Skip to main content

Advertisement

SpringerLink
Log in

Proteomics of embryogenic and non-embryogenic calli of a Liriodendron hybrid

  • Original Article
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

An increasing interest is focused on somatic embryogenesis induction in plants. This process usually generates both embryogenic calli (EC) and non-embryogenic calli (NEC) from the same explant. To identify specific proteins involved in embryogenesis competence, a comparative proteomics of EC and NEC in Liriodendron hybrid was performed. Proteins of EC and NEC were separated by two-dimensional gel electrophoresis (2-DE) and 14 proteins specific embryogenesis were characterized by matrix-assisted laser desorption ionization time-of-flight/time-of-flight. Among these identifying proteins, profilin may be indispensable for cell survival and division, and eIF-5A may play a functional role in embryogenic competence and further embryo development. Regulation of programmed cell death by cathepsin b-like cysteine proteinase and proteasome 20S beta1.1 subunit may have an essential part in maintaining cellular pluripotency and reprogramming for embryogenic mass. Reactive oxygen species (ROS) have a central effect on triggering cell division. However, methionine sulfoxide reductase is probably involved in protecting the cell from damage from excessive reactive oxygen species. Expression of EF-hand family proteins in embryogenic calli may mediate the calcium ion gradient for polarization and organ patterning. These identified embryogenic calli-specific proteins provide clues to understanding low conversion rate from calli cells to embryogenic cells.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Abbreviations

2-DE:

Two-dimensional gel electrophoresis

CHAPS:

3-[(3-Cholamidopropyl) dimethylammonio]-1-propanesulfonate

DTT:

Dithiothreitol

MALDI TOF/TOF MS:

Matrix-assisted laser desorption ionization tandem time-of-flight mass spectrometry

PCD:

Programmed cell death

ROS:

Reactive oxygen species

References

  • Allu PK, Marada A, Boggula Y, Karri S, Krishnamoorthy T, Sepuri NB (2015) Methionine sulfoxide reductase 2 reversibly regulates Mge1, a cochaperone of mitochondrial Hsp70, during oxidative stress. Mol Biol Cell 26:406–419

    Article  PubMed Central  PubMed  Google Scholar 

  • Anil VS, Rao KS (2000) Calcium-mediated signaling during sandalwood somatic embryogenesis. Role for exogenous calcium as second messenger. Plant Physiol 123:1301–1312

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Arruda SCC, Souza GM, Almeida M, Gonçalves AN (2000) Anatomical and biochemical characterization of the calcium effect on Eucalyptus urophylla callus morphogenesis in vitro. Plant Cell Tissue Organ Cult 63:142–154

    Article  Google Scholar 

  • Bian F, Zheng C, Qu F, Gong X, You C (2010) Proteomic analysis of somatic embryogenesis in Cyclamen persicum Mill. Plant Mol Biol Rep 28:22–31

    Article  CAS  Google Scholar 

  • Bozhkov PV, Filonova LH, Suarez MF, Helmersson A, Smertenko AP, Zhivotovsky B, von Arnold S (2004) VEIDase is a principal caspase-like activity involved in plant programmed cell death and essential for embryonic pattern formation. Cell Death Differ 11:175–182

    Article  CAS  PubMed  Google Scholar 

  • Buckley SM, Aranda-Orgilles B, Strikoudis A, Apostolou E, Loizou E, Moran-Crusio K, Farnsworth CL, Koller AA, Dasgupta R, Silva JC, Stadtfeld M, Hochedlinger K, Chen EI, Aifantis I (2013) Regulation of pluripotency and cellular reprogramming by the ubiquitin-proteasome system. Cell Stem Cell 11:783–798

    Article  Google Scholar 

  • Chatelain E, Satour P, Laugier E, Vu BL, Payet N, Rey P, Montrichard F (2013) Evidence for participation of the methionine sulfoxide reductase repair system in plant seed longevity. Proc Natl Acad Sci USA 110:3633–3638

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chesarone MA, DuPage AG, Goode BL (2010) Unleashing formins to remodel the actin and microtubule cytoskeletons. Nat Rew Mol Cell Bio 11:62–74

