Skip to main content
SpringerLink
Log in

Monitoring of cell wall modifications during callogenesis in Stylosanthes guianensis (Fabaceae) under salt stress conditions

  • Published:
Brazilian Journal of Botany Aims and scope Submit manuscript

Abstract

Callogenesis was induced from Stylosanthes guianensis (Aubl.) Sw. cv. CIAT-184 hypocotyl explants cultured in the presence of different concentrations of NaCl. Whereas calluses formed at 50 mM NaCl did not show significant changes, concentrations in the range of 100–250 mM NaCl influenced callus formation and survival. The concentrations which reduced the callus formation and survival by 50 % with respect to the controls (I 50) were 190 and 225 mM NaCl, respectively. Callus growth was also affected being 160 mM NaCl the concentration that reduced the fresh weight gain in 50 %, in comparison to the control. The cell walls of calluses formed at higher NaCl concentrations showed a lower cellulose content, which was accompanied by an increase in protein, phenolics, and esters, as revealed by Fourier transform infrared spectroscopy. These overall cell wall modifications were accompanied by the formation of cell wall appositions enriched with homogalacturonan and rhamnogalacturonan components, and also with an increase of arabinogalactan proteins in cell walls. These results evidence the ability of cells to adjust the cell wall composition under salt stress conditions, as part of the strategy to sustain their growth in such environment.

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
Figs. 5–12
Figs. 13–18

Similar content being viewed by others

References

  • Alonso-Simón A, García-Angulo P, Mélida H, Encina A, Álvarez JM, Acebes JL (2011) The use of FTIR spectroscopy to monitor modifications in plant cell wall architecture caused by cellulose biosynthesis inhibitors. Plant Sign Behav 6:1104–1110

    Article  Google Scholar 

  • Benderradji L, Bouzerzou H, Djekoun A, Benmahammed A (2007) Effects of NaCl stress on callus proliferation and plant regeneration from mature embryos of bread wheat (Triticum aestivum L.) cultivar Mahom Demias and Hidhab. Plant Tissue Cult Biotech 17:19–27

    Google Scholar 

  • Ben-Hayyim G (1987) Relationship between salt tolerance and resistance to polyethylene glycol-induced water stress in cultured citrus cells. Plant Physiol 85:430–433

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bressan RA, Nelson DE, Iraki NM, LaRosa PC, Singh NK, Hasegawa PM, Carpita NC (1990) Reduced cell expansion and changes in cell walls of plant cells adapted to NaCl. In: Kattermann F (ed) Environmental injury to plants. Academic Press, New York, pp 137–171

    Google Scholar 

  • Casas AM, Bressan RA, Hasegawa PM (1991) Cell growth and water relations of the halophyte, Atriplex nummularia L., in response to NaCl. Plant Cell Rep 10:81–84

    Article  CAS  PubMed  Google Scholar 

  • Chandra A (2006) A partial genetic map of Stylosanthes developed using inter-specific F2 cross. Cytologia 71:353–358

    Article  CAS  Google Scholar 

  • Cherian S, Reddy MP (2003) Evaluation of NaCl tolerance in the callus cultures of Suaeda nudiflora Moq. Biol Plant 46:193–198

    Article  CAS  Google Scholar 

  • Consoli L, Vieira MLC, de Souza Lopes, Jr C, Garcia AAF (1996) Tissue culture effects on quantitative traits in Stylosanthes guianensis (Leguminosae). Braz J Genet 19:469–474

    Google Scholar 

  • Dische Z (1962) Color reaction of carbohydrates. In: Whistler RL, Wolfrom ML (eds) Methods in carbohydrate chemistry. Academic Press, New York, pp 475–514

    Google Scholar 

  • Dornelas MC, Vieira MLC, Appezzato-da-Glória B (1992) Histological analysis of organogenesis and somatic embryogenesis induced in immature tissues of Stylosanthes scabra. Ann Bot 70:477–482

    CAS  Google Scholar 

  • El-Aref HM (2002) In vitro selection of salt-tolerant tomato plants and the changes in gene expression under salinity stress. Assiut J Agric Sci 33:23–46

    Google Scholar 

  • Ellis M, Egelund J, Schultz CJ, Bacic A (2010) Arabinogalactan-proteins: key regulators at the cell surface? Plant Physiol 153:403–419

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Encina A, Moral R, Acebes JL, Alvarez J (2001) Characterization of cell walls in bean (Phaseolus vulgaris L.) callus cultures tolerant to 2,6-dichlorobenzonitrile. Plant Sci 160:331–339

    Article  CAS  PubMed  Google Scholar 

  • Fan P, Nie L, Jiang P, Feng J, Lv S et al (2013) Transcriptome analysis of Salicornia europaea under saline conditions revealed the adaptive primary metabolic pathways as early events to facilitate salt adaptation. PLoS One 8:e80595

