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Proteomic identification of lipid-bodies-associated proteins in maize seeds

  • Cui Du
  • Aimei Liu
  • Liangjie Niu
  • Di Cao
  • Hui LiuEmail author
  • Xiaolin Wu
  • Wei WangEmail author
Original Article
  • 82 Downloads

Abstract

Seeds store lipids in the form of lipid bodies (LBs) for germination and early seedling growth. LBs can be easily isolated by the established floating-extraction method from oleaginous seeds containing a large quantity of LBs. Compared to oleaginous seeds, maize and other cereal seeds contain a small quantity of LBs, so it is difficult to isolate a sufficient quantity of LBs from their embryos for 2DE-based proteomic analysis. At present, only a limited number of LBs-associated proteins in maize embryos have been identified. We here reported a modified floating-extraction method using polyvinylidene difluoride disc to collect floating LBs from maize embryo extracts. The LBs-associated proteins were resolved with two-dimensional electrophoresis and identified with mass spectrometry. As a result, several well-known LBs proteins were identified in the purified LBs fraction, such as oleosin, caleosin, and steroleosin. We also identified another two LBs proteins, corticosteroid 11-β-dehydrogenase 1 and 11-β-hydroxysteroid dehydrogenase-like 5. In particular, steroleosin, corticosteroid 11-β-dehydrogenase 1, 11-β-hydroxysteroid dehydrogenase-like, and hydroxyproline-rich glycoprotein were found as the most abundant protein components in maize LBs. The data set of maize LBs subproteome would provide insights into functional research of LBs-associated proteins during seed development and germination. Additionally, the protocol developed here is expected to be applicable for isolating LBs in other seeds or tissues containing a low quantity of LBs.

Keywords

Lipid-bodies isolation Maize embryos Proteomic analysis Polyvinylidene difluoride (PVDF) Two-dimensional gel electrophoresis (2DE) 

Notes

Acknowledgements

This work was supported by the Program for Innovative Research Team (in Science and Technology) in University of Henan Province (15IRTSTHN015).

Supplementary material

11738_2019_2854_MOESM1_ESM.docx (15 kb)
Supplementary material 1 (DOCX 15 kb)