    Article  CAS  Google Scholar 

  • Day IS, Reddy VS, Ali GS, Reddy ASN (2002) Analysis of EF-hand-containing proteins in Arabidopsis. Genome Biol. doi:10.1186/gb-2002-3-10-research0056

    PubMed Central  PubMed  Google Scholar 

  • de Jong AJ, Schmidt ED, de Vries SC (1993) Early events in higher-plant embryogenesis. Plant Mol Biol 22:367–377

    Article  PubMed  Google Scholar 

  • Dihazi H, Dihazi GH, Jahn O, Meyer S, Nolte J, Asif AR, Mueller GA, Engel W (2011) Multipotent adult germline stem cells and embryonic stem cells functional proteomics revealed an important role of eukaryotic initiation factor 5A (Eif5a) in stem cell differentiation. J Proteome Res 10:1962–1973

    Article  CAS  PubMed  Google Scholar 

  • Dresselhaus T, Cordts S, Lorz H (1999) A transcript encoding translation initiation factor eIF-5A is stored in unfertilized egg cells of maize. Plant Mol Biol 39:1063–1071

    Article  CAS  PubMed  Google Scholar 

  • Dunn MJ (2007) Two-dimensional electrophoretic analysis of proteins associated with somatic embryogenesis development in Cupressus sempervirens L. Electrophoresis 20:1109–1119

    Google Scholar 

  • Endress V, Barriuso J, Ruperez P, Pedro Martin J, Blazquez A, Villalobos N, Guerra H, Martin L (2009) Differences in cell wall polysaccharide composition between embryogenic and non-embryogenic calli of Medicago arborea L. Plant Cell, Tissue Organ Cult 97:323–329

    Article  CAS  Google Scholar 

  • Fehér A (2014) Somatic embryogenesis-Stress-induced remodeling of plant cell fate. Biochim Biophys Acta-GRM. doi:10.1016/j.bbagrm.2014.07.005

  • Feher A, Otvos K, Pasternak TP, Szandtner AP (2008) The involvement of reactive oxygen species (ROS) in the cell cycle activation (G(0)-to-G(1) transition) of plant cells. Plant Signal Behav 3:823–826

    Article  PubMed Central  PubMed  Google Scholar 

  • Feng H, Chen Q, Feng J, Zhang J, Yang X, Zuo J (2007) Functional characterization of the arabidopsis eukaryotic translation initiation factor 5A-2 that plays a crucial role in plant growth and development by regulating cell division, cell growth, and cell death. Plant Physiol 144:1531–1545

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Friehs I (2008) Proteasome inhibition in hypertrophied myocardium. Am J Physiol Heart Circ Physiol 295:H1373–H1374

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ge ZY, Wan PJ, Li GQ, Xia Y, Han ZJ (2014) Characterization of cysteine protease-like genes in the striped rice stem borer, Chilo suppressalis. Genome. doi:10.1139/gen-2013-0188

    Google Scholar 

  • Guillen G, Lopez-Sanchez LML, San Roman-Roque C, Sanchez F, Villanueva MA (2001) Biochemical characterization of profilin from seeds of Phaseolus vulgaris L. Plant Cell Physiol 42:54–62

    Article  CAS  PubMed  Google Scholar 

  • Hussey PJ, Ketelaar T, Deeks MJ (2006) Control of the actin cytoskeleton in plant cell growth. Annu Rev Plant Biol

  • Imin N, De Jong F, Mathesius U, van Noorden G, Saeed NA, Wang XD, Rose RJ, Rolfe BG (2004) Proteome reference maps of Medicago truncatula embryogenic cell cultures generated from single protoplasts. Proteomics 4:1883–1896

    Article  CAS  PubMed  Google Scholar 

  • Imin N, Nizamidin M, Daniher D, Nolan KE, Rose RJ, Rolfe BG (2005) Proteomic analysis of somatic embryogenesis in Medicago truncatula. Explant cultures grown under 6-benzylaminopurine and 1-naphthalene acetic acid treatments. Plant Physiol 137:1250–1260

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jian R, Cheng X, Jiang J, Deng S, Hu F, Zhang J (2007) A cDNA-based random RNA interference library for functional genetic screens in embryonic stem cells. Stem Cells 25:1904–1912

