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A systematic proteomic analysis of NaCl-stressed germinating maize seeds

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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.

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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

  1. 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

    Article  Google Scholar 

  2. 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

    Article  CAS  Google Scholar 

  3. 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

    Article  CAS  PubMed  Google Scholar 

  4. Alsheikh M, Heyen B, Randall S (2003) Ion binding properties of the dehydrin ERD14 are dependent upon phosphorylation. J Biol Chem 278:40882–40889

    Article  CAS  PubMed  Google Scholar 

  5. Bewley J, Black M (1994) Seeds: physiology of development and germination. Springer, New York

    Book  Google Scholar 

  6. 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

    Article  PubMed  Google Scholar 

  7. Boyer J (1982) Plant productivity and environment. Science 218:443–448

    Article  CAS  PubMed  Google Scholar 

  8. 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

    Article  CAS  PubMed  Google Scholar 

  9. 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

    Article  CAS  PubMed  Google Scholar 

  10. 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

    Article  CAS  PubMed  Google Scholar 

  11. 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

    Article  CAS  Google Scholar 

  12. 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

    Article  CAS  PubMed  Google Scholar 

  13. 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  14. Finch-Savage W, Leubner-Metzger G (2006) Seed dormancy and the control of germination. New Phytol 171:501–523

    Article  CAS  PubMed  Google Scholar 

  15. 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  16. 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

    Google Scholar 

  17. 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  18. 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

    Article  CAS  PubMed  Google Scholar 

  19. 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

    Article  CAS  PubMed  Google Scholar 

  20. 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  21. 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

    Article  Google Scholar 

  22. 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  23. 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  24. 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

    Article  CAS  PubMed  Google Scholar 

  25. 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

    Article  CAS  PubMed  Google Scholar 

  26. Huang H, Moller IM, Song SQ (2012) Proteomics of desiccation tolerance during development and germination of maize embryos. J Proteomics 75:1247–1262

    Article  CAS  PubMed  Google Scholar 

  27. Hynek R, Svensson B, Jensen O, Barkholt V, Finnie C (2009) The plasma membrane proteome of germinating barley embryos. Proteomics 9:3787–3794

    Article  CAS  PubMed  Google Scholar 

  28. 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

    Article  CAS  PubMed  Google Scholar 

  29. 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  30. 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

    Article  CAS  PubMed  Google Scholar 

  31. 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  32. 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

    Article  CAS  PubMed  Google Scholar 

  33. 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

    Article  CAS  PubMed  Google Scholar 

  34. 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

    Article  CAS  PubMed  Google Scholar 

  35. Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444:139–158

    Article  CAS  PubMed  Google Scholar 

  36. Mortenson E, Dreyfuss G (1989) Rnp in maize protein. Nature 337:312

    Article  CAS  PubMed  Google Scholar 

  37. Jensen ON (2004) Modification-specific proteomics: characterization of post-translational modifications by mass spectrometry. Curr Opin Chem Biol 8(1):33–41

    Article  PubMed  Google Scholar 

  38. 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  39. 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

    Article  CAS  Google Scholar 

  40. Pawlowski TA (2007) Proteomics of European beech (Fagus sylvatica L.) seed dormancy breaking: influence of abscisic and gibberellic acids. Proteomics 7:2246–2257

    Article  CAS  PubMed  Google Scholar 

  41. 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

    Article  PubMed Central  PubMed  Google Scholar 

  42. 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

    Article  CAS  PubMed  Google Scholar 

  43. 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  44. 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  45. 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

    Article  CAS  PubMed  Google Scholar 

  46. 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

    Article  CAS  PubMed  Google Scholar 

  47. 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

    Article  CAS  PubMed  Google Scholar 

  48. Stone S, Arnoldo M, Goring D (1999) A breakdown of Brassica self-incompatibility in ARC1 antisense transgenic plants. Science 286:1729

    Article  CAS  PubMed  Google Scholar 

  49. 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

    Article  PubMed Central  PubMed  Google Scholar 

  50. Tan LY, Chen SX, Wang T, Dai SJ (2013) Proteomic insights into seed germination in response to environmental factors. Proteomics 13:1850–1870

    Article  CAS  PubMed  Google Scholar 

  51. Thiel T (1988) Phosphate transport and arsenate resistance in the cyanobacterium Anabaena variabilis. J Bacteriol 170:1143–1147

    PubMed Central  CAS  PubMed  Google Scholar 

  52. 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

    Article  CAS  PubMed  Google Scholar 

  53. 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

    Article  CAS  PubMed  Google Scholar 

  54. 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

    Article  CAS  Google Scholar 

  55. 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

    Article  CAS  PubMed  Google Scholar 

  56. 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

    Article  CAS  PubMed  Google Scholar 

  57. 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  58. 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

    Article  PubMed  Google Scholar 

  59. Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6:66–71

    Article  CAS  PubMed  Google Scholar 

  60. 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  61. 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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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).

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Correspondence to Xiao-Hui Li or Bai-Chen Wang.

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Ling-Bo Meng and Yi-Bo Chen have contributed equally to this work.

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Fig. S1 The MASCOT search results for HSP68 (spot 10) (DOC 296 kb)

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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

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