References

  1. Baud S, Dichow NR, Kelemen Z, d’Andréa S, To A, Berger N et al (2009) Regulation of HSD1 in seeds of Arabidopsis thaliana. Plant Cell Physiol 50:1463–1478CrossRefPubMedGoogle Scholar
  2. Capuano F, Beaudoin F, Napier JA, Shewry PR (2007) Properties and exploitation of oleosins. Biotechnol Adv 25:203–206CrossRefPubMedGoogle Scholar
  3. Chapman KD, Dyer JM, Mullen RT (2012) Biogenesis and functions of lipid droplets in plants: thematic review series: Lipid droplet synthesis and metabolism: from yeast to man. J Lipid Res 53:215–226CrossRefPubMedPubMedCentralGoogle Scholar
  4. d’Andréa S, Canonge M, Beopoulos A, Jolivet P, Hartmann MA, Miquel M et al (2007) At5g50600 encodes a member of the short-chain dehydrogenase reductase superfamily with 11β- and 17β-hydroxy steroid dehydrogenase activities associated with Arabidopsis thaliana seed oil bodies. Biochimie 89:222–229CrossRefPubMedGoogle Scholar
  5. Das AK, Cohen PTW, Barford D (1998) The structure of the tetratricopeptide repeats of protein phosphatase 5: implications for TPR-mediated protein–protein interactions. EMBO J 17:1192–1199CrossRefPubMedPubMedCentralGoogle Scholar
  6. Ding YF, Zhang SY, Yang L, Na HM, Zhang P, Zhang HN et al (2013) Isolating lipid droplets from multiple species. Nat Protoc 8:43–51CrossRefPubMedGoogle Scholar
  7. Dinis AM, Coutinho AP (2009) Interaction of lipid bodies with other cell organelles in the maturing pollen of Magnolia × soulangeana (Magnoliaceae). Protoplasm 238:35–46CrossRefGoogle Scholar
  8. Dyas L, Goad LJ (1994) The occurrence of free and esterified sterols in the oil bodies isolated from maize seed scutella and a celery cell suspension culture. Plant Physiol Biochem 32:799–805Google Scholar
  9. Ebbinghaus S, Kim SJ, Heyden M, Yu X, Gruebele M, Leitner DM et al (2008) Protein sequence- and pH-dependent hydration probed by terahertz spectroscopy. J Am Chem Soc 130:2374–2375CrossRefPubMedGoogle Scholar
  10. Farese RV, Walther TC (2009) Lipid droplets finally get a little R-E-S-P-E-C-T. Cell 139:855–860CrossRefPubMedPubMedCentralGoogle Scholar
  11. Fernandez DE, Qu R, Huang AH, Staehelin LA (1988) Immunogold localization of the L3 protein of maize lipid bodies during germination and seedling growth. Plant Physiol 86:270–274CrossRefPubMedPubMedCentralGoogle Scholar
  12. Frandsen GI, Mundy J, Tzen JTC (2001) Oil bodies and their associated proteins, oleosin and caleosin. Physiol Plant 112:301–307CrossRefPubMedGoogle Scholar
  13. Fujimoto T, Parton RG (2011) Not just fat: the structure and function of the lipid droplet. Cold Spring Harb Perspect Biol 3:a004838CrossRefPubMedPubMedCentralGoogle Scholar
  14. Furse S, Liddell S, Ortori CA, Williams HE, Neylon DC, Scott DJ et al (2013) The lipidome and proteome of oil bodies from Helianthus annuus (common sunflower). J Chem Biol 6:63–676CrossRefPubMedPubMedCentralGoogle Scholar
  15. Gorovits R, Fridman L, Kolot M, Rotem O, Ghanim M, Shriki O et al (2016) Tomato yellow leaf curl virus confronts host degradation by sheltering in small/midsized protein aggregates. Virus Res 213:304–313CrossRefPubMedGoogle Scholar
  16. Graham IA (2008) Seed storage oil mobilization. Ann Rev Plant Biol 59:115–142CrossRefGoogle Scholar
  17. Herman EM (2009) Seed oil body ontogeny. Microsc Microanal 15:874–875CrossRefGoogle Scholar
  18. Horn PJ, James CN, Gidda SK, Kilaru A, Dyer JM, Mullen RT et al (2013) Identification of a new class of lipid droplet-associated proteins in plants. Plant Physiol 162:1926–1936CrossRefPubMedPubMedCentralGoogle Scholar