    Article  CAS  PubMed  Google Scholar 

  • Jockusch BM, Murk K, Rothkegel M (2007) The profile of profilins. Rev Physiol Biochem Pharmacol 159:131–149

    CAS  PubMed  Google Scholar 

  • Karami O, Aghavaisi B, Mahmoudi Pour A (2009) Molecular aspects of somatic-to-embryogenic transition in plants. J Chem Biol 2:177–190

    Article  PubMed Central  PubMed  Google Scholar 

  • Kozieradzka-Kiszkurno M, Swierczynska J, Bohdanowicz J (2011) Embryogenesis in Sedum acre L.: structural and immunocytochemical aspects of suspensor development. Protoplasma 248:775–784

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kretsinger RH, Nockolds CE (1973) Carp muscle calcium-binding protein. II. Structure determination and general description. J Biol Chem 248:3313–3326

    CAS  PubMed  Google Scholar 

  • Lemanski BLF, Zhang C, Kochegarov A, Moses A, Lian W, Meyer J, Jia P, Jia Y, Li Y, Webster KA, Huang X, Hanna M, Achary MP, Lemanski SL, Weissbach H (2012) Protection of mouse embryonic stem cells from oxidative stress by methionine sulfoxide reductases, InTech

  • Lippert D, Zhuang J, Ralph S, Ellis DE, Gilbert M, Olafson R, Ritland K, Ellis B, Douglas CJ, Bohlmann J (2005) Proteome analysis of early somatic embryogenesis in Picea glauca. Proteomics 5:461–473

    Article  CAS  PubMed  Google Scholar 

  • Livanos P, Apostolakos P, Galatis B (2012) Plant cell division: rOS homeostasis is required. Plant Signal Behav 7:771–778

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lyngved R, Renaut J, Hausman J, Iversen T, Hvoslef-Eide A (2008) Embryo-specific proteins in Cyclamen persicum analyzed with 2-D DIGE. J Plant Growth Regul 27:353–369

    Article  CAS  Google Scholar 

  • Marsoni M, Bracale M, Espen L, Prinsi B, Negri AS, Vannini C (2008) Proteomic analysis of somatic embryogenesis in Vitis vinifera. Plant Cell Rep 27:347–356

    Article  CAS  PubMed  Google Scholar 

  • Martinez M, Rubio-Somoza I, Carbonero P, Diaz I (2003) A cathepsin B-like cysteine protease gene from Hordeum vulgare (gene CatB) induced by GA in aleurone cells is under circadian control in leaves. J Exp Bot 54:951–959

    Article  CAS  PubMed  Google Scholar 

  • Moon J, Parry G, Estelle M (2004) The ubiquitin-proteasome pathway and plant development. Plant Cell 16:3181–3195

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mtango NR, Latham KE (2007) Ubiquitin proteasome pathway gene expression varies in rhesus monkey oocytes and embryos of different developmental potential. Physiol Genomics 31:1–14

    Article  CAS  PubMed  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Namasivayam P (2007) Acquisition of embryogenic competence during somatic embryogenesis. Plant Cell, Tissue Organ Cult 90:1–8

    Article  CAS  Google Scholar 

  • Namasivayam P, Skepper J, Hanke D (2006) Identification of a potential structural marker for embryogenic competency in the Brassica napus spp. oleifera embryogenic tissue. Plant Cell Rep 25:887–895

    Article  CAS  PubMed  Google Scholar 

  • Naujokat C, Hoffmann S (2002) Role and function of the 26S proteasome in proliferation and apoptosis. Lab Invest 82:965–980

    Article  CAS  PubMed  Google Scholar 

  • Nogueira FC, Gonçalves EF, Jereissati ES, Santos M, Costa JH, Oliveira-Neto OB, Soares AA, Domont GB, Campos FA (2007) Proteome analysis of embryogenic cell suspensions of cowpea (Vigna unguiculata). Plant Cell Rep 26:1333–1343

    Article  CAS  PubMed  Google Scholar 

  • Park MH (2006) The post-translational synthesis of a polyamine-derived amino acid, hypusine, in the eukaryotic translation initiation factor 5A (eIF5A). J Biochem 139:161–169

