Advertisement

Plant Cell Reports

, Volume 36, Issue 1, pp 163–178 | Cite as

Differential proteome analysis during early somatic embryogenesis in Musa spp. AAA cv. Grand Naine

  • Marimuthu Kumaravel
  • Subbaraya Uma
  • Suthanthiram Backiyarani
  • Marimuthu Somasundaram Saraswathi
  • Muthu Mayil Vaganan
  • Muthusamy Muthusamy
  • Kallu Purayil Sajith
Original Article

Abstract

Key message

Endogenous hormone secretion proteins along with stress and defense proteins play predominant role in banana embryogenesis. This study reveals the underlying molecular mechanism during transition from vegetative to embryogenic state.

Abstract

Banana (Musa spp.) is well known globally as a food fruit crop for millions. The requirement of quality planting material of banana is enormous. Although mass multiplication through tissue culture is in vogue, high-throughput techniques like somatic embryogenesis (SE) as a mass multiplication tool needs to be improved. Apart from clonal propagation, SE has extensive applications in genetic improvement and mutation. SE in banana is completely genome-dependent and most of the commercial cultivars exhibit recalcitrance. Thus, understanding the molecular basis of embryogenesis in Musa will help to develop strategies for mass production of quality planting material. In this study, differentially expressed proteins between embryogenic calli (EC) and non-embryogenic calli (NEC) with respect to the explant, immature male flower buds (IMFB), of cv. Grand Naine (AAA) were determined using two-dimensional gel electrophoresis (2DE). The 2DE results were validated through qRT-PCR. In total, 65 proteins were identified: 42 were highly expressed and 23 were less expressed in EC compared to NEC and IMFB. qRT-PCR analysis of five candidate proteins, upregulated in EC, were well correlated with expression at transcript level. Further analysis of proteins showed that embryogenesis in banana is associated with the control of oxidative stress. The regulation of ROS scavenging system and protection of protein structure occurred in the presence of heat shock proteins. Alongside, high accumulation of stress-related cationic peroxidase and plant growth hormone-related proteins like indole-3-pyruvate monooxygenase and adenylate isopentenyltransferase in EC revealed the association with the induction of SE.

Keywords

Somatic embryogenesis Embryogenic callus Non-embryogenic callus 2DE Protein expression qRT-PCR 

Abbreviations

ACN

Acetonitrile

CHAPS

3-[(3-Cholamidopropyl) dimethylammonio] propanesulfonic acid

DAPI

4′,6-Diamidino-2-phenylindole

DTT

Dithiotreitol

EC

Embryogenic calli

3-IAA

Indole-3-acetic acid

IAA

Iodoacetamide

IMFB

Immature male flower bud

MALDI-TOF

Matrix-assisted laser desorption ionization time-of-flight

MS

Mass spectrum

NAA

Naphthaleneacetic acid

NEC

Non-embryogenic calli

PEM

Pro-embryogenic mass

ROS

Reactive oxygen species

SE

Somatic embryogenesis

2DE

Two-dimensional gel electrophoresis

Notes

Acknowledgements

Authors acknowledge the Director, NRCB for her support to conduct this research program at National Research Centre for Banana, Trichy. We are thankful to Dr. A. Akbar, Mr. K. Arun, Mr. G. Kannan, Mrs. K. Udhayanjali, Mrs. S. Lakshmi, Mr. A. Chandrasekar, Mr. A. S. Saravanakumar, Mrs. G. Valarmathi, Mr. K. Raja and Mr. Sriram Vishwanathan of NRCB for their support and critical comments while carrying out the work, data analysis and preparation of the manuscript.

Compliance with ethical standards

Conflict of interest

The authors have no conflict of interest.

Supplementary material

299_2016_2067_MOESM1_ESM.doc (296 kb)
Supplementary material 1 (DOC 295 kb)
299_2016_2067_MOESM2_ESM.doc (753 kb)
Supplementary material 2 (DOC 753 kb)
299_2016_2067_MOESM3_ESM.doc (542 kb)
Supplementary material 3 (DOC 542 kb)

