Skip to main content
SpringerLink
Log in

Cell wall remodelling involving galactomannan de-branching influence Agrobacterium tumefaciens-mediated transformation of Coffea canephora somatic embryos

  • Original Article
  • Published:
Plant Cell, Tissue and Organ Culture (PCTOC) Aims and scope Submit manuscript

Abstract

Direct somatic embryogenesis is favoured over indirect methods for the in vitro propagation of Coffea canephora, as the frequency of somaclonal variation is usually reduced. Ethylene action inhibitors improve the tissue culture response and thus silver nitrate (AgNO3) is used for direct somatic embryogenesis in coffee. It was observed that silver thiosulphate (STS) that is a more potent ethylene action inhibitor, induced a much robust response in C. canephora cotyledonary leaf explants with 7.49 ± 0.57 and 7.08 ± 0.12 embryos/explant at 60 and 80 µM AgNO3, respectively compared to 3.3 ± 0.18 embryos/explant at 40 µM AgNO3. Transient transformation indicated that STS improved the transformation potential of embryos by enhancing Agrobacterium tumefaciens adherence to surfaces. In vitro adherence assays demonstrated that the cell wall material from STS-derived embryos provide a better substratum for adherence of Agrobacterium. Furthermore, blocking this substratum with anti-mannan hybridoma supernatant negatively effects the adherence. The presence of galactose and mannose residues in the decomposed cellulose fraction of STS treated somatic embryos are indicative of de-branching and re-modelling of galactomannan in response to ethylene inhibition. Genes of mannan biosynthesis, degradation and de-branching enzyme were affected to different extents in embryos derived in AgNO3 and STS containing somatic embryogenesis medium. The results indicate that ethylene-mediated cell wall galactomannan remodelling is vital for improving the transgenic potential in coffee.

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
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

AgNO3 :

Silver nitrate

AIR:

Alcohol insoluble residue

CSL:

Cellulose synthase-like gene

CWM:

Cell wall material

DSE:

Direct somatic embryogenesis

ISE:

Indirect somatic embryogenesis

SEMB:

Somatic embryogenesis

STS:

Silver thiosulphate

References

  • Alpizar E, Dechamp E, Espeout S, Royer M, Lecouls AC, Nicole M, Bertrand B, Lashermes P, Etienne H (2006) Efficient production of Agrobacterium rhizogenes-transformed roots and composite plants for studying gene expression in coffee roots. Plant Cell Rep 25:959–967

    Article  PubMed  CAS  Google Scholar 

  • Ashby AM, Watson MD, Loake GJ, Shaw CH (1988) Ti plasmid-specified chemotaxis of Agrobacterium tumefaciens C58C1 toward vir-inducing phenolic compounds and soluble factors from monocotyledonous and dicotyledonous plants. J Bacteriol 170:4181–4187

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bobadilla Landey R, Cenci A, Guyot R, Bertrand B, Georget F, Dechamp E, Herrera J-C, Aribi J, Lashermes P, Etienne H (2015) Assessment of genetic and epigenetic changes during cell culture ageing and relations with somaclonal variation in Coffea arabica. Plant Cell Tissue Organ Cult 122:517–531

    Article  CAS  Google Scholar 

  • de Aquino SO, de Araújo Carneiro F, Rêgo ECS, Costa Alves GS, Andrade AC, Marraccini (2018) Functional analysis of different promoter haplotypes of the coffee (Coffea canephora) CcDREB1D gene through genetic transformation of Nicotiana tabacum. Plant Cell Tissue Organ Cult 132:279–294

    Article  CAS  Google Scholar 

  • Ellis C, Karafyllidis I, Wasternack C, Turner JG (2002) The Arabidopsis mutant cev1 links cell wall signaling to jasmonate and ethylene responses. Plant Cell 14:1557–1566

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Etienne H, Bertrand B (2003) Somaclonal variation in Coffea arabica: effects of genotype and embryogenic cell suspension age on frequency and phenotype of variants. Tree Physiol 23:419–426

