Skip to main content
SpringerLink
Log in

Salt stress enhances xylem development and expression of S-adenosyl-l-methionine synthase in lignifying tissues of tomato plants

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

S-Adenosyl-l-methionine synthase (SAM; ATP:l-methionine adenosyltransferase, EC 2.5.1.6) catalyzes the biosynthesis of S-adenosyl-l-methionine (AdoMet), a universal methyl-group donor. This enzyme is induced by salinity stress in tomato (Lycopersicon esculentum Mill.). To elucidate the role of SAM and AdoMet in the adaptation of plants to a saline environment, the expression pattern and histological distribution of SAM was investigated in control and salt-stressed tomato plants. Immunohistochemical analysis showed that SAM proteins were expressed in all cell types and plant organs, albeit with preferential accumulation in lignified tissues. Lignin deposition was estimated by histochemical tests and the extent of tissue lignification in response to salinity was quantified by image analysis. The average number of lignified cells in vascular bundles was significantly greater in plants under salt stress, with a maximal expansion of the lignified area found in the root vasculature. Accordingly, the greatest abundance of SAM gene transcripts and proteins occurred in roots. These results indicate that increased SAM activity correlated with a greater deposition of lignin in the vascular tissues of plants under salinity stress. A model is proposed in which an increased number of lignified tracheary elements in tomato roots under salt stress may enhance the cell-to-cell pathway for water transport, which would impart greater selectivity and reduced ion uptake, and compensate for diminished bulk flow of water and solutes along the apoplastic pathway.

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. 2a–n
Fig. 3a–d

Similar content being viewed by others

Abbreviations

AdoMet :

S-Adenosyl-l-methionine

SAM :

S-Adenosyl-l-methionine synthase

References

  • Azaizeh H, Steudle E (1991) Effects of salinity on water transport of excised maize (Zea mays L.) roots. Plant Physiol 97:1136–1145

    CAS  Google Scholar 

  • Belda RM, Ho C (1993) Salinity effects on the network of vascular bundles during tomato fruit development. J Hort Sci 68:557–564

    Google Scholar 

  • Boerjan W, Bauw G, Inzé D (1994) Distinct phenotypes generated by overexpression and suppression of S-adenosyl-l-methionine synthetase reveal developmental patterns of gene silencing in tobacco. Plant Cell 6:1401–1414

    Article  CAS  PubMed  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Campbell M, Sederoff RR (1996) Variation in lignin content and composition. Plant Physiol 110:3–13

    CAS  PubMed  Google Scholar 

  • Cuartero J, Fernandez-Muñoz R (1999) Tomato and salinity. Sci Hort 78:83–125

    Article  CAS  Google Scholar 

  • Cruz RT, Jordan WR, Drew MC (1992) Structural changes and associated reduction of hydraulic conductance in roots of Sorghum bicolor L. following exposure to water deficit. Plant Physiol 99:203–212

    CAS  Google Scholar 

  • De Boer AH, Volkov V (2003) Logistics of water and salt transport through the plant: structure and functioning of the xylem. Plant Cell Environ 26:87–101

    Article  Google Scholar 

  • Degenhardt B, Gimmler H (2000) Cell wall adaptations to multiple environmental stresses in maize roots. J Exp Bot 51:595–603

    Article  CAS  PubMed  Google Scholar 

  • Espartero J, Pintor-Toro JA, Pardo JM (1994) Differential accumulation of S-adenosylmethionine synthetase transcripts in response to salt stress. Plant Mol Biol 25:217–227

    CAS  PubMed  Google Scholar 

  • Gowri G, Bugos RC, Campbell WH, Maxwell, CA, Dixon RA (1991) Stress response in alfalfa (Medicago sativa L.). X. Molecular cloning and expression of S-adenosyl-l-methionine:caffeic acid 3-O-methyltranferase, a key enzyme of lignin biosynthesis. Plant Physiol 97:7–14

    CAS  Google Scholar 

  • Hall TC, Ma Y, Buchbinder BU, Pyne JW, Sun SM and Bliss FA (1978) Messenger RNA for G1 protein of french bean seeds: cell-free translation and product characterization. Proc Natl Acad Sci USA 75:3196–3200

