Abstract
Salt (NaCl) is a common physiological stressor of plants. To better understand how germinating seeds respond to salt stress, we examined the changes that occurred in the proteome of maize seeds during NaCl-treated germination. Phenotypically, salt concentrations less than 0.2 M appear to delay germination, while higher concentrations disrupt development completely, leading to seed death. The identities of 96 proteins with expression levels altered by NaCl-incubation were established using 2-DE-MALDI-TOF–MS and 2-DE-MALDI-TOF–MS/MS. Of these 96 proteins, 79 were altered greater than twofold when incubated with a 0.2 M salt solution, while 51 were altered when incubated with a 0.1 M salt solution. According to their functional annotations in the Swiss-Prot protein-sequence databases, these proteins are mainly involved in seed storage, energy metabolism, stress response, and protein metabolism. Notably, the expression of proteins that respond to abscisic acid signals increased in response to salt stress. The results of this study provide important clues as to how NaCl stresses the physiology of germinating maize seeds.
Similar content being viewed by others
Abbreviations
- ABA:
-
Abscisic acid
- CHAPS:
-
3-(3-Chloamidopropyl)
- DTT:
-
Dithiothreitol
- IEF:
-
Isoelectric focusing
- 2-DE:
-
Two-dimensional polyacrylamide gel electrophoresis
- MALDI-TOF–MS:
-
Matrix assisted laser desorption ionization-time of flight-mass spectrometry
- MS/MS:
-
Tandem mass spectrometry
References
Aalenf R, Opsahl-Ferstad H, Linnestad C, Olsen O (1994) Transcripts encoding an oleosin and a dormancy-related protein are present in both the aleurone layer and the embryo of developing barley (Hordeum vulgare L.) seeds. Plant J 5:385–396
Abdul Jaleel C, Gopi R, Sankar B, Manivannan P, Kishorekumar A, Sridharan R, Panneerselvam R (2007) Studies on germination, seedling vigour, lipid peroxidation and proline metabolism in Catharanthus roseus seedlings under salt stress. S Afr J Bot 73:190–195
Ali-Rachedi S, Bouinot D, Wagner M, Bonnet M, Sotta B, Grappin P, Jullien M (2004) Changes in endogenous abscisic acid levels during dormancy release and maintenance of mature seeds: studies with the Cape Verde islands ecotype, the dormant model of Arabidopsis thaliana. Planta 219:479–488
Alsheikh M, Heyen B, Randall S (2003) Ion binding properties of the dehydrin ERD14 are dependent upon phosphorylation. J Biol Chem 278:40882–40889
Bewley J, Black M (1994) Seeds: physiology of development and germination. Springer, New York
Bonsager B, Finnie C, Roepstorff P, Svensson B (2007) Spatio-temporal changes in germination and radical elongation of barley seeds tracked by proteome analysis of dissected embryo, aleurone layer, and endosperm tissues. Proteomics 7:4528–4540
Boyer J (1982) Plant productivity and environment. Science 218:443–448
Cadman C, Toorop P, Hilhorst H, Finch-Savage W (2006) Gene expression profiles of Arabidopsis Cvi seeds during dormancy cycling indicate a common underlying dormancy control mechanism. Plant J 46:805
Carles C, Bies-Etheve N, Aspart L, Leon-Kloosterziel K, Koornneef M, Echeverria M, Delseny M (2002) Regulation of Arabidopsis thaliana Em genes: role of ABI5. Plant J 30:373
Chen Q, Yang L, Ahmad P, Wan X, Hu X (2011) Proteomic profiling and redox status alteration of recalcitrant tea (Camellia sinensis) seed in response to desiccation. Planta 233:583–592
Cheng L, Gao X, Li S, Shi M, Javeed H, Jing X, Yang G, He G (2010) Proteomic analysis of soybean [Glycine max (L.) Meer.] seeds during imbibition at chilling temperature. Mol Breed 26:1–17
Chivasa S, Simon WJ, Yu XL, Yalpani N, Slabas AR (2005) Pathogen elicitor-induced changes in the maize extracellular matrix proteome. Proteomics 5:4894–4904
Cramer G, Bowman D (1991) Short-term leaf elongation kinetics of maize in response to salinity are independent of the root. Plant Physiol 95:965–967
Finch-Savage W, Leubner-Metzger G (2006) Seed dormancy and the control of germination. New Phytol 171:501–523
Gallardo K, Job C, Groot S, Puype M, Demol H, Vandekerckhove J, Job D (2001) Proteomic analysis of Arabidopsis seed germination and priming. Plant Physiol 126:835–848
Gamble SC, Dunn MJ, Wheeler CH, Joiner MC, Adu-Poku A, Arrand JE (2000) Expression of proteins coincident with inducible radioprotection in human lung epithelial cells. Cancer Res 60: 2146-2151
