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Label-free quantitative proteomics analysis of dormant terminal buds of poplar

Molecular Biology Reports volume 40, pages 4529–4542 (2013)Cite this article

Abstract

Induction and break of bud dormancy are important features for perennial plants surviving extreme seasonal variations in climate. However, the molecular mechanism of the dormancy regulation, still remain poorly understood. To better understand the molecular basis of poplar bud dormancy, we used a label-free quantitative proteomics method based on nanoscale ultra performance liquid chromatography-ESI-MSE for investigation of differential protein expression during dormancy induction, dormancy, and dormancy break in apical buds of poplar (Populus simonii × P. nigra). Among these identified over 300 proteins during poplar bud dormancy, there are 74 significantly altered proteins, most of which involved in carbohydrate metabolism (22 %), redox regulation (19 %), amino acid transport and metabolism (10 %), and stress response (8 %). Thirty-one of these proteins were up-regulated, five were down-regulated during three phase, and thirty-eight were expressed specifically under different conditions. Pathway analysis suggests that there are still the presence of various physiological activities and a particular influence on photosynthesis and energy metabolism during poplar bud dormancy. Differential expression patterns were identified for key enzymes involved in major metabolic pathways such as glycolysis and the pentose phosphate pathway, thus manifesting the interplay of intricate molecular events in energy generation for new protein synthesis in the dormant buds. Furthermore, there are significant changes present in redox regulation and defense response proteins, for instance in peroxidase and ascorbate peroxidase. Overall, this study provides a better understanding of the possible regulation mechanisms during poplar bud dormancy.

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Abbreviations

EMRT:

Exact mass and retention time

MSE :

Low/high collision energy MS

LC:

Liquid chromatography

nano-UPLC:

Nanoscale ultra performance LC

PLGS:

ProteinLynx Global-Server

UPLC:

Ultra performance LC

TCA:

Trichloroacetic acid

BSA:

Bovine serum albumin

DTT:

Dithiothreitol

OEE1:

Oxygen-evolving enhancer protein 1

OEE2:

Oxygen-evolving enhancer protein 2

AdoMetS:

S-Adenosylmethionine synthetase

AdoMet:

S-Adenosylmethionine

LRR:

Leucine-rich repeat

APX:

Ascorbate peroxidase

MDAR:

Monodehydroascorbate reductase

SOD:

Superoxide dismutase

AKR:

Aldo/keto reductase

PDI:

Protein disulfide isomerase

References

  1. Arora R, Rowland LJ, Tanino K (2003) Induction and release of bud dormancy in woody perennials: a science comes of age. HortScience 38(5):911–921

    Google Scholar 

  2. Lang GA (1987) Dormancy—a New Universal Terminology. HortScience 22(5):817–820

    Google Scholar 

  3. Horvath DP, Anderson JV, Chao WS, Foley ME (2003) Knowing when to grow: signals regulating bud dormancy. Trends Plant Sci 8(11):534–540

    PubMed  CAS  Article  Google Scholar 

  4. Rohde A, Ruttink T, Hostyn V, Sterck L, Van Driessche K, Boerjan W (2007) Gene expression during the induction, maintenance, and release of dormancy in apical buds of poplar. J Exp Bot 58(15–16):4047–4060

    PubMed  CAS  Article  Google Scholar 

  5. Nitsch J (1957) Growth responses of woody plants to photoperiodic stimuli. Proc Am Soc Hort Sci 70:512–525

    Google Scholar 

  6. Sylven N (1940) Long- and short-day types of Swedish forest trees. Svensk Papperstidning 43:317–324

    Google Scholar 

  7. Allona I, Ramos A, Ibáñez C, Contreras A, Casado R, Aragoncillo C (2008) Review. Molecular control of winter dormancy establishment in trees. Span J Agric Res 6:201–210

    Google Scholar 

  8. Wareing P (1956) Photoperiodism in woody plants. Annu Rev Plant Physiol 7(1):191–214

    CAS  Article  Google Scholar 

  9. Howe GT, Hackett WP, Furnier GR, Klevorn RE (1995) Photoperiodic responses of a northern and southern ecotype of black cottonwood. Physiol Planta 93(4):695–708