    Article  PubMed  CAS  Google Scholar 

  • Freitas NC, Barreto HG, Fernandes-Brum CN, Moreira RO, Chalfun-Junior A, Paiva LV (2017) Validation of reference genes for qPCR Analysis of Coffea arabica L. somatic embryogenesis-related tissues. Plant Cell Tissue Organ Cult 128:663–678

    Article  CAS  Google Scholar 

  • Fuentes SRL, Calheiros MBP, Manetti-Filho J, Vieira LGE (2000) The effects of silver nitrate and different carbohydrate sources on somatic embryogenesis in Coffea canephora. Plant Cell Tissue Org Cult 60:5–13

    Article  CAS  Google Scholar 

  • Giridhar P, Indu EP, Ramu DV, Ravishankar GA (2003) Effect of silver nitrate on in vitro shoot growth of coffee. Trop Sci 43:144–146

    Article  Google Scholar 

  • Giridhar P, Indu EP, Ravishankar GA, Chandrasekar A (2004a) Influence of triacontanol on somatic embryogenesis in Coffea arabica L. and Coffea canephora P. Ex Fr. In Vitro Cell Dev Biol-Plant 40:200–203

    Article  Google Scholar 

  • Giridhar P, Kumar V, Indu EP, Ravishankar GA, Chandrasekar A (2004b) Thidiazuron induced somatic embryogenesis in Coffea arabica L. and Coffea canephora P ex Fr. Acta Bot Croat 63:25–33

    CAS  Google Scholar 

  • Giridhar P, Indu EP, Vinod K, Chandrashekar A, Ravishankar GA (2004c) Direct somatic embryogenesis from Coffea arabica L. and Coffea canephora P ex Fr. under the influence of ethylene action inhibitor-silver nitrate. Acta Physiol Plant 26:299–305

    Article  CAS  Google Scholar 

  • Heredia JB, Cisneros-Zevallos L (2009) The effects of exogenous ethylene and methyl jasmonate on the accumulation of phenolic antioxidants in selected whole and wounded fresh produce. Food Chem 115:1500–1508

    Article  CAS  Google Scholar 

  • Hrmova M, Burton RA, Biely P, Lahstein J, Fincher GB (2006) Hydrolysis of (1,4)-β-D-mannans in barley (Hordeum vulgare L.) is mediated by the concerted action of (1,4)-β-D-mannan endohydrolase and β-D-mannosidase. Biochem J 399:77–90

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Joët T, Laffargue A, Salmona J, Doulbeau S, Descroix F, Bertrand B, Lashermes P, Dussert S (2014) Regulation of galactomannan biosynthesis in coffee seeds. J Exp Bot 65:323–337

    Article  PubMed  CAS  Google Scholar 

  • Klimaszewska K, Rutledge RG, Séguin A (2005) Genetic transformation of conifers utilizing somatic embryogenesis. In: Peña L (ed) Methods in molecular biology, vol 286, Humana Press Inc., Totowa, pp. 151–164

    Google Scholar 

  • Kong L, Yeung EC (1994) Effects of ethylene and ethylene inhibitors on white spruce somatic embryo maturation. Plant Sci 104:71–80

    Article  CAS  Google Scholar 

  • Kumar PP, Lakshmanan P, Thorpe TA (1998) Regulation of morphogenesis in plant tissue culture by ethylene. In vitro Cell Dev Biol - Plant 34:94–103

    Article  CAS  Google Scholar 

  • Kumar V, Naidu MM, Ravishankar GA (2006a) Developments in coffee biotechnology- in vitro plant propagation and crop improvement. Plant Cell Tissue Organ Cult 87:49–65

    Article  CAS  Google Scholar 

  • Kumar V, Satyanarayana KV, Itty SS, Indu EP, Giridhar P, Chandrashekar A, Ravishankar GA (2006b) Stable transformation and direct regeneration in Coffea canephora P ex. Fr. by Agrobacterium rhizogenes mediated transformation without hairy-root phenotype. Plant Cell Rep 25:214–222