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Fuentes L, Pérez Y, Alemán S, Sosa D, Sosa M, González S, Infante D, Domínguez D, Mesa AR (2010) Physiological and biochemical response of Stylosanthes guianensis cv. CIAT-184 and Centrosema molle to sodium chloride stress. Pastos y Forrajes 3:173–186

    Google Scholar 

  • Gandonou CB, Errabii T, Abrini J, Idaomar M, Senhaji NS (2006) Selection of callus cultures of sugarcane (Saccharum sp.) tolerant to NaCl and their response to salt tolerance. Plant Cell Tissue Organ Cult 87:9–16

    Article  CAS  Google Scholar 

  • García-Angulo P, Willats WGT, Encina AE, Alonso-Simón A, Álvarez JM, Acebes JL (2006) Immunocytochemical characterization of the cell walls of bean cell suspensions during habituation and dehabituation to dichlobenil. Physiol Plant 27:87–99

    Article  Google Scholar 

  • Gaspar Y, Johnson KL, McKenna JA, Bacic A, Schultz CJ (2001) The complex structures of arabinogalactan-proteins and the journey towards understanding function. Plant Mol Biol 47:161–176

    Article  CAS  PubMed  Google Scholar 

  • Gonela A, Lemos EGM, Rodrigues TJD, Paterniani MLS (2004) Notas Científicas Reação enzimática ao estresse salino durante a germinação de estilosantes. Pesq Agropec Bras 39:93–95

    Article  Google Scholar 

  • González LM, López RC, Fonseca I, Ramírez R (2000) Growth stomatal frequency, DM yield and accumulation of ions in nine species of grassland legumes grown under saline conditions. Pastos y Forrajes 23:299–308

    Google Scholar 

  • Grant GT, Morris ER, Rees DA, Smith PJC, Thorn D (1973) Biological interactions between polysaccharides and divalent cations: the egg-box model. FEBS Lett 32:195–198

    Article  CAS  Google Scholar 

  • Iraki NM, Singh N, Bressan RA, Carpita NC (1989) Cell walls of tobacco cells and changes in composition associated with reduced growth upon adaptation to water and saline stress. Plant Physiol 91:48–53

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Iwai H, Ishii T, Satoh S (2001) Absence of arabinan in the side chains of the pectic polysaccharides strongly associated with cell walls of Nicotiana plumbaginifolia non-organic callus with loosely attached constituent cell. Planta 213:907–915

    Article  CAS  PubMed  Google Scholar 

  • Jones L, Seymour GB, Knox JP (1997) Localization of pectic galactan in tomato cell walls using a monoclonal antibody specific to (1-4)-β-D-galactan. Plant Physiol 113:1405–1412

    PubMed Central  CAS  PubMed  Google Scholar 

  • Kaviani B (2008) Proline accumulation and growth of soybean callus under salt and water stress. Int J Agric Biol 10:221–223

    CAS  Google Scholar 

  • Kikuchi A, Edashige Y, Ishii T, Fujii T, Satoh S (1996) Variations in the structure of neutral sugar chains in the pectic polysaccharides of morphologically different carrot calli and correlation with the size of cell clusters. Planta 198:634–639

    Article  CAS  PubMed  Google Scholar 

  • Lamport DTA, Kieliszewski MJ, Showalter AM (2006) Salt stress upregulates periplasmic arabinogalactan proteins: using salt stress to analyse AGP function. New Phytol 169:479–492

    Article  CAS  PubMed  Google Scholar 

  • Largo-Gosens A, Hernandez-Altamirano M, Garcia-Calvo L, Alonso-Simón A, Álvarez JM, Acebes JL (2014) Fourier transform mid infrared spectroscopy applications for monitoring the structural plasticity of plant cell walls. Front Plant Sci 5:303

    Article  PubMed Central  PubMed  Google Scholar 

  • Le Gall H, Philippe F, Domon JM, Gillet F, Pelloux J, Rayon C (2015) Cell wall metabolism in response to abiotic stress. Plants 4:112–166

    Article  Google Scholar 

  • Liu T-H, Nada K, Handa C, Kitashiba H, Wen X-P, Pan X-M, Moriguchi T (2006) Polyamine biosynthesis of apple callus under salts stress: importance of arginine decarboxylase pathway in stress response. J Exp Bot 57:2589–2599

    Article  CAS  PubMed  Google Scholar 

  • Lovato MB, Martins PS (1997) Genetic variability in salt tolerance during germination of Stylosanthes humilis H.B.K. and association between salt tolerance and isozymes. Braz J Genet 20:25–33

    Article  Google Scholar 

  • Lovato MB, Martins PS, Lemos Filho JPD (1994) Germination in Stylosanthes humilis populations in the presence of NaCl. Aust J Bot 42:717–723

    Article  CAS  Google Scholar 

  • Lovato MB, Lemos Filho JP, Martins PS (1999) Growth responses of Stylosanthes humilis (Fabaceae) populations to saline stress. Environ Exp Bot 41:145–153

    Article  Google Scholar 

  • Ma H, Zhao J (2010) Genome-wide identification, classification, and expression analysis of the arabinogalactan protein gene family in rice (Oryza sativa L.). J Exp Bot 61:2647–2668

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Manfield IW, Orfila C, McCartney L, Harholt J, Bernal AJ, Scheller HV, Gilmartin PM, Mikkelsen J, Knox JP, Willats WGT (2004) Novel cell wall architecture of isoxaben-habituated Arabidopsis suspension-cultured cells: global transcript profiling and cellular analysis. Plant J 40:260–275

    Article  CAS  PubMed  Google Scholar 

  • McCann MC, Shi J, Roberts K, Carpita NC (1994) Changes in pectin structure and localization during the growth of unadapted and NaCl-adapted tobacco-cells. Plant J 5:773–785

    Article  CAS  Google Scholar 

  • Mélida H, Largo-Gosens A, Novo-Uzal E, Santiago R, Pomar F, García P, García-Angulo P, Acebes JL, Alvarez J, Encina A (2015) Ectopic lignification in primary cellulose-deficient cell walls of maize cell suspension cultures. J Integr Plant Biol 57:357–372

    Article  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Muszynska A, Jarocka K, Kurczynska EU (2014) Plasma membrane and cell wall properties of an aspen hybrid (Populus tremula x tremuloides) parenchyma cells under the influence of salt stress. Acta Physiol Plant 36:1155–1165

    Article  CAS  Google Scholar 

  • Park MH, Suzuki Y, Chono M, Knox JP, Yamaguchi I (2003) CsAGP1, a gibberellin-responsive gene from cucumber hypocotyls, encodes a classical arabinogalactan protein and is involved in stem elongation. Plant Physiol 131:1450–1459

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Partridge I (1996) Protecting stylos from anthracnose. Rural Res 171:29–32

    Google Scholar 

  • Pennell RI, Knox JP, Scofield GN, Selvendran R, Roberts K (1989) A family of abundant plasma membrane-associated glycoproteins related to the arabinogalactan proteins is unique to flowering plants. J Cell Biol 108:1967–1977

    Article  CAS  PubMed  Google Scholar 

  • Pennell RI, Janniche L, Kjellbom P, Scofield GN, Peart JM, Roberts K (1991) Developmental regulation of a plasma membrane arabinogalactan protein epitope in oilseed rape flowers. Plant Cell 3:1371–1376

    Article  Google Scholar 

  • Pesqueira J, Garcia MD, Staltari S, Molina MC (2006) NaCl effects in Zea mays L. x Tripsacum dactyloides (L.) L. hybrid calli and plants. Electron J Biotechnol 9:286–290

    Article  CAS  Google Scholar 

  • Quecini VM, Alves AC, Oliveira CA, Aragao FJL, Rech EL, Almeida ERP, Gander ES, Vieira MLC (2006) Microparticle bombardment of Stylosanthes guianensis: transformation parameters and expression of a methionine-rich 2S albumin gene. Plant Cell Tissue Organ Cult 87:167–179

    Article  CAS  Google Scholar 

  • Sabba RP, Durso NA, Vaughn KC (1999) Structural and immunocytochemical characterization of the walls of DCB-habituated BY-2 tobacco cells. Int J Plant Sci 160:272–290

    Article  Google Scholar 

  • Saeman JF, Moore WE, Millet MA (1963) Sugar units present. In: Whistler RL (ed) Methods in carbohydrate chemistry, vol 3., CelluloseAcademic Press, New York, pp 54–69

    Google Scholar 

  • Sahi C, Singh A, Kumar K, Blumwald E, Grover A (2006) Salt stress response in rice: genetics, molecular biology, and comparative genomics. Funct Integr Genom 6:263–284

    Article  CAS  Google Scholar 

  • Serra AA, Couée I, Renault D, Gouesbet G, Sulmon C (2015) Metabolic profiling of Lolium perenne shows functional integration of metabolic responses to diverse subtoxic conditions of chemical stress. J Exp Bot 66:1801–1816

    Article  PubMed  Google Scholar 

  • Shedletzky E, Shmuel M, Delmer DP, Lamport DTA (1990) Adaptation and growth of tomato cells on the herbicide 2,6-dichlorobenzonitrile leads to production of unique cell walls virtually lacking a cellulose-xyloglucan network. Plant Physiol 94:980–987