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Parreiras-e-Silva LT, Luchessi AD, Reis RI, Oliver C, Jamur MC, Ramos RGP, Oliveira EB, Curi R, Costa-Neto CM (2010) Evidences of a role for eukaryotic translation initiation factor 5A (eIF5A) in mouse embryogenesis and cell differentiation. J Cell Physiol Suppl 225:500–505

    Article  CAS  Google Scholar 

  • Pasternak TP, Prinsen E, Ayaydin F, Miskolczi P, Potters G, Asard H, Van Onckelen HA, Dudits D, Feher A (2002) The role of auxin, pH, and stress in the activation of embryogenic cell division in leaf protoplast-derived cells of alfalfa. Plant Physiol 129:1807–1819

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pasternak TP, Otvos K, Domoki M, Feher A (2007) Linked activation of cell division and oxidative stress defense in alfalfa leaf protoplast-derived cells is dependent on exogenous auxin. Plant Growth Regul 51:109–117

    Article  CAS  Google Scholar 

  • Rani AR, Reddy VD, Prakash Babu P, Padmaja G (2005) Changes in protein profiles associated with somatic embryogenesis in peanut. Biol Plant 49:347–354

    Article  CAS  Google Scholar 

  • Rantong G, Gunawardena AHLAN (2015) Programmed cell death: genes involved in signaling, regulation, and execution in plants and animals. Botany 93:193–210

    Article  CAS  Google Scholar 

  • Rawe VY, Payne C, Schatten G (2006) Profilin and actin-related proteins regulate microfilament dynamics during early mammalian embryogenesis. Hum Reprod 21:1143–1153

    Article  CAS  PubMed  Google Scholar 

  • Santner A, Estelle M (2010) The ubiquitin-proteasome system regulates plant hormone signaling. Plant J 61:1029–1040

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sghaier-Hammami B, Drira N, Jorrín-Novo JV (2009) Comparative 2-DE proteomic analysis of date palm (Phoenix dactylifera L.) somatic and zygotic embryos. J Proteomics 73:161–177

    Article  CAS  PubMed  Google Scholar 

  • Shevchenko A, Wilm M, Vorm O, Mann M (1996) Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal Chem 68:850–858

    Article  CAS  PubMed  Google Scholar 

  • Silva Rde C, Carmo LS, Luis ZG, Silva L, Scherwinski-Pereira JE, Mehta A (2014) Proteomic identification of differentially expressed proteins during the acquisition of somatic embryogenesis in oil palm (Elaeis guineensis Jacq.). J Proteomics 104:112–127

    Article  PubMed  Google Scholar 

  • Silveira V, de Vita AM, Macedo AF, Dias MFR, Floh ES, Santa-Catarina C (2013) Morphological and polyamine content changes in embryogenic and non-embryogenic callus of sugarcane. Plant cell Tiss Organ Cult 114:351–364

    Article  CAS  Google Scholar 

  • Smertenko A, Bozhkov PV (2014) Somatic embryogenesis: life and death processes during apical–basal patterning. J Exp Bot. doi:10.1093/jxb/eru005

    PubMed  Google Scholar 

  • Sun L, Wu Y, Zou H, Su S, Li S, Shan X, Xi Jinghui, Yuan Y (2013) Comparative proteomic analysis of the H99 inbred maize (Zea mays L.) line in embryogenic and non-embryogenic callus during somatic embryogenesis. Plant cell Tiss Organ Cult 113:103–119

    Article  CAS  Google Scholar 

  • Thompson JE, Hopkins MT, Taylor C, Wang TW (2004) Regulation of senescence by eukaryotic translation initiation factor 5A: implications for plant growth and development. Trends Plant Sci 9:174–179

    Article  CAS  PubMed  Google Scholar 

  • Varhaníková M, Uvackova L, Skultety L, Pretova A, Obert B, Hajduch M (2014) Comparative quantitative proteomic analysis of embryogenic and non-embryogenic calli in maize suggests the role of oxylipins in plant totipotency. J Proteomics 104:57–65

    Article  PubMed  Google Scholar 

  • Wang S-L, Fan K-Q, Yang X, Lin Z-X, Xu X-P, Yang K-Q (2008) CabC, an EF-hand calcium-binding protein, is involved in Ca2+-mediated regulation of spore germination and aerial hypha formation in Streptomyces coelicolor. J Bacteriol 190:4061–4068