    CAS  Article  Google Scholar 

  10. Li CY, Puhakainen T, Welling A, Vihera-Aarnio A, Ernstsen A, Junttila O, Heino P, Pavla ET (2002) Cold acclimation in silver birch (Betula pendula). Development of freezing tolerance in different tissues and climatic ecotypes. Physiol Planta 116(4):478–488

    CAS  Article  Google Scholar 

  11. Nooden L, Weber J (1978) Environmental and hormonal control of dormancy in terminal buds of plants. Dormancy and developmental arrest. Academic Press, New York, pp 222–268

    Google Scholar 

  12. Suttle JC (2000) The role of endogenous hormones in potato tuber dormancy. Dormancy in plants. CAB Publishing, New York, pp 211–226

    Google Scholar 

  13. Liu CC, Liu CF, Wang HX, Shen ZY, Yang CP, Wei ZG (2011) Identification and analysis of phosphorylation status of proteins in dormant terminal buds of poplar. BMC Plant Biol 11

  14. Rohde A, Bhalerao RP (2007) Plant dormancy in the perennial context. Trends Plant Sci 12(5):217–223

    PubMed  CAS  Article  Google Scholar 

  15. Mazzitelli L, Hancock RD, Haupt S, Walker PG, Pont SDA, McNicol J, Cardle L, Morris J, Viola R, Brennan R, Hedley PE, Taylor MA (2007) Co-ordinated gene expression during phases of dormancy release in raspberry (Rubus idaeus L.) buds. J Exp Bot 58(5):1035–1045

    PubMed  CAS  Article  Google Scholar 

  16. Mathiason K, He D, Grimplet J, Venkateswari J, Galbraith D, Or E, Fennell A (2009) Transcript profiling in Vitis riparia during chilling requirement fulfillment reveals coordination of gene expression patterns with optimized bud break. Funct Integr Genomic 9(1):81–96

    CAS  Article  Google Scholar 

  17. Jimenez S, Li ZG, Reighard GL, Bielenberg DG (2010) Identification of genes associated with growth cessation and bud dormancy entrance using a dormancy-incapable tree mutant. Bmc Plant Biol 10

  18. Liu CC, Lu TC, Li HH, Wang HX, Liu GF, Ma L, Yang CP, Wang BC (2010) Phosphoproteomic identification and phylogenetic analysis of ribosomal P-proteins in Populus dormant terminal buds. Planta 231(3):571–581

    PubMed  CAS  Article  Google Scholar 

  19. Muthalif MM, Rowland LJ (1994) Identification of dehydrin-like proteins responsive to chilling in floral buds of blueberry (Vaccinium, Section Cyanococcus). Plant Physiol 104(4):1439–1447

    PubMed  CAS  Article  Google Scholar 

  20. Renaut J, Lutts S, Hoffmann L, Hausman JF (2004) Responses of poplar to chilling temperatures: proteomic and physiological aspects. Plant Biol 6(1):81–90

    PubMed  CAS  Article  Google Scholar 

  21. Bassett CL, Wisniewski ME, Artlip TS, Richart G, Norelli JL, Farrell RE (2009) Comparative expression and transcript initiation of three peach dehydrin genes. Planta 230(1):107–118

    PubMed  CAS  Article  Google Scholar 

  22. Palonen P, Buszard D, Donnelly D (2000) Changes in carbohydrates and freezing tolerance during cold acclimation of red raspberry cultivars grown in vitro and in vivo. Physiol Planta 110(3):393–401

    CAS  Article  Google Scholar 

  23. Rinne PLH, van der Schoot C (1998) Symplasmic fields in the tunica of the shoot apical meristem coordinate morphogenetic events. Development 125(8):1477–1485

    PubMed  CAS  Google Scholar 

  24. Rinne PLH, Kaikuranta PM, van der Schoot C (2001) The shoot apical meristem restores its symplasmic organization during chilling-induced release from dormancy. Plant J 26(3):249–264