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Shedletzky E, Shmuel M, Trainin T, Kalman S, Delmer DP (1992) Cell wall structure in cells adapted to growth on the cellulose-synthesis inhibitor 2,6-dichlorobenzonitrile. Plant Physiol 100:120–130

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Shen H, Mazarei M, Hisano H et al (2013) A genomics approach to deciphering lignin biosynthesis in switchgrass. Plant Cell 25:4342–4361

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Silva PO, Medina EF, Barros RS, Ribeiro DM (2014) Germination of salt-stressed seeds as related to the ethylene biosynthesis ability in three Stylosanthes species. J Plant Physiol 171:14–22

    Article  CAS  PubMed  Google Scholar 

  • Smallwood M, Yates EA, Willats WGT, Martin H, Knox JP (1996) Immunochemical comparison of membrane associated and secreted arabinogalactan proteins in rice and carrot. Planta 198:452–459

    Article  CAS  Google Scholar 

  • Talmadge KM, Keegstra K, Bauer WD, Albersheim P (1973) The structure of plant cell walls I. The macromolecular components of the walls of suspension-cultured sycamore cells with a detailed analyses of the pectic polysaccharides. Plant Physiol 51:159–173

    Google Scholar 

  • Tan L, Showalter AM, Egelund J, Hernandez-Sanchez A, Doblin MS, Bacic A (2012) Arabinogalactan-proteins and the research challenges for these enigmatic plant cell surface proteoglycans. Front Plant Sci 3:140

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Uddin MN, Hanstein S, Leubner R, Schubert S (2013) Leaf cell-wall components as influenced in the first phase of salt stress in three maize (Zea mays L.) hybrids differing in salt resistance. J Agro Crop Sci 199:405–415

    Article  CAS  Google Scholar 

  • Updegraff DM (1969) Semi-micro determination of cellulose in biological materials. Anal Biochem 32:420–424

    Article  CAS  PubMed  Google Scholar 

  • Valarini MJ, Otsuk IP, Vieira MLC (1997) Changes in N2 fixation in Stylosanthes scabra derived from tissue culture. Braz J Genet 20:713–716

    Article  CAS  Google Scholar 

  • von Hedenström H, Breckle S-W (1974) Obligate halophytes? A test with tissue culture methods. Z Pflanzenphysiol 4:183–185

    Article  Google Scholar 

  • Wells B, McCann MC, Shedletzky E, Delmer D, Roberts K (1994) Structural features of cell walls from tomato cells adapted to grow on the herbicide 2,6-dichlorobenzonitrile. J Microsc 173:155–164

    Article  CAS  Google Scholar 

  • Willats WGT, Steele-King CG, Marcus SE, Knox JP (1999) Side chains of pectic polysaccharides are regulated in relation to cell proliferation and cell differentiation. Plant J 20:619–628

    Article  CAS  PubMed  Google Scholar 

  • Wilson RH, Smith AC, Kacuráková M, Saunders PK, Wellner N, Waldron KW (2000) The mechanical properties and molecular dynamics of plant cell wall polysaccharides studied by Fourier-transform infrared spectroscopy. Plant Physiol 124:397–405

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zagorchev L, Kamenova P, Odjakova M (2014) The role of plant cell wall proteins in response to salt stress. Sci World J ID 764089. doi:10.1155/2014/764089

  • Zhong H, Läuchli A (1993) Changes of cell wall composition and polymer size in primary roots of cotton seedlings under high salinity. J Exp Bot 44:773–778

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank Dr. Antonio Encina for his helpful scientific discussion and Denise P for his help with the English revision of the manuscript.

Author information

Authors and Affiliations

  1. Centro de Estudios Biotecnológicos, Facultad de Agronomía, Universidad de Matanzas “Camilo Cienfuegos”, 44740, Matanzas, Cuba

    Leticia Fuentes, Amalia Domínguez & Yunel Pérez

  2. EEPF “Indio Hatuey”, 44800, Matanzas, Cuba

    Anesio Mesa

  3. Facultad de Biología, Universidad de la Habana, 10400, La Habana, Cuba

    Sergio González

  4. Área de Fisiología Vegetal, Facultad de Ciencias Biológicas y Ambientales, Universidad de León, 24071, León, Spain

    José Luis Acebes & Penélope García-Angulo

Authors
  1. Leticia Fuentes
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Amalia Domínguez
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yunel Pérez
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Anesio Mesa
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sergio González
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. José Luis Acebes
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Penélope García-Angulo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to José Luis Acebes.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fuentes, L., Domínguez, A., Pérez, Y. et al. Monitoring of cell wall modifications during callogenesis in Stylosanthes guianensis (Fabaceae) under salt stress conditions. Braz. J. Bot 38, 783–793 (2015). https://doi.org/10.1007/s40415-015-0196-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40415-015-0196-0

Keywords

Search

Navigation