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wang F, Jing Y, Wang Z, Mao T, Samaj J, Yuan M, Ren H (2009) Arabidopsis profilin isoforms, PRF1 and PRF2 show distinctive binding activities and subcellular dsistributions. J Integr Plant Biol 51:113–121

    Article  CAS  PubMed  Google Scholar 

  • Wang T-Z, Zhang J-L, Tian Q-Y, Zhao M-G, Zhang W-H (2013) A medicago truncatula EF-hand family gene, MtCaMP1, is involved in drought and salt stress tolerance. PLoS One. doi:10.1371/journal.pone.0058952

    Google Scholar 

  • Wasteneys GO, Yang YB (2004) New views on the plant cytoskeleton. Plant Physiol 136:3884–3891

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Winkelmann T, Heintz D, Van Dorsselaer A, Serek M, Braun HP (2006) Proteomic analyses of somatic and zygotic embryos of Cyclamen persicum Mill. reveal new insights into seed and germination physiology. Planta 4:508–519

    Article  Google Scholar 

  • Witke W, Sutherland JD, Sharpe A, Arai M, Kwiatkowski DJ (2001) Profilin I is essential for cell survival and cell division in early mouse development. Proc Natl Acad Sci USA 98:3832–3836

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ye JS, Wang ZR (2002) Genetic analysis of heterosis for hybrid tulip tree. Scentia Silvae Sinicae 38:67–71

    CAS  Google Scholar 

  • Zhao P, Zhou X-M, Zhang L-Y, Wang W, Ma L-G, Yang L-B, Peng X-B, Bozhkov PV, Sun M-X (2013) A bipartite molecular module controls cell death activation in the basal cell lineage of plant embryos. PLoS Biol. doi:10.1371/journal.pbio.1001655

    Google Scholar 

  • Zhen Y, Shi J (2011) Evaluation of sample extraction methods for proteomic analysis of coniferous seeds. Acta Physiol Plant 33:1623–1630

    Article  CAS  Google Scholar 

  • Zhen Y, Zhao Z-Z, Zheng R-H, Shi J (2012) Proteomic analysis of early seed development in Pinus massoniana L. Plant Physiol Biochem 54:97–104

    Article  CAS  PubMed  Google Scholar 

  • Zhu D-Y, Cui R, Zhang Y-Y, Li H, Zhou L-M, Lou Y-J (2011) Involvement of ubiquitin-proteasome system in icariin-induced cardiomyocyte differentiation of embryonic stem cells using two-dimensional gel electrophoresis. J Cell Biochem 112:3343–3353

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by grants from the Major Research project of the Natural Science Foundation of Jiangsu Higher Education Institutions (No. 12KJA220002), and the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD).

Author information

Author notes

    Authors and Affiliations

    1. Co-Innovation Center for the Sustainable Forestry in Southern, Nanjing Forestry University, Nanjing, 210037, People’s Republic of China

      Yan Zhen, Chunying Li, Jinhui Chen, Qin Chen & Jisen Shi

    2. Department of Plant and Microbial Biology, University of California, Berkeley, CA, 94720, USA

      Yan Zhen

    Authors
    1. Yan Zhen
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Chunying Li
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Jinhui Chen
      View author publications

      You can also search for this author in PubMed Google Scholar

    4. Qin Chen
      View author publications

      You can also search for this author in PubMed Google Scholar

    5. Jisen Shi
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding author

    Correspondence to Jisen Shi.

    Additional information

    Communicated by M. Hajduch.

    Yan Zhen and Chunying Li contributed equally to this article.

    Electronic supplementary material

    Below is the link to the electronic supplementary material.

    Supplementary material 1 (DOC 4313 kb)

    Supplementary material 2 (XLS 56 kb)

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Zhen, Y., Li, C., Chen, J. et al. Proteomics of embryogenic and non-embryogenic calli of a Liriodendron hybrid. Acta Physiol Plant 37, 211 (2015). https://doi.org/10.1007/s11738-015-1963-z

    Download citation

    • Received:

    • Revised:

    • Accepted:

    • Published:

    • DOI: https://doi.org/10.1007/s11738-015-1963-z

    Keywords

    Search

    Navigation