    Article  PubMed  CAS  Google Scholar 

  • Kumar V, Parvatam G, Ravishankar GA (2006c) AgNO3—a potential regulator of ethylene activity and plant growth modulator. Electr J Biotech 12:1–15

    Google Scholar 

  • Kumar V, Ramakrishna A, Ravishankar GA (2007) Influence of different ethylene inhibitors on somatic embryogenesis and secondary embryogenesis from Coffea canephora P ex Fr. In Vitro Cell Dev Biol - Plant 43:602–607

    Article  CAS  Google Scholar 

  • Kumar A, Simmi PS, Shetty NP, Giridhar P (2016) Developing sustainable disease resistance in coffee: breeding vs. transgenic approaches. In: Collinge DB (ed) Plant pathogen resistance biotechnology. Wiley, Hoboken, pp 217–243

    Chapter  Google Scholar 

  • Liepman AH, Wilkerson CG, Keegstra K (2005) Expression of cellulose synthase-like (Csl) genes in insect cells reveals that CslA family members encode mannan synthases. Proc Natl Acad Sci USA 102:2221–2226

    Article  PubMed  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2–∆∆CT method. Methods 25:402–408

    Article  PubMed  CAS  Google Scholar 

  • Marcus SE, Blake AW, Benians TAS, Lee KJD, Poyser C, Donaldson L, Leroux O, Rogowski A, Petersen HL, Boraston A, Gilbert HJ, Willats WGT, Knox JP (2010) Restricted access of proteins to mannan polysaccharides in intact plant cell walls. Plant J 64:191–203

    Article  PubMed  CAS  Google Scholar 

  • Menéndez-Yuffá A, de García EG (1997) Morphogenic events during indirect somatic embryogenesis in coffee “Catimor”. Protoplasma 199:208–214

    Article  Google Scholar 

  • Mishra MK, Slater A (2012) Recent advances in genetic transformation of coffee. Biotechnol Res Int. https://doi.org/10.1155/2012/580857

    Article  PubMed  PubMed Central  Google Scholar 

  • Mofatto LS, Carneiro FA, Vieira NG, Duarte KE, Vidal RO, Alekcevetch JC, Cotta MG, Verdeil JL, Lapeyre-Montes F, Lartaud M, Leroy T, De Bellis F, Pot D, Rodrigues GC, Carazzolle MF, Pereira GAG, Andrade AC, Marraccini P (2016) Identification of candidate genes for drought tolerance in coffee by highthroughput, sequencing in the shoot apex of different Coffea arabica cultivars. BMC Plant Biol 16:94. https://doi.org/10.1186/s12870-016-0777-5

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mohanan S, Satyanarayana KV, Sridevi V, Gowda K, Giridhar P, Chandrashekar A, Ravishankar GA (2014) Evaluating the effect and effectiveness of different constructs with a conserved sequence for silencing of Coffea canephora N-methyltransferases. J Plant Biochem Biotechnol 23:399–409

    Article  CAS  Google Scholar 

  • Nascimento WM, Cantliffe DJ, Huber DJ (2004) Ethylene evolution and endo β-mannanase activity during lettuce seed germination at high temperature. Sci Agric 61:156–163

    Article  CAS  Google Scholar 

  • Nishiyama K, Guis M, Rose JKC, Kubo Y, Bennett KA, Wangjin L, Kato K, Ushijima K, Nakano R, Inaba A, Bouzayen M, Latche A, Peck JC, Bennett AB (2007) Ethylene regulation of fruit softening and cell wall disassembly in Charentais melon. J Exp Bot 58:1281–1290

    Article  PubMed  CAS  Google Scholar 

  • Nissen P (1994) Stimulation of somatic embryogenesis in carrot by ethylene: effects of modulators of ethylene biosynthesis and action. Physiol Plant 92:397–403

    Article  CAS  Google Scholar 

  • Nonaka S, Yuhashi KI, Takada K, Sugaware M, Minamisawa K, Ezura H (2008) Ethylene production in plants during transformation suppresses vir gene expression in Agrobacterium tumefaciens. New Phytol 178:647–656