  19. Hsieh K, Huang AH (2004) Endoplasmic reticulum, oleosins, and oils in seeds and tapetum cells. Plant Physiol 136:3427–3434CrossRefPubMedPubMedCentralGoogle Scholar
  20. Hu ZY, Wang XF, Zhan GM, Liu GH, Hua W, Wang HZ (2009) Unusually large oil bodies are highly correlated with lower oil content in Brassica napus. Plant Cell Rep 28:541–549CrossRefPubMedGoogle Scholar
  21. Huang AHC (1992) Oil bodies and oleosins in seeds. Ann Rev Plant Physiol Mol Biol 43:177–200CrossRefGoogle Scholar
  22. Huang AHC (1996) Oleosin and oil bodies in seeds and other organs. Plant Physiol 110:1055–1061CrossRefPubMedPubMedCentralGoogle Scholar
  23. Jolivet P, Roux E, D’Andrea S, Davanture M, Negroni L, Zivy M et al (2004) Protein composition of oil bodies in Arabidopsis thaliana ecotype WS. Plant Physiol Biochem 42:501–509CrossRefPubMedGoogle Scholar
  24. Jolivet P, Boulard C, Bellamy A, Larré C, Barre M, Rogniaux H et al (2009) Protein composition of oil bodies from mature Brassica napus seeds. Proteomics 9:3268–3284CrossRefPubMedGoogle Scholar
  25. Katavic V, Agrawal GK, Hajduch M, Harris SL, Thelen JJ (2006) Protein and lipid composition analysis of oil bodies from two Brassica napus cultivars. Proteomics 6:4586–4598CrossRefPubMedGoogle Scholar
  26. Krahmer N, Guo Y, Farese RV, Walther TC (2009) SnapShot: lipid droplets. Cell 139:1024–1024.e1CrossRefPubMedGoogle Scholar
  27. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 222:680–685CrossRefGoogle Scholar
  28. Lagos CF, Vecchiola A, Allende F, Fuentes CA, Tichauer JE, Valdivia C et al (2014) Identification of novel 11β-HSD1 inhibitors by combined ligand- and structure-based virtual screening. Mol Cell Endocrinol 384:71–82CrossRefPubMedGoogle Scholar
  29. Lersten NR, Czlapinski AR, Curtis JD, Freckmann R, Horner HT (2006) Oil bodies in leaf mesophyll cells of angiosperms: overview and a selected survey. Am J Bot 93:1731–1739CrossRefPubMedGoogle Scholar
  30. Lin LJ, Tzen JT (2004) Two distinct steroleosins are present in seed oil bodies. Plant Physiol Biochem 42:601–618CrossRefPubMedGoogle Scholar
  31. Lin LJ, Tai SS, Peng CC, Tzen JT (2002) Steroleosin, a sterol-binding dehydrogenase in seed oil bodies. Plant Physiol 128:1200–1211PubMedPubMedCentralGoogle Scholar
  32. Ludwig R, Appelhagen A (2005) Calculation of clathrate-like water clusters including H2O-buckminsterfullerene. Angew Chem Int Ed 44:811–815CrossRefGoogle Scholar
  33. Meesapyodsuk D, Qiu X (2011) A peroxygenase pathway involved in the biosynthesis of epoxy fatty acids in oat. Plant Physiol 157:454–463CrossRefPubMedPubMedCentralGoogle Scholar
  34. Millichip M, Tatham AS, Jackson F, Griffiths G, Shewry PR, Stobart AK (1996) Purification and characterization of oil-bodies (oleosomes) and oil-body boundary proteins (oleosins) from the developing cotyledons of sunflower (Helianthus annuus L.). Biochem J 314:333–337CrossRefPubMedPubMedCentralGoogle Scholar
  35. Murphy DJ (2001) Biogenesis and functions of lipid bodies in animals, plants and microorganisms. Prog Lipid Res 40:325–438CrossRefPubMedGoogle Scholar
  36. Murphy DJ (2012) The dynamic roles of intracellular lipid droplets: from archaea to mammals. Protoplasma 249:541–585CrossRefPubMedGoogle Scholar
  37. Murphy DJ, Vance J (1999) Mechanisms of lipid-body formation. Trends Biol Sci 24:109–115CrossRefGoogle Scholar
  38. Murphy S, Martin S, Parton RG (2009) Lipid droplet-organelle interactions; sharing the fats. BBA-Mol Cell Biol Lipids 1791:441–447CrossRefGoogle Scholar