    CAS  Google Scholar 

  • Hanson AD, Rivoal J, Burnet M, Rathinasabapathi B (1994) Biosynthesis of quaternary ammonium and tertiary sulphonium compounds in response to water deficit. In: Smirnoff N (ed) Environment and plant metabolism. Bios, Oxford, pp 189–198

  • Higuchi T (1981) Biosynthesis of lignin. In: Tanner W, Loewus FA (eds) Plant carbohydrates II. Encyclopedia of plant physiology, NS, vol 13B. Springer, Berlin Heidelberg New York, pp 194–224

  • Jones JB (1982) Hydroponics: its history and use in plant nutrition studies. J Plant Nutr 5:1003–1030

    CAS  Google Scholar 

  • Kende H (1993) Ethylene biosynthesis. Annu Rev Plant Physiol Plant Mol Biol 44:283–307

    Article  CAS  Google Scholar 

  • Lewis Ng, Yamamoto E (1990) Lignin: occurrence, biogenesis and biodegradation. Annu Rev Plant Physiol Plant Mol Biol 41:455–496

    Article  CAS  PubMed  Google Scholar 

  • Liu L, Dean JFD, Friedman WE, Eriksson KL (1994) A laccase-like phenoloxidase is correlated with lignin biosynthesis in Zinnia elegans stem tissues. Plant J 6:213–224

    Article  CAS  Google Scholar 

  • Lovisolo C, Schubert A (1998) Effects of water stress on vessel size and xylem hydraulic conductivity in Vitis vinifera L. J Exp Bot 49:693–700

    Article  CAS  Google Scholar 

  • Mathur M, Saluja D, Sachar RD (1991) Post-transciptional regulation of S-adenosylmethionine synthetase from its stored mRNA in germinating wheat embryos. Biochim Biophys Acta 1078:161–170

    CAS  PubMed  Google Scholar 

  • Peleman J, Boerjan W, Engker G, Seurinck J, Botterman J, Alliotte T, Van Montagu M, Inzé D (1989a) Strong cellular preference in the expression of a housekeeping gene of Arabidopsis thaliana encoding S-adenosylmethionine synthetase. Plant Cell 1:81–93

    Article  CAS  PubMed  Google Scholar 

  • Peleman J, Saito K, Cottyn B, Engler G, Seurinck J, Van Montagu M, Inzé D (1989b) Structure and expression analyses of the S-adenosylmethionine gene family in Arabidopsis thaliana. Gene 84:359–369

    Article  CAS  PubMed  Google Scholar 

  • Peyrano G, Taleisnik E, Quiroga M, de Forchetti SM, Tigier H (1997) Salinity effects on hydraulic conductance, lignin content and peroxidase activity in tomato roots. Plant Physiol Biochem 35:387–393

    CAS  Google Scholar 

  • Quiroga M, Guerrero G, Botella MA, Barceló A, Amaya I, Medina, Alonso FJ, Milrad de Forchetti S, Tigier H, Valpuesta V (2000) A tomato peroxidase involved in the synthesis of lignin and suberin. Plant Physiol 122:1119–1127

    Article  CAS  PubMed  Google Scholar 

  • Roth R, Boudet AM, Pont-Lezica R (1997) Lignification and cinnamyl alcohol dehydrogenase activity in developing stems of tomato and poplar: a spatial and kinetic study through tissue printing. J Exp Bot 48:247–254

    CAS  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY

    Google Scholar 

  • Schröder G, Eichel J, Breining S, Schröder J (1997) Three differentially expressed S-adenosylmethionine synthetase from Catharantus roseus: molecular and functional characterization. Plant Mol Biol 33:211–222

    Article  PubMed  Google Scholar 

  • Sewalt VHJ, Ni W, Blount JW, Jung HG, Masoud SA, Howles, PA, Lamb Ch, Dixon RA (1997) Reduced lignin content and altered lignin composition in transgenic tobacco down-regulated in expression on l-phenylalanine ammonia-lyase or cinnamate 4-hydroