple integrated functions. Annu Rev Plant Biol 59:595–624
Munns R, Tester M (2008) Mechanisms of salinity tolerance. Ann Rev Plant Biol 59:651–681
Munns R, James RA, Xu B, Athman A, Conn SJ, Jordans C, Byrt CS, Hare RA, Tyerman SD, Tester M, Plett D, Gilliham M (2012) Wheat grain yield on saline soils is improved by an ancestral Na+ transporter gene. Nat Biotech 30:360–364
Nevo E (2007) Evolution of wild wheat and barley and crop improvement: studies at the institute of evolution. Isr J Plant Sci 55(3–4):251–262
Qiu L, Wu DZ, Ali S, Cai SG (2011) Evaluation of salinity tolerance and analysis of allelic function of HvHKT1 and HvHKT2 in Tibetan wild barley. Theor Appl Genet 122:695–703
Rasoulnia A, Bihamta MR, Peyghambari SA, Alizadeh H, Rahnama A (2011) Proteomic response of barley leaves to salinity. Mol Biol Rep 38:5055–5063
Rengasamy P (2010) Soil processes affecting crop production in salt-affected soils. Funct Plant Biol 37:613–620
Rosenthal DM, Locke AM, Khozaei M, Raines CA, Long SP, Ort DR (2011) Over-expressing the C3 photosynthesis cycle enzyme sedoheptulose-1-7 bisphosphatase improves photosynthetic carbon gain and yield under fully open air CO2 fumigation (FACE). BMC Plant Biol 11:123
Shabala S (2000) Ionic and osmotic components of salt stress specifically modulate net ion fluxes from bean leaf mesophyll. Plant, Cell Environ 23(8):825–837
Shabala S, Cuin TA (2008) Potassium transport and plant salt tolerance. Physiol Plantarum 133(4):651–669
Shabala S, Shabala S, Cuin TA, Pang JY, Percey W, Chen ZH, Conn S, Eing C, Wegner LH (2010) Xylem ionic relations and salinity tolerance in barley. Plant J 61:839–853
Tester M, Davenport R (2003) Na+ tolerance and Na+ transport in higher plants. Ann Bot 91(5):503–527
Tyerman SD, Niemietz CM, Bramley H (2002) Plant aquaporins: multifunctional water and solute channels with expanding roles. Plant Cell Environ 25:173–194
Wang WS, Zhao XQ, Li M, Huang LY, Xu JL, Zhang F, Cui YR, Fu BY, Li ZK (2016) Complex molecular mechanisms underlying seedling salt tolerance in rice revealed by comparative transcriptome and metabolomic profiling. J Exp Bot 67(1):405–419
Wen GQ, Cai L, Liu Z, Li DK, Luo Q, Li XF, Wan JM, Yang Y (2011) Arabidopsis thaliana VDAC2 involvement in salt stress response pathway. Afr J Biotechnol 10(55):11588–11593
Wu DZ, Qiu L, Xu LL, Ye LZ et al (2011) Genetic variation of HvCBF genes and their association with salinity tolerance in Tibetan annual wild barley. PLoS ONE 6:e22938
Wu DZ, Cai SG, Chen MX, Ye LZ, Chen ZH, Zhang HT, Dai F, Wu FB, Zhang GP (2013a) Tissue metabolic responses to salt stress in wild and cultivated barley. PLoS One 8:55431
Wu DZ, Shen QF, Cai SG, Chen ZH, Dai F, Zhang GP (2013b) Ionomic responses and correlations between elements and metabolites under salt stress in wild and cultivated barley. Plant Cell Physiol 54(12):1976–1988
Wu DZ, Shen QF, Qiu L, Han Y, Ye LZ, Jabben Z, Shu QY, Zhang GP (2014) Identification of proteins associated with ion homeostasis and salt tolerance in barley. Proteomics 14:1381–1392
Zhang B, Li PF, Fan FC (2012a) Ionic relations and proline accumulation in shoots of two Chinese Iris germplasms during NaCl stress and subsequent relief. Plant Growth Regul 68(1):49–56
Zhang H, Han B, Wang T, Chen S, Li HY, Zhang YH, Dai SJ (2012b) Mechanisms of plant salt response: insights from proteomics. J Proteome Res 11:49–67
Zhu JK (2002) Salt and drought stress signal transduction in plants. Ann Rev Plant Biol 53:247–273
Acknowledgments
We are grateful to Prof. Dongfa Sun (Huazhong Agricultral University, China) for providing seeds of Tibetan wild barley accession. This research was supported by Natural Science Foundation of China (31330055, 31301246), China Agriculture Research System (CARS-05) and the Fundamental Research Funds for the Central Universities (2016QNA6013).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Shen, Q., Fu, L., Qiu, L. et al. Time-course of ionic responses and proteomic analysis of a Tibetan wild barley at early stage under salt stress. Plant Growth Regul 81, 11–21 (2017). https://doi.org/10.1007/s10725-016-0180-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10725-016-0180-0