  39. Naested H, Frandsen GI, Jauh GY, Hernandez-Pinzon I, Nielsen HB, Murphy DJ et al (2000) Caleosins: Ca2+-binding proteins associated with lipid bodies. Plant Mol Biol 44:463–476CrossRefPubMedGoogle Scholar
  40. Nelson DR, Nebert DW (2018) Cytochrome P450 (CYP) gene superfamily. In: eLS. Wiley, Chichester.  https://doi.org/10.1002/9780470015902.a0005667.pub3
  41. Nikiforidis CV, Kiosseoglou V, Scholten E (2013) Oil bodies: an insight on their microstructure—maize germ vs. sunflower seed. Food Res Int 52:136–141CrossRefGoogle Scholar
  42. Ning F, Wu XL, Zhang H, Wu ZK, Niu LJ, Yang H et al (2017) Accumulation profiles of embryonic salt-soluble proteins in maize hybrids and parental lines indicate matroclinous inheritance: a proteomic analysis. Front Plant Sci 8:1824CrossRefPubMedPubMedCentralGoogle Scholar
  43. Niu LJ, Yuan HY, Gong FP, Wu XL, Wang W (2018) Protein extraction methods shape much of the extracted proteomes. Front Plant Sci 9:802CrossRefPubMedPubMedCentralGoogle Scholar
  44. Purkrtova Z, d’Andrea S, Jolivet P, Lipovova P, Kralova B, Kodicek M et al (2007) Structural properties of caleosin: a MS and CD study. Arch Biochem Biophys 46:4335–4343Google Scholar
  45. Roberts MR, Hodge R, Ross JHE, Sorensen A, Murphy DJ, Draper J et al (1993) Characterization of a new class of oleosins suggests a male gametophyte-specific lipid storage pathway. Plant J 3:629–636CrossRefPubMedGoogle Scholar
  46. Ross JHE, Sanchez J, Millan F, Murphy DJ (1993) Differential presence of oleosins in oleogenic seed and mesocarp tissues in olive (Olea europea) and avocado (Persea americana). Plant Sci 93:203–210CrossRefGoogle Scholar
  47. Schmidt MA, Herman EM (2008) Suppression of soybean oleosin produces micro-oil bodies that aggregate into oil body/ER complexes. Mol Plant 1:910–924CrossRefPubMedGoogle Scholar
  48. Shi Q, Araie H, Bakku RK, Fukao Y, Rakwal R, Suzuki I et al (2015) Proteomic analysis of lipid body from the alkenone-producing marine haptophyte alga Tisochrysis lutea. Proteomics 15:4145–4158CrossRefPubMedPubMedCentralGoogle Scholar
  49. Shimada TL, Hara-Nishimura I (2010) Oil-body-membrane proteins and their physiological functions in plants. Biol Pharm Bullet 33:360–363CrossRefGoogle Scholar
  50. Siegler H, Valerius O, Ischebeck T, Popko J, Tourasse NJ, Vallon O et al (2017) Analysis of the lipid body proteome of the oleaginous alga Lobosphaera incisa. BMC Plant Biol 17:98CrossRefPubMedPubMedCentralGoogle Scholar
  51. Siloto RM, Findlay K, Lopez-Villalobos A, Yeung EC, Nykiforuk CL, Moloney MM (2006) The accumulation of oleosins determines the size of seed oil bodies in Arabidopsis. Plant Cell. 18:1961–1974CrossRefPubMedPubMedCentralGoogle Scholar
  52. Stroud H, Otero S, Desvoyes B, Ramírez-Parra E, Jacobsen SE, Gutierrez C (2012) Genome-wide analysis of histone H3.1 and H3.3 variants in Arabidopsis thaliana. Proc Natl Acad Sci USA 109:5370–5375CrossRefPubMedGoogle Scholar
  53. Ting JT, Lee K, Ratnayake C, Platt KA, Balsamo RA, Huang AH (1996) Oleosin genes in maize kernels having diverse oil contents are constitutively expressed independent of oil contents. Size and shape of intracellular oil bodies are determined by the oleosins/oils ratio. Planta 199:158–165CrossRefPubMedGoogle Scholar
  54. Tnani H, López I, Jouenne T, Vicient CM (2011) Protein composition analysis of oil bodies from maize embryos during germination. J Plant Physiol 168:510–513CrossRefPubMedGoogle Scholar
  55. Tnani H, López I, Jouenne T, Vicient CM (2012) Quantitative subproteomic analysis of germinating related changes in the scutellum oil bodies of Zea mays. Plant Sci 191–192:1–7CrossRefPubMedGoogle Scholar