References

  1. Akbar A (2011) Somatic embryogenesis through cell suspension culture in Indian commercial cultivars of Banana (Musa spp.) Thesis PhD, Bharathidasan University, TiruchirappalliGoogle Scholar
  2. Anil VS, Rao KS (2000) Calcium mediated signaling during sandalwood somatic embryogenesis. Role for exogenous calcium as second messenger. Plant Physiol 123:1301–1311CrossRefPubMedPubMedCentralGoogle Scholar
  3. Backhausen JE, Vetter S, Baalmann E, Kitzmann C, Scheibe R (1998) NAD-dependent malate dehydrogenase and glyceraldehydes 3-phosphate dehydrogenase isoenzymes play an important role in dark metabolism of various plastid types. Planta 205:359–366CrossRefGoogle Scholar
  4. Baldwin TC, Domingo C, Schindler T, Seetharaman G, Stacey N, Roberts K (2001) DcAGP1, a secreted arabinogalactan protein, is related to a family of basic proline-rich proteins. Plant Mol Biol 45:421–435CrossRefPubMedGoogle Scholar
  5. Barberini S, Savona M, Raffi D, Leonardi M, Pistelli L, Stochmal A, Vainstein A, Pistelli L, Ruffoni B (2013) Molecular cloning of SoHPPR encoding a hydroxyphenylpyruvate reductase and its expression in cell suspension cultures of Salvia officinalis. Plant Cell Tissue Organ Culture. doi: 10.1007/s11240-013-0300-8 Google Scholar
  6. Blum H, Beier H, Gross HJ (1987) Improved silver staining of plant proteins, RNA and DNA in polyacrylamide gels. Electrophoresis 8:93–99CrossRefGoogle Scholar
  7. Boutilier K, Offringa R, Sharma VK, Kieft H, Ouellet T, Zhang LM, Hattori J, Liu CM, van Lammeren AAM, Miki BLA et al (2002) Ectopic expression of BABY BOOM triggers a conversion from vegetative to embryonic growth. Plant Cell 14:1737–1749CrossRefPubMedPubMedCentralGoogle Scholar
  8. Brukhin V, Gheyselinck J, Gagliardini V, Genschik P, Grossniklaus U (2005) The RPN1 subunit of the 26S proteasome in Arabidopsis is essential for embryogenesis. Plant Cell 17:2723–2737CrossRefPubMedPubMedCentralGoogle Scholar
  9. Canovas FM, Gaudot ED, Recorbet G, Jorrin J, Mock HP, Rossignol M (2004) Plant proteome analysis. Proteomics 4:285–298CrossRefPubMedGoogle Scholar
  10. Carpentier SC, Witters E, Laukens K, Deckers P, Swennen R, Panis B (2005) Preparation of protein extracts from recalcitrant plant tissues: an evaluation of different methods for two dimensional gel electrophoresis analysis. Proteomics 5:2497–2507CrossRefPubMedGoogle Scholar
  11. Carpentier SC, Witters E, Laukens K, Van Onckelen H, Swennen R, Panis B (2007) Banana (Musa spp.) as a model to study the meristem proteome: acclimation to osmotic stress. Proteomics 7:92–105CrossRefPubMedGoogle Scholar
  12. Chen L, Zhong HY, Kuang JF, Li JG, Lu WJ, Chen JY (2011) Validation of reference genes for RT-qPCR studies of gene expression in banana fruit under different experimental conditions. Planta 234:377–390CrossRefPubMedGoogle Scholar
  13. Cordewener J, Booij H, Zandt DH, Engelen VF, Kammen A, Vries DS (1991) Tunicamycininhibited carrot somatic embryogenesis can be restored by secreted cationic peroxidase isoenzymes. Planta 184:478–486CrossRefPubMedGoogle Scholar
  14. Correia S, Vinhas R, Manadas B, Lourenco AS, Verissimo P, Canhoto JM (2012) Comparative proteomic analysis of auxin-induced embryogenic and nonembryogenic tissues of the solanaceous tree Cyphomandra betacea (Tamarillo). J Proteome Res 11:1666–1675CrossRefPubMedGoogle Scholar
  15. Dudits D, Bogre L, Gyorgyey J (1991) Molecular and cellular approaches to the analysis of plant embryo development from somatic cells in vitro. J Cell Sci 99:475–484Google Scholar
  16. Feher A, Pasternak TP, Dudits D (2003) Transition of somatic plant cells to an embryogenic state. Plant Cell Tissue Organ Culture 74:201–228CrossRefGoogle Scholar