Goday A, Jensen A, Culianez-Macia F, Alba M, Figueras M, Serratosa J, Torrent M, Pages M (1994) The maize abscisic acid-responsive protein Rab17 is located in the nucleus and interacts with nuclear localization signals. Plant Cell 6:351–360
Goldmark P, Curry J, Morris C, Walker-Simmons M (1992) Cloning and expression of an embryo-specific mRNA up-regulated in hydrated dormant seeds. Plant Mol Biol 19:433–441
Gomez J, Sanchez-Martinez D, Stiefel V, Rigau J, Puigdomenech P, Pages M (1988) A gene induced by the plant hormone abscisic acid in response to water stress encodes a glycine-rich protein. Nature 334:262–264
Gruis D, Schulze J, Jung R (2004) Storage protein accumulation in the absence of the vacuolar processing enzyme family of cysteine proteases. Plant Cell 16:270
Haslek SC, Stacy R, Nygaard V, Culiá ez-Macià F, Aalen R (1998) The expression of a peroxiredoxin antioxidant gene, AtPer1, in Arabidopsis thaliana is seed-specific and related to dormancy. Plant Mol Biol 36:833–845
Haslekas C, Viken M, Grini P, Nygaard V, Nordgard S, Meza T, Aalen R (2003) Seed 1-cysteine peroxiredoxin antioxidants are not involved in dormancy, but contribute to inhibition of germination during stress 1. Plant Physiol 133:1148–1157
Heyen B, Alsheikh M, Smith E, Torvik C, Seals D, Randall S (2002) The calcium-binding activity of a vacuole-associated, dehydrin-like protein is regulated by phosphorylation. Plant Physiol 130:675–687
Hochholdinger F, Guo L, Schnable P (2004) Lateral roots affect the proteome of the primary root of maize (Zea mays L.). Plant Mol Biol 56:397–412
Hochholdinger F, Woll K, Guo L, Schnable PS (2005) The accumulation of abundant soluble proteins changes early in the development of the primary roots of maize (Zea mays L.). Proteomics 5:4885–4893
Huang H, Moller IM, Song SQ (2012) Proteomics of desiccation tolerance during development and germination of maize embryos. J Proteomics 75:1247–1262
Hynek R, Svensson B, Jensen O, Barkholt V, Finnie C (2009) The plasma membrane proteome of germinating barley embryos. Proteomics 9:3787–3794
Jensen A, Goday A, Figueras M, Jessop A, Pages M (1998) Phosphorylation mediates the nuclear targeting of the maize Rab17 protein. Plant J 13:691
Kawasaki S, Borchert C, Deyholos M, Wang H, Brazille S, Kawai K, Galbraith D, Bohnert H (2001) Gene expression profiles during the initial phase of salt stress in rice. Plant Cell 13:889–906
Kim M, Cho H, Kim D, Lee J, Pai H (2003) CHRK1, a chitinase-related receptor-like kinase, interacts with NtPUB4, an armadillo repeat protein, in tobacco. Biochim Biophys Acta 1651:50–59
Lee S, Chen T (1993) Molecular cloning of abscisic acid-responsive mRNAs expressed during the induction of freezing tolerance in bromegrass (Bromus inermis Leyss) suspension culture. Plant Physiol 101:1089–1096
Lewis M, Miki K, Ueda T (2000) FePer 1, a gene encoding an evolutionarily conserved 1-Cys peroxiredoxin in buckwheat (Fagopyrum esculentum Moench), is expressed in a seed-specific manner and induced during seed germination. Gene 246:81–91
Li K, Xu C, Zhang K, Yang A, Zhang J (2007) Proteomic analysis of roots growth and metabolic changes under phosphorus deficit in maize (Zea mays L.) plants. Proteomics 7:1501–1512
Liu Y, Lamkemeyer T, Jakob A, Mi GH, Zhang FS, Nordheim A, Hochholdinger F (2006) Comparative proteome analyses of maize (Zea mays L.) primary roots prior to lateral root initiation reveal differential protein expression in the lateral root initiation mutant rum1. Proteomics 6:4300–4308
Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444:139–158
Mortenson E, Dreyfuss G (1989) Rnp in maize protein. Nature 337:312
Jensen ON (2004) Modification-specific proteomics: characterization of post-translational modifications by mass spectrometry. Curr Opin Chem Biol 8(1):33–41
Neumann P, Van Volkenburgh E, Cleland R (1988) Salinity stress inhibits bean leaf expansion by reducing turgor, not wall extensibility 1. Plant Physiol 88:233–237
Ozturk Z, Talamé V, Deyholos M, Michalowski C, Galbraith D, Gozukirmizi N, Tuberosa R, Bohnert H (2002) Monitoring large-scale changes in transcript abundance in drought-and salt-stressed barley. Plant Mol Biol 48:551–573
Pawlowski TA (2007) Proteomics of European beech (Fagus sylvatica L.) seed dormancy breaking: influence of abscisic and gibberellic acids. Proteomics 7:2246–2257
Pawlowski TA (2009) Proteome analysis of Norway maple (Acer platanoides L.) seeds dormancy breaking and germination: influence of abscisic and gibberellic acids. BMC Plant Biol 9:48
Pla M, Vilardell J, Guiltinan M, Marcotte W, Niogret M, Quatrano R, Pagès M (1993) The cis-regulatory element CCACGTGG is involved in ABA and water-stress responses of the maize gene rab28. Plant Mol Biol 21:259–266
Rajjou L, Gallardo K, Debeaujon I, Vandekerckhove J, Job C, Job D (2004) The effect of α-amanitin on the Arabidopsis seed proteome highlights the distinct roles of stored and neosynthesized mRNAs during germination 1. Plant Physiol 134:1598–1613
Rajjou L, Belghazi M, Huguet R, Robin C, Moreau A, Job C, Job D (2006) Proteomic investigation of the effect of salicylic acid on Arabidopsis seed germination and establishment of early defense mechanisms. Plant Physiol 141:910–923
Sauer M, Jakob A, Nordheim A, Hochholdinger F (2006) Proteomic analysis of shoot-borne root initiation in maize (Zea mays L.). Proteomics 6:2530–2541
Seki M, Narusaka M, Ishida J, Nanjo T, Fujita M, Oono Y, Kamiya A, Nakajima M, Enju A, Sakurai T (2002) Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J 31:279
Stacy R, Munthe E, Steinum T, Sharma B, Aalen R (1996) A peroxiredoxin antioxidant is encoded by a dormancy-related gene, Per1, expressed during late development in the aleurone and embryo of barley grains. Plant Mol Biol 31:1205–1216
Stone S, Arnoldo M, Goring D (1999) A breakdown of Brassica self-incompatibility in ARC1 antisense transgenic plants. Science 286:1729
Stone S, Anderson E, Mullen R, Goring D (2003) ARC1 is an E3 ubiquitin ligase and promotes the ubiquitination of proteins during the rejection of self-incompatible Brassica pollen. Plant Cell 15:885
Tan LY, Chen SX, Wang T, Dai SJ (2013) Proteomic insights into seed germination in response to environmental factors. Proteomics 13:1850–1870
Thiel T (1988) Phosphate transport and arsenate resistance in the cyanobacterium Anabaena variabilis. J Bacteriol 170:1143–1147
Tomlinson D, Stevens E, Diemel L (1994) Aldose reductase inhibitors and their potential for the treatment of diabetic complications. Trends Pharmacol Sci 15:293–297
Wang B-C, Wang H-X, Feng J-X, Meng D-Z, Qu L-J, Zhu Y-X (2006) Post-translational modifications, but not transcriptional regulation, of major chloroplast RNA-binding proteins are related to Arabidopsis seedling development. Proteomics 6:2555–2563
Xu Y, Dixon S, Brereton R, Soini H, Novotny M, Trebesius K, Bergmaier I, Oberzaucher E, Grammer K, Penn D (2007) Comparison of human axillary odour profiles obtained by gas chromatography/mass spectrometry and skin microbial profiles obtained by denaturing gradient gel electrophoresis using multivariate pattern recognition. Metabolomics 3:427–437
Yang PF, Li XJ, Wang XQ, Chen H, Chen F, Shen SH (2007) Proteomic analysis of rice (Oryza sativa) seeds during germination. Proteomics 7:3358–3368
Yang F, Svensson B, Finnie C (2011) Response of germinating barley seeds to Fusarium graminearum: the first molecular insight into Fusarium seedling blight. Plant Physiol Biochem 49:1362–1368
Zhang HX, Lian CL, Shen ZG (2009) Proteomic identification of small, copper-responsive proteins in germinating embryos of Oryza sativa. Ann Bot 103:923–930
Zhang Heng, Han Bing, Wang Tai, Chen Sixue, Li Haiying, Zhang Yuhong, Dai Shaojun (2012) Mechanisms of plant salt response: insights from proteomics. J Proteome Res 11:49–67
Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6:66–71
Zhu J, Chen S, Alvarez S, Asirvatham V, Schachtman D, Wu Y, Sharp R (2006) Cell wall proteome in the maize primary root elongation zone. I. extraction and identification of water-soluble and lightly ionically bound proteins 1. Plant Physiol 140:311–325
Zimmermann G, Baumlein H, Mock H, Himmelbach A, Schweizer P (2006) The multigene family encoding germin-like proteins of barley. Regulation and function in basal host resistance. Plant Physiol 142:181
Acknowledgments
This research was supported by grants from the National High-Tech Research and Development Program of China (Grant No. 2012AA10A300) and the Chinese Special Fund for Agro-scientific Research in the Public Interest (20093001-06-5).
Author information
Authors and Affiliations
Corresponding authors
Additional information
Ling-Bo Meng and Yi-Bo Chen have contributed equally to this work.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Meng, LB., Chen, YB., Lu, TC. et al. A systematic proteomic analysis of NaCl-stressed germinating maize seeds. Mol Biol Rep 41, 3431–3443 (2014). https://doi.org/10.1007/s11033-014-3205-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11033-014-3205-7