    Article  PubMed  CAS  Google Scholar 

  • O’Rourke C, Gregson T, Murray L, Sadler IH, Fry SC (2015) Sugar composition of the pectic polysaccharides of charophytes, the closest algal relatives of land-plants: presence of 3-O-methyl-D-galactose residues. Ann Bot 116:225–236

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ogita S, Uefuji H, Morimoto M, Sano H (2004) Application of RNAi to confirm theobromine as the major intermediate for caffeine biosynthesis in coffee plants with potential for construction of decaffeinated varieties. Plant Mol Biol 54:931–941

    Article  PubMed  CAS  Google Scholar 

  • Park SY, Shin KS, Paek KY (2006) Increased ethylene and decreased phenolic compounds stimulate somatic embryo regeneration in leaf thin section cultures of Doritaenopsis hybrid. J Plant Biol 49:358–363

    Article  CAS  Google Scholar 

  • Quiroz-Figueroa F, Méndez-Zeel M, Larqué-Saavedra A, Loyola-Vargas V (2001) Picomolar concentrations of salicylates induce cellular growth and enhance somatic embryogenesis in Coffea arabica tissue culture. Plant Cell Rep 20:679–684

    Article  CAS  Google Scholar 

  • Quiroz-Figueroa FR, Fuentes-Cerda CFJ, Rojas-Herrera R, Loyola-Vargas VM (2002) Histological studies on the developmental stages and differentiation of two different somatic embryogenesis systems of Coffea arabica. Plant Cell Rep 20:1141–1149

    Article  CAS  Google Scholar 

  • Quiroz-Figueroa FR, Rojas-Herrera R, Galaz-Avalos RM, Loyola-Vargas VM (2006) Embryo production through somatic embryogenesis can be used to study cell differentiation in plants. Plant Cell Tissue Org Cult 86:285–301

    Article  Google Scholar 

  • Ratte HT (1999) Bioaccumulation and toxicity of silver compounds: a review. Environ Toxic Chem 18:89–108

    Article  CAS  Google Scholar 

  • Redgwell RJ, Curti D, Rogers J, Nicolas P, Fischer M (2003) Changes to the galactose/mannose ratio in galactomannans during coffee bean (Coffea arabica L.) development: implications for in vivo modification of galactomannan synthesis. Planta 217:316–326

    PubMed  CAS  Google Scholar 

  • Ribas AF, Kobayashi AK, Pereira LFP, Vieira LGE (2005) Genetic transformation of Coffea canephora by particle bombardment. Biol Plant 49:493–497

    Article  CAS  Google Scholar 

  • Ribas AF, Dechamp E, Champion A, Bertrand B, Combes M-C, Verdeil J-L, Lapeyre F, Lashermes P, Etienne H (2011) Agrobacterium-mediated genetic transformation of Coffea arabica (L.) is greatly enhanced by using established embryogenic callus cultures. BMC Plant Biol 11:92–107

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Roh KH, Kwak BK, Kim JB, Lee KR, Kim HU, Kim SH (2012) The influence of silver thiosulfate and thidiazuron on shoot regeneration from cotyledon explants of Brassica napus. J Plant Biotechnol 39:133–139

    Article  Google Scholar 

  • Roustan JP, Latche A, Fallot J (1990) Control of carrot somatic embryogenesis by AgNO3, an inhibitor of ethylene action: effect on arginine decarboxylase activity. Plant Sci 67:89–95

    Article  CAS  Google Scholar 

  • Schröder R, Atkinson RG, Redgwell RJ (2009) Re-interpreting the role of endo-β-mannanases as mannan endotransglycosylase/hydrolases in the plant cell wall. Ann Bot 104:197–204

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sridevi V, Giridhar P (2014) Establishment of somaclonal variants of Robusta coffee with reduced levels of cafestol and kahweol. In Vitro Cell Dev Biol - Plant 50:618–626