  56. Tomlinson JW, Walker EA, Bujalska IJ, Draper N, Lavery GG, Cooper MS et al (2004) 11 beta-hydroxysteroid dehydrogenase type 1: a tissue-specific regulator of glucocorticoid response. Endocr Rev 25:831866CrossRefGoogle Scholar
  57. Tzen JTC, Huang AHC (1992) Surface structure and properties of plant seed oil bodies. J Cell Biol 117:327–335CrossRefPubMedGoogle Scholar
  58. Tzen JTC, Caom Y, Laurent P, Ratnayake C, Huang A (1993) Lipids, proteins and structure of seed oil bodies from diverse species. Plant Physiol 101:267–276CrossRefPubMedPubMedCentralGoogle Scholar
  59. Tzen JTC, Peng CC, Cheng DJ, Chen ECF, Chiu JMH (1997) A new method for seed oil body purification and examination of oil body integrity following germination. J Biochem 121:762–768CrossRefPubMedGoogle Scholar
  60. Wang N, Wu XL, Ku LX, Chen YH, Wang W (2016) Evaluation of three protein-extraction methods for proteome analysis of maize leaf midrib, a compound tissue rich in sclerenchyma cells. Front Plant Sci 7:856PubMedPubMedCentralGoogle Scholar
  61. Waschatko G, Billecke N, Schwendy S, Jaurich H, Bonn M, Vilgis TA et al (2016) Label-free in situ imaging of oil body dynamics and chemistry in germination. J R Soc Interface 13:20160677CrossRefPubMedPubMedCentralGoogle Scholar
  62. Wilkins MR, Gasteiger E, Tonella L, Ou K, Tyler M, Sanchez JC et al (1998) Protein identification with N and C-terminal sequence tags in proteome projects. J Mol Biol 278:599–608CrossRefPubMedGoogle Scholar
  63. Wood K, Frölich A, Paciaroni A, Moulin M, Härtlein M, Zaccai G et al (2008) Coincidence of dynamical transitions in a soluble protein and its hydration water: direct measurements by neutron scattering and MD simulations. J Am Chem Soc 130:4586–4587CrossRefPubMedGoogle Scholar
  64. Wu XL, Scali M, Faleri C, Wang W (2013) Polyclonal antibody preparation and immunolocalization of maize (Zea mays) seed protein EMB564. Plant Omics 6:359–363Google Scholar
  65. Wu XL, Gong FP, Yang L, Tai FJ, Hu XL, Wang W (2014a) Proteomic analysis reveals differential accumulation of small HSPs and late embryogenesis abundant proteins between ABA-deficient mutant vp5 seeds and wild-type Vp5 seeds in maize. Front Plant Sci 5:801CrossRefPubMedGoogle Scholar
  66. Wu XL, Xiong EH, Wang W, Scali M, Cresti M (2014b) Universal sample preparation method integrating trichloroacetic acid/acetone precipitation with phenol extraction for crop proteomic analysis. Nat Protoc 9:362–374CrossRefPubMedGoogle Scholar
  67. Zechner R, Zimmermann R, Eichmann TO, Kohlwein SD, Haemmerle G, Lass A et al (2012) FAT SIGNALS–lipases and lipolysis in lipid metabolism and signaling. Cell Metab 15:279–291CrossRefPubMedPubMedCentralGoogle Scholar
  68. Zehmer JK, Huang YG, Peng G, Pu J, Anderson RG, Liu P (2009) A role for lipid droplets in inter-membrane lipid traffic. Proteomics 9:914–921CrossRefPubMedPubMedCentralGoogle Scholar
  69. Zienkiewicz A, Zienkiewicz K, Rejón JD, Alché JD, Castro AJ, Rodríguez-García MI (2014) Olive seed protein bodies store degrading enzymes involved in mobilization of oil bodies. J Exp Bot 65:103–115CrossRefPubMedGoogle Scholar

Copyright information

© Franciszek Górski Institute of Plant Physiology, Polish Academy of Sciences, Kraków 2019

Authors and Affiliations

  1. 1.State Key Laboratory of Wheat and Maize Crop Science, College of Life SciencesHenan Agricultural UniversityZhengzhouChina

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