  17. Ganapathi TR, Suprasanna P, Bapat VA, Kulkarni VM, Rao PS (1999) Somatic embryogenesis and plant regeneration from male flower buds in banana. Curr Sci 76:1228–1230Google Scholar
  18. Garavaglia BS, Thomas L, Zimaro T, Gottig N, Daurelio LD, Ndimba B, Orellano EG, Ottado J, Gehring C (2010) A plant natriuretic peptide-like molecule of the pathogen Xanthomonas axonopodis pv. Citri causes rapid changes in the proteome of its citrus host. Plant Biol 10(51):1–10Google Scholar
  19. Heck GR, Perry SE, Nichols KW, Fernandez DE (1995) AGL15, a MADS domain protein expressed in developing embryos. Plant Cell Online 7:1271CrossRefGoogle Scholar
  20. Hoenemann C, Richardt S, Kruger K, Zimmer AD, Hohe A, Rensing SA (2010) Large impact of the apoplast on somatic embryogenesis in Cyclamen persicum offers possibilities for improved developmental control invitro. Plant Biol 10(77):1–17Google Scholar
  21. Hu X, Liu L, Xiao B, Li D, Xing X, Kong X, Li D (2010) Enhanced tolerance to low temperature in tobacco by over-expression of a new maize protein phosphatase 2C, ZmPP2C2. Plant Physiol 167:1307–1315CrossRefGoogle Scholar
  22. Hurkman WJ, Tanaka CK (1986) Solubilization of plant membrane proteins for analysis by two-dimensional gel electrophoresis. Plant Physiol 81:802–806CrossRefPubMedPubMedCentralGoogle Scholar
  23. Hussein S, Ibrahim R, Kiong ALP (2006) Somatic embryogenesis: an alternate method for in vitro micropropagation. Iran J Biotechnol 4:156–161Google Scholar
  24. Imin N, Jong FD, Mathesius U, Noorden GV, Saeed NA, Wang XD, Rose RJ, Rolfe BG (2004) Proteome reference maps of Medicago truncatula embryogenic cell cultures generated from single protoplasts. Protemics 4:1883–1896CrossRefGoogle Scholar
  25. Ito D (2012) Functional analysis of Arabidopsis Nudix hydrolases having CoA and guanosine-3,5,-tetraphosphate (ppGpp) specific pyrophosphohydrolase activities. Thesis PhD, Kinki UniversityGoogle Scholar
  26. Ji A, Geng X, Zhang Y, Yang H, Wu G (2011) Advances in somatic embryogenesis research of horticultural plants. Am J Plant Sci 2:727–732CrossRefGoogle Scholar
  27. Kintzios S, Nikolaou A, Skoula M (1999) Somatic embryogenesis and invitro rosmarinic acid accumulation in Salvia officinalis and S. fruticosa leaf callus cultures. Plant Cell Rep 18:462–466CrossRefGoogle Scholar
  28. Kuroda H, Takahashi N, Shimada H, Seki M, Shinozaki K, Matsui M (2002) Classification and expression analysis of Arabidopsis F-box-containing protein genes. Plant Cell Physiol 43:1073–1085CrossRefPubMedGoogle Scholar
  29. Laemmli UK (1970) Cleavage of structural protein during the assembly of the head of bacteriophage T4. Nature 227:680–685CrossRefPubMedGoogle Scholar
  30. Lippert D, Zhuang J, Ralp 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 5:461–473CrossRefPubMedGoogle Scholar
  31. Liu H, Xie WF, Zhang L, Valpuesta V, Ye ZW, Gao QH, Duan K (2013) Auxin biosynthesis by the YUCCA6 flavin monooxygenase gene in woodland strawberry. J Integr Plant Biol 56:350–363CrossRefGoogle Scholar
  32. Lotan T, Ohto M, Yee KM, West MAL, Lo R, Kwong RW, Yamagishi K, Fischer RL, Goldberg RB, Harada JJ (1998) Arabidopsis LEAFY COTYLEDON1 is sufficient to induce embryo development in vegetative cells. Cell 93:1195–1205CrossRefPubMedGoogle Scholar
  33. Ma L, Xie L, Lin G, Jiang S, Chen H, Li H, Taka T, Samaj J, Xu C (2012) Histological changes and differences in activities of some antioxidant enzymes and hydrogen peroxide content during somatic embryogenesis of Musa AAA cv. Yueyoukang 1. Sci Hortic 144(2012):87–92CrossRefGoogle Scholar
  34. Marsoni M, Bracale M, Espen L, Prinsi B, Negri AS, Vannini C (2008) Proteomic analysis of somatic embryogenesis in Vitis vinifera. Plant Cell Rep 27:347–356CrossRefPubMedGoogle Scholar