    PubMed  CAS  Article  Google Scholar 

  25. Nir G, Shulman Y, Fanberstein L, Lavee S (1986) Changes in the activity of catalase (EC 1.11. 1.6) in relation to the dormancy of grapevine (Vitis vinifera L.) buds. Plant Physiol 81(4):1140

    PubMed  CAS  Article  Google Scholar 

  26. Or E, Vilozny I, Fennell A, Eyal Y, Ogrodovitch A (2002) Dormancy in grape buds: isolation and characterization of catalase cDNA and analysis of its expression following chemical induction of bud dormancy release. Plant Sci 162(1):121–130

    CAS  Article  Google Scholar 

  27. Wang SY, Jiao HJ, Faust M (1991) Changes in ascorbate, glutathione, and related enzyme-activities during thidiazuron-induced bud break of apple. Physiol Planta 82(2):231–236

    CAS  Article  Google Scholar 

  28. Halaly T, Pang XQ, Batikoff T, Crane O, Keren A, Venkateswari J, Ogrodovitch A, Sadka A, Lavee S, Or E (2008) Similar mechanisms might be triggered by alternative external stimuli that induce dormancy release in grape buds. Planta 228(1):79–88

    PubMed  CAS  Article  Google Scholar 

  29. Shen Z, Li P, Ni RJ, Ritchie M, Yang CP, Liu GF, Ma W, Liu GJ, Ma L, Li SJ, Wei ZG, Wang HX, Wang BC (2009) Label-free quantitative proteomics analysis of etiolated maize seedling leaves during greening. Mol Cell Proteomics 8(11):2443–2460

    PubMed  CAS  Article  Google Scholar 

  30. Silva JC, Denny R, Dorschel C, Gorenstein MV, Li GZ, Richardson K, Wall D, Geromanos SJ (2006) Simultaneous qualitative and quantitative analysis of the Escherichia coli proteome—a sweet tale. Mol Cell Proteomics 5(4):589–607

    PubMed  CAS  Google Scholar 

  31. Silva JC, Gorenstein MV, Li GZ, Vissers JPC, Geromanos SJ (2006) Absolute quantification of proteins by LCMSE—a virtue of parallel MS acquisition. Mol Cell Proteomics 5(1):144–156

    PubMed  CAS  Google Scholar 

  32. Zhou YL, Dong SL, Nie SQ (1986) Heilongjiang sylva. Heilongjiang science and technology press, Harbin, p118

  33. Yang CP, Liu GF, Liang HW, Zhang H (2001) Study on the transformation of Populus simonii × P. nigra with salt resistance gene Bet-A. Sci Silvae Sinicae 37:34–38

    Google Scholar 

  34. Jonsson TH (2006) Terminal bud failure of black cottonwood (Populus trichocarpa) exposed to salt-laden winter storms. Tree Physiol 26(7):905–914

    PubMed  Article  Google Scholar 

  35. Way DA (2011) Tree phenology responses to warming: spring forward, fall back? Tree Physiol 31(5):469–471

    PubMed  Article  Google Scholar 

  36. Washburn MP, Wolters D, Yates JR (2001) Large-scale analysis of the yeast proteome by multidimensional protein identification technology. Nat Biotechnol 19(3):242–247

    PubMed  CAS  Article  Google Scholar 

  37. Meng YY, Liu F, Pang CY, Fan SL, Song MZ, Wang D, Li WH, Yu SX (2011) Label-free quantitative proteomics analysis of cotton leaf response to nitric oxide. J Proteome Res 10(12):5416–5432

    PubMed  CAS  Article  Google Scholar 

  38. Silva JC, Denny R, Dorschel CA, Gorenstein M, Kass IJ, Li GZ, McKenna T, Nold MJ, Richardson K, Young P, Geromanos S (2005) Quantitative proteomic analysis by accurate mass retention time pairs. Anal Chem 77(7):2187–2200

    PubMed  CAS  Article  Google Scholar 

  39. Hughes MA, Silva JC, Geromanos SJ, Townsend CA (2006) Quantitative proteomic analysis of drug-induced changes in mycobacteria. J Proteome Res 5(1):54–63

    PubMed  CAS  Article  Google Scholar 

  40. Li GZ, Vissers JPC, Silva JC, Golick D, Gorenstein MV, Geromanos SJ (2009) Database searching and accounting of multiplexed precursor and product ion spectra from the data independent analysis of simple and complex peptide mixtures. Proteomics 9(6):1696–1719

    PubMed  CAS  Article  Google Scholar 

  41. Vissers JPC, Langridge JI, Aerts JMFG (2007) Analysis and quantification of diagnostic serum markers and protein signatures for Gaucher disease. Mol Cell Proteomics 6(5):755–766

    PubMed  CAS  Article  Google Scholar 

  42. Kopp RF, Abrahamson LP, White EH, Volk TA, Nowak CA, Fillhart RC (2001) Willow biomass production during ten successive annual harvests. Biomass Bioenerg 20(1):1–7

    CAS  Article  Google Scholar 

  43. Oja V, Bichele I, Huve K, Rasulov B, Laisk A (2004) Reductive titration of photosystem I and differential extinction coefficient of P700(+) at 810–950 nm in leaves. Biochim Biophys Acta 1658(3):225–234

    PubMed  CAS  Article  Google Scholar 

  44. Whitelegge JP, Koo D, Diner BA, Domian I, Erickson JM (1995) Assembly of the photosystem II oxygen-evolving complex is inhibited in psbA site-directed mutants of Chlamydomonas reinhardtii—Aspartate-170 of the D1 polypeptide. J Biol Chem 270(1):225–235

    PubMed  CAS  Article  Google Scholar 

  45. Mayfield SP, Bennoun P, Rochaix JD (1987) Expression of the nuclear encoded Oee1 protein is required for oxygen evolution and stability of photosystem II particles in Chlamydomonas reinhardtii. EMBO J 6(2):313–318

    PubMed  CAS  Google Scholar 

  46. Miyao M, Murata N (1989) The mode of binding of 3 extrinsic proteins of 33 kDa, 23 kDa and 18 kDa in the photosystem II complex of spinach. Biochim Biophys Acta 977(3):315–321

    CAS  Article  Google Scholar 

  47. Ghanotakis DF, Yocum CF (1990) Photosystem II and the oxygen-evolving complex. Annu Rev Plant Phys 41:255–276

    CAS  Article  Google Scholar 

  48. Szegő D, Kósa E, Horváth E (2007) Role of S-methylmethionine in the plant metabolism. Acta Agron Hung 55(4):491–508

    Article  Google Scholar 

  49. Ho P, Kong K, Chan Y, Tsang J, Wong J (2007) An unusual S-adenosylmethionine synthetase gene from dinoflagellate is methylated. BMC Mol Biol 8(1):87

    PubMed  Article  Google Scholar 

  50. Newman EB, Budman LI, Chan EC, Greene RC, Lin RT, Woldringh CL, D’Ari R (1998) Lack of S-adenosylmethionine results in a cell division defect in Escherichia coli. J Bacteriol 180(14):3614–3619

    PubMed  CAS  Google Scholar 

  51. Ben-Haj-Salah H, Tardieu F (1995) Temperature affects expansion rate of maize leaves without change in spatial distribution of cell length (analysis of the coordination between cell division and cell expansion). Plant Physiol 109(3):861–870

    PubMed  CAS  Google Scholar 

  52. Bergervoet JHW, Jing HC, Van Den Hout JWE, Delmondez de Castro R, Kunneman BPAM, Bino RJ, Groot SPC (1999) Expression of beta-tubulin during dormancy induction and release in apical and axillary buds of five woody species. Physiol Planta 106(2):238–245

    CAS  Article  Google Scholar 

  53. Nordin K, Vahala T, Palva ET (1993) Differential expression of two related, low-temperature-induced genes in Arabidopsis thaliana (L.) Heynh. Plant Mol Biol 21(4):641–653

    PubMed  CAS  Article  Google Scholar 

  54. Lin CT, Thomashow MF (1992) A cold-regulated Arabidopsis gene encodes a polypeptide having potent cryoprotective activity. Biochem Bioph Res Co 183(3):1103–1108

    CAS  Article  Google Scholar 

  55. Hon WC, Griffith M, Chong PL, Yang DSC (1994) Extraction and isolation of antifreeze proteins from winter rye (Secale-Cereale L.) leaves. Plant Physiol 104(3):971–980

    PubMed  CAS  Google Scholar 

  56. Grudkowska M, Zagdanska B (2004) Multifunctional role of plant cysteine proteinases. Acta Biochim Pol 51(3):609–624

    PubMed  CAS  Google Scholar 

  57. Meyer K, Keil M, Naldrett MJ (1999) A leucine-rich repeat protein of carrot that exhibits antifreeze activity. FEBS Lett 447(2–3):171–178

    PubMed  CAS  Article  Google Scholar 

  58. Johnson R, Narvaez J, An G, Ryan C (1989) Expression of proteinase inhibitors I and II in transgenic tobacco plants: effects on natural defense against Manduca sexta larvae. Proc Natl Acad Sci USA 86(24):9871

    PubMed  CAS  Article  Google Scholar 

  59. Thomas S, Mooney PFJ, Burrell MM, Fell DA (1997) Metabolic control analysis of glycolysis in tuber tissue of potato (Solanum tuberosum): explanation for the low control coefficient of phosphofructokinase over respiratory flux. Biochem J 322:119–127

    PubMed  CAS  Google Scholar 

  60. Wurtele ES, Nikolau BJ (1986) Enzymes of glucose oxidation in leaf tissues: the distribution of the enzymes of glycolysis and the oxidative pentose phosphate pathway between epidermal and mesophyll tissues of C3-plants and epidermal, mesophyll, and bundle sheath tissues of C4-plants. Plant Physiol 82(2):503

    PubMed  CAS  Article  Google Scholar 

  61. Kato-Noguchi H (2007) Low temperature acclimation to chilling tolerance in rice roots. Plant Growth Regul 51(2):171–175

    CAS  Article  Google Scholar 

  62. De Vries FWTP (1975) The cost of maintenance processes in plant cells. Ann Bot 39(1):77–92

    Google Scholar 

  63. Hachiya T, Terashima I, Noguchi K (2007) Increase in respiratory cost at high growth temperature is attributed to high protein turnover cost in Petunia × hybrida petals. Plant Cell Environ 30(10):1269–1283

    PubMed  CAS  Article  Google Scholar 

  64. Noguchi K, Nakajima N, Terashima I (2001) Acclimation of leaf respiratory properties in Alocasia odora following reciprocal transfers of plants between high- and low-light environments. Plant Cell Environ 24(8):831–839

    CAS  Article  Google Scholar 

  65. Nelson EA, Dickson RE (1981) Accumulation of food reserves in cottonwood stems during dormancy induction. Can J Forest Res 11(1):145–154

    Article  Google Scholar 

  66. Colmer TD, Epstein E, Dvorak J (1995) Differential solute regulation in leaf blades of various ages in salt-sensitive wheat and a salt-tolerant wheat x Lophopyrum elongatum (Host) A. Love amphiploid. Plant Physiol 108(4):1715–1724

    PubMed  CAS  Google Scholar 

  67. Chinnusamy V, Zhu JK, Sunkar R (2010) Gene regulation during cold stress acclimation in plants. Plant Stress Tolerance: Methods and Protocols 639:39–55

    CAS  Article  Google Scholar 

  68. Korkmaz A, Dufault RJ (2001) Developmental consequences of cold temperature stress at transplanting on seedling and field growth and yield. II. Muskmelon. J Am Soc Hortic Sci 126(4):410–413

    Google Scholar 

  69. Dat J, Vandenabeele S, Vranova E, Van Montagu M, Inzé* D, Van Breusegem F (2000) Dual action of the active oxygen species during plant stress responses. Cell Mol Life Sci 57(5):779–795

    PubMed  CAS  Article  Google Scholar 

  70. Bailly C (2004) Active oxygen species and antioxidants in seed biology. Seed Sci Res 14(2):93–108

    CAS  Article  Google Scholar 

  71. Pastori GM, Foyer CH (2002) Common components, networks, and pathways of cross-tolerance to stress. The central role of “redox” and abscisic acid-mediated controls. Plant Physiol 129(2):460–468