    Article  CAS  Google Scholar 

  • Sridevi V, Giridhar P, Simmi PS, Ravishankar GA (2010) Direct shoot organogenesis on hypocotyl explants with collar region from in vitro seedlings of Coffea canephora Pierre ex. Frohner cv. CxR and Agrobacterium tumefaciens-mediated transformation. Plant Cell Tissue Org Cult 101:339–347

    Article  Google Scholar 

  • Sridhar TM, Preethi D, Naidu CV (2011) Effect of silver thiosulphate on in vitro plant regeneration of Solanum nigrum (Linn.)—an important antiulcer medicinal plant. Curr Bot 2:14–16

    CAS  Google Scholar 

  • Stachel SE, Nester EW, Zambryski PC (1986) A plant cell factor induces Agrobacterium tumefaciens vir gene expression. Proc Natl Acad Sci USA 83:379–383

    Article  PubMed  CAS  Google Scholar 

  • Steinitz B, Bilavendran AD (2011) Thiosulfate stimulates growth and alleviates silver and copper toxicity in tomato root cultures. Plant Cell Tissue Org Cult 107:355–363

    Article  CAS  Google Scholar 

  • Torné JM, Moysset L, Santos M, Simón E (2001) Effects of light quality on somatic embryogenesis in Araujia sericifera. Physiol Plant 111:405–411

    Article  PubMed  Google Scholar 

  • Veen H (1983) Silver thiosulphate: an experimental tool in plant sciences. Sci Hort 20:211–224

    Article  CAS  Google Scholar 

  • Zhang W, Hu W, Wen CK (2010) Ethylene preparation and its application to physiological experiments. Plant Signal Behav 5:453–457

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhao Y, Song D, Sun J, Li L (2013) Populus endo-beta-mannanase PtrMAN6 plays a role in coordinating cell wall remodeling with suppression of secondary wall thickening through generation of oligosaccharide signals. Plant J 74:473–485

    Article  PubMed  CAS  Google Scholar 

  • Zhu Y, Nam J, Carpita NC, Matthysse AG, Gelvin SB (2003) Agrobacterium-mediated root transformation is inhibited by mutation of an Arabidopsis cellulose synthase-like gene. Plant Physiol 133:1000–1010

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Acknowledgements

The Authors thank the Director of Research, and Dr. Surya Prakash Rao (Head, Plant breeding Division), Central Coffee Research Institute, Balehonnur, Chikmagalur, India for access to the farms and collection of seed material. AK and SPS acknowledge the research fellowship from the Council of Scientific and Industrial Research (CSIR), New Delhi. The authors thank Prof. Paul Knox, University of Leeds, for LM21 Hybridoma supernatant and Dr. Prakash M. Halami and Dr. Padmaja R.J. (Department of Microbiology and Fermentation Technology, CSIR-CFTRI, Mysore, India) for extending help with ELISA. The experiment was partly funded by the SERB, Department of Science and Technology, New Delhi, India (SERB/SR/SO/PS/20/2012).

Author information

Authors and Affiliations

  1. Plant Cell Biotechnology Department, CSIR-Central Food Technological Research Institute, Mysuru, Karnataka, 570020, India

    Avinash Kumar, P. S. Simmi & Parvatam Giridhar

Authors
  1. Avinash Kumar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. P. S. Simmi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Parvatam Giridhar
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

AK conceived and designed the experiments. AK contributed to Agrobacterium-mediated transformation, CWM analysis, SEM studies and Quantitative RT-PCR for mannan metabolic genes. AK, SPS and PG contributed to production of stock for coffee in vitro cultures and somatic embryos. AK drafted the manuscript and all authors proofread the manuscript.

Corresponding author

Correspondence to Parvatam Giridhar.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Sergio J. Ochatt.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kumar, A., Simmi, P.S. & Giridhar, P. Cell wall remodelling involving galactomannan de-branching influence Agrobacterium tumefaciens-mediated transformation of Coffea canephora somatic embryos. Plant Cell Tiss Organ Cult 134, 369–382 (2018). https://doi.org/10.1007/s11240-018-1428-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11240-018-1428-3

Keywords

Search

Navigation