  35. Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Science 7:405–410CrossRefGoogle Scholar
  36. Neuhoff V, Arnold N, Taube D, Ehrhardt W (1988) Improved staining of proteins in polyacrylamide gels including isoelectric focusing gels with clear background at nanogram sensitivity using Coomassie Brilliant Blue G-250 and R-250. Electrophoresis 9:255–262CrossRefPubMedGoogle Scholar
  37. Nievesi N, Nieto MS, Blanco MA, Sanchez M, Gonzalez A, Gonzalea JL, Castillo R (2003) Biochemical characterization of embryogenic and non embryogenic calluses of sugarcane. In Vitro Cell Dev Biol 39:343–345CrossRefGoogle Scholar
  38. Nolan KE, Irwanto RR, Rose RJ (2003) Auxin up-regulates MtSERK1 expression in both Medicago truncatula root-forming and embryogenic cultures. Plant Physiol 133:218–230CrossRefPubMedPubMedCentralGoogle Scholar
  39. Overvoorde PJ, Grimes HD (1994) The role of calcium and calmodulin in carrot somatic embryogenesis. Plant Cell Physiol 35:135Google Scholar
  40. Owiti J, Grossmann J, Gehrig P, Dessimoz C, Laloi C, Hansen MB, Gruissem W, Vanderschuren H (2011) iTRAQ-based analysis of changes in the cassava root proteome reveals pathways associated with post-harvest physiological deterioration. Plant J 67:145–156CrossRefPubMedGoogle Scholar
  41. Palmieri L, Picault N, Arrigoni R, Besin E, Palmieri F, Hodges M (2008) Molecular identification of three Arabidopsis thaliana mitochondrial dicarboxylate carrier isoforms: organ distribution, bacterial expression, reconstitution into liposomes and functional characterization. J Biochem 410:621–629CrossRefGoogle Scholar
  42. Pan Z, Guan R, Zhu S, Deng X (2009) Proteomic analysis of somatic embryogenesis in valencia sweet orange (Citrus sinensis Osbeck). Plant Cell Rep 28:281–289CrossRefPubMedGoogle Scholar
  43. Pan X, Yanga X, Linb G, Zoua R, Chena H, Samaj J, Xua C (2011) Ultrastructural changes and the distribution of arabinogalactan proteins during somatic embryogenesis of banana (Musa spp. AAA cv. ‘Yueyoukang 1′). Physiol Plant 142:372–389CrossRefPubMedGoogle Scholar
  44. Papaevgeniou N, Chondrogianni N (2014) The ubiquitin proteasome system in Caenorhabditis elegans and its regulation. Redox Biol 2:333–347CrossRefPubMedPubMedCentralGoogle Scholar
  45. Patena LF, Refuerzo LRC, Barba RC (2002) Somatic embryogenesis and plantlet regeneration in mango (Mangifera indica L.). In vitro cell. Dev Biol 38:173–177Google Scholar
  46. Ravi I, Uma S (2011) Phenotyping banana and plantains for adaptation to drought, in drought phenotyping in crops: from theory to practice. In: CGIAR Generation Challenge Programme, c/o CIMMYT, Mexico, pp 417–430Google Scholar
  47. Ribeiro LO, Paiva LV, Padua MS, Santos BR, Alves E, Stein VC (2012) Morphological and ultrastructural analysis of various types of Banana callus, cv. Prata ana. Acta Sci 34:423–429Google Scholar
  48. Rode C, Lindhorst K, Braun HP, Winkelmann T (2011) From callus to embryo: a proteomic view on the development and maturation of somatic embryos in Cyclamen persicum. Planta. doi: 10.1007/s00425-011-1554-1 PubMedGoogle Scholar
  49. Rodrigues EP, Torres AR, Batista JSS, Huergo L, Hungria M (2012) A simple, economical and reproducible protein extraction protocol for proteomics studies of soybean roots. Genet Mol Biol 35:348–352CrossRefPubMedPubMedCentralGoogle Scholar
  50. Sales EK, Butardo NG (2014) Molecular analysis of somaclonal variation in tissue culture derived bananas using MSAP and SSR markers. Int J Biol Biomol Agricult Food Biotechnol Eng 8(6):615–622Google Scholar
  51. Scheible WR, Pauly M (2004) Glycosyltransferases and cell wall biosynthesis: novel players and insights. Curr Opin Plant Biol 7:285–295CrossRefPubMedGoogle Scholar
  52. Schoofs H (1997) The origin of embryogenic cells in Musa. Thesis PhD, KU Leuven, LeuvenGoogle Scholar
  53. Sharifi G, Ebrahimzadeh H, Ghareyazie B, Gharechahi J, Vatankhah E (2012) Identification of differentially accumulated proteins associated with embryogenic and non-embryogenic calli in saffron (Crocus sativus L.). Proteome Sci 10(3):1–15Google Scholar
  54. Sharma SK, Millam S, Hedley PE, McNicol J, Bryan GJ (2008) Molecular regulation of somatic embryogenesis in potato: an auxin led perspective. Plant Mol Biol 68:185–201CrossRefPubMedGoogle Scholar
  55. Sidha M, Suprasanna P, Bapat VA, Kulkarni UG, Shinde BN (2006) Developing somatic embryogenic culture system and plant regeneration in banana. BARC Newslett 285:153–161Google Scholar
  56. Singh A, Pandey GK (2012) Protein phosphatases: a genomic outlook to understand their function in plants. J Plant Biochem Biotechnol. doi: 10.1007/s13562-012-0150-1
  57. Singh HP, Uma S, Selvarajan R, Karihaloo JL (2011) Micropropagation for production of quality banana planting material in Asia–Pacific. Asia–Pacific Consortium on Agricultural Biotechnology (APCoAB), New DelhiGoogle Scholar
  58. Smertenko A, Bozhkov PV (2014) Somatic embryogenesis: life and death processes during apical and basal patterning. J Exp Bot 65:1343–1360CrossRefPubMedGoogle Scholar
  59. Strosse H, Domergue R, Panis B, Escalant JV, Cote F (2003) Banana and plantain embryogenic cell suspension. In: INIBAP technical guidelines 8, MontpellierGoogle Scholar
  60. Sun L, Wu Y, Zou H, Su S, Li S, Shan X, Xi J, 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 Tissue Organ Culture 113:103–119CrossRefGoogle Scholar
  61. Suprasanna P, Desai NS, Nishanth G, Ghosh SB, Laxmi N, Bapat VA (2004) Differential gene expression in embryogenic, non-embryogenic and desiccation induced cultures of sugarcane. Sugar Technol 6:305–309CrossRefGoogle Scholar
  62. Tan EC, Karsani SA, Foo GT, Wong SM, Rahman NA, Khalid N, Othman S, Yusof R (2012) Proteomic analysis of cell suspension cultures of Boesenbergia rotunda induced by phenylalanine: identification of proteins involved in flavonoid and phenylpropanoid biosynthesis pathways. Plant Cell Tissue Organ Culture. doi: 10.1007/s11240-012-0188-8 Google Scholar
  63. Tang H, Ren Z, Krczal G (2000) Somatic embryogenesis and organogenesis from immature embryo cotyledons of three sour cherry cultivars (Prunus cerasus L.). Sci Hortic 83:109–126CrossRefGoogle Scholar
  64. Torres LF, Diniz LEC, Livramento KGD, Freire LL, Paiva LV (2015) Gene expression and morphological characterization of cell suspensions of Coffea Arabica L. cv. Catigua MG2 in different cultivation stages. Acta Physiol Plant 37:175CrossRefGoogle Scholar
  65. Tsai HL, Lue WL, Lu KJ, Hsieh MH, Wang SM, Chen J (2009) Starch synthesis in Arabidopsis is achieved by spatial cotranscription of core starch metabolism genes. Plant Physiol 151:1582–1595CrossRefPubMedPubMedCentralGoogle Scholar
  66. Uhrig RG, Labandera AM, Moorhead GB (2013) Arabidopsis PPP family of serine/threonine protein phosphatases: many targets but few engines. Trends Plant Sci 18:505–510CrossRefPubMedGoogle Scholar
  67. Uma S, Lakshmi S, Saraswathi MS, Akbar A, Mustaffa MM (2012) Plant regeneration through somatic embryogenesis from immature and mature zygotic embryos of Musa accuminata ssp. Burmannica. In vitro Cell Dev Biol Plant 48:539–545CrossRefGoogle Scholar
  68. Verdeil JL, Hocher V, Huet C, Grosdemange F, Escoute J, Ferriere N, Nicole M (2001) Ultrastructural changes in coconut calli associated with the acquisition of embryogenic competence. Annu Bot 88:9–18CrossRefGoogle Scholar
  69. Vierstra RD (1996) Proteolysis in plants: mechanisms and functions. Plant Mol Biol 32:275–302CrossRefPubMedGoogle Scholar