    PubMed  CAS  Article  Google Scholar 

  72. Foyer CH, Noctor G (2003) Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiol Planta 119(3):355–364

    CAS  Article  Google Scholar 

  73. Kocsy G, Galiba G, Brunold C (2001) Role of glutathione in adaptation and signalling during chilling and cold acclimation in plants. Physiol Planta 113(2):158–164

    CAS  Article  Google Scholar 

  74. Wang SY, Jiao HJ, Faust M (1991) Changes in ascorbate, glutathione, and related enzyme activities during thidiazuron-induced bud break of apple. Physiol Planta 82(2):231–236

    CAS  Article  Google Scholar 

  75. Wang SY, Faust M (1994) Changes in the antioxidant system associated with budbreak in anna’apple (Malus domestica Borkh.) buds. J Am Soc Hortic Sci 119(4):735–741

    CAS  Google Scholar 

  76. Perez FJ, Lira W (2005) Possible role of catalase in post-dormancy bud break in grapevines. J Plant Physiol 162(3):301–308

    PubMed  CAS  Article  Google Scholar 

  77. Bi YD, Wei ZG, Shen Z, Lu TC, Cheng YX, Wang BC, Yang CP (2011) Comparative temporal analyses of the Pinus sylvestris L. var. mongolica litv. apical bud proteome from dormancy to growth. Mol Biol Rep 38(2):721–729

    PubMed  CAS  Article  Google Scholar 

  78. Bartels D (2001) Targeting detoxification pathways: an efficient approach to obtain plants with multiple stress tolerance? Trends Plant Sci 6(7):284–286

    PubMed  CAS  Article  Google Scholar 

  79. Schultz-Norton JR, McDonald WH, Yates JR, Nardulli AM (2006) Protein disulfide isomerase serves as a molecular chaperone to maintain estrogen receptor α structure and function. Mol Endocrinol 20(9):1982–1995

    PubMed  CAS  Article  Google Scholar 

  80. Wells WW, Xu DP, Yang YF, Rocque PA (1990) Mammalian thioltransferase (Glutaredoxin) and protein disulfide isomerase have dehydroascorbate reductase-activity. J Biol Chem 265(26):15361–15364

    PubMed  CAS  Google Scholar 

  81. Liu JJ, Ekramoddoullah AKM (2006) The family 10 of plant pathogenesis-related proteins: their structure, regulation, and function in response to biotic and abiotic stresses. Physiol Mol Plant Pathol 68(1):3–13

    CAS  Article  Google Scholar 

  82. Hon WC, Griffith M, Mlynarz A, Kwok YC, Yang DSC (1995) Antifreeze proteins in winter rye are similar to pathogenesis-related proteins. Plant Physiol 109(3):879–889

    PubMed  CAS  Article  Google Scholar 

  83. Gaudet DA, Laroche A, Frick M, Davoren J, Puchalski B, Ergon A (2000) Expression of plant defence-related (PR-protein) transcripts during hardening and dehardening of winter wheat. Physiol Mol Plant P 57(1):15–24

    CAS  Article  Google Scholar 

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Acknowledgments

The authors acknowledge grant support from the National Basic Research Priorities Program (Grant No. 2009CB119102).

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Affiliations

  1. State Key Laboratory of Forest Genetics and Tree Breeding, Northeast Forestry University, 26 Hexing Road, Harbin, 150040, China

    De-Li Ning, Chang-Cai Liu, Jin-Wen Liu, Zhuo Shen, Su Chen, Bai-Chen Wang & Chuan-Ping Yang

  2. National Center of Biomedical Analysis, 27 Taiping Road, Beijing, 100850, China

    Feng Liu

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  1. De-Li Ning
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Ning, DL., Liu, CC., Liu, JW. et al. Label-free quantitative proteomics analysis of dormant terminal buds of poplar. Mol Biol Rep 40, 4529–4542 (2013). https://doi.org/10.1007/s11033-013-2548-9

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Keywords

  • Populus
  • Large-scale proteomics
  • NanoUPLC–ESI–MS/MS
  • Dormancy