  70. Vinodhana NK, Ganesan NM (2013) Studies on embryogenic competence and regeneration potential with relation to anthocyanin biosynthesis in cotton (G. hirsutum). Plant Gene Trait 4:53–59Google Scholar
  71. Wang X, Niu Q, Teng C, Li C, Mu J, Chua NH, Zuo J (2009) Overexpression of PGA37/MYB118 and MYB115 promotes vegetative-to-embryonic transition in Arabidopsis. Cell Res 19:224–235CrossRefPubMedGoogle Scholar
  72. Wang X, Shia L, Linb G, Pana X, Chena H, Wua X, Taka T, Samaj J, Xua C (2013) A systematic comparison of embryogenic and non-embryogenic cells of banana (Musa spp. AAA): ultrastructural, biochemical and cell wall component analyses. Sci Hortic 159:178–185CrossRefGoogle Scholar
  73. Wisniewska A, Grabowska A, Bogiel A, Tagashira N, Zuzga S, Woycicki R, Przybecki Z, Malepszy S, Filipecki M (2012) Identification of genes up-regulated during somatic embryogenesis of cucumber. Plant Physiol Biochem 50:54–64CrossRefPubMedGoogle Scholar
  74. Wu MC, Tseng KC, Huang TH, Chang HM (2002) Pectinesterase inhibitor in rubbery Banana (Musa sapientum L.). J Food Sci 67:1337–1340CrossRefGoogle Scholar
  75. Xu C, Zhao L, Pan X, Samaj J (2011) Developmental localization and methylesterification of pectin epitopes during somatic embryogenesis of banana (Musa spp. AAA). PLoS One 6(8):e22992. doi: 10.1371/journal.pone.0022992 CrossRefPubMedPubMedCentralGoogle Scholar
  76. Yang X, Zhang X (2010) Regulation of somatic embryogenesis in higher plants. Crit Rev Plant Sci 29:36–57CrossRefGoogle Scholar
  77. Yang X, Zhang X, Yuan D, Jin F, Zhang Y, Xu J (2012) Transcript profiling reveals complex auxin signalling pathway and transcription regulation involved in dedifferentiation and redifferentiation during somatic embryogenesis in cotton. Plant Biol 12(110):1–19Google Scholar
  78. Yeh CS, Hsieh LS, Yang CC, Lee PD (2011) Molecular characterization of isopentenyltransferase (BoAIPT1) from Bambusa oldhamii expressed in Escherichia coli. Bot Stud 52:249–256Google Scholar
  79. Yuffa AM, Garcia EG, Nieto MS (1993) Comparative study of protein electrophoretic patterns during embryogenesis in Coffea arabica cv. Catimor. Plant Cell Rep 13:197–202Google Scholar
  80. Zaffagnini M, Fermani S, Costa A, Lemaire SD, Trost P (2013) Plant cytoplasmic GAPDH: redox post-translational modification and moonlighting properties. Front Plant Sci 4:1–18CrossRefGoogle Scholar
  81. Zavattieri MA (2010) Induction of somatic embryogenesis as an example of stress-related plant reactions. Electron J Biotechnol 13:1–14CrossRefGoogle Scholar
  82. Zhang J, Ma H, Chen S, Ji M, Perl A, Kovacs L, Chen S (2009) Stress response proteins’ differential expression in embryogenic and non-embryogenic callus of Vitis vinifera L. cv. Cabernet Sauvignon—a proteomic approach. Plant Sci 177:103–113CrossRefGoogle Scholar
  83. Zhao Y, Christensen SK, Fankhauser C, Cashman JR, Cohen JD, Weigel D, Chory J (2001) A role for flavin monooxygenase-like enzymes in auxin biosynthesis. Science 291:306–309CrossRefPubMedGoogle Scholar
  84. Zuo J, Niu QW, Frugis G, Chua NH (2002) The WUSCHEL gene promotes vegetative to embryonic transition in Arabidopsis. Plant J 30:349–359CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Marimuthu Kumaravel
    • 1
  • Subbaraya Uma
    • 1
  • Suthanthiram Backiyarani
    • 1
  • Marimuthu Somasundaram Saraswathi
    • 1
  • Muthu Mayil Vaganan
    • 2
  • Muthusamy Muthusamy
    • 1
  • Kallu Purayil Sajith
    • 1
  1. 1.Crop Improvement DivisionICAR, National Research Centre for BananaTiruchirappalliIndia
  2. 2.Crop Protection DivisionICAR, National Research Centre for BananaTiruchirappalliIndia

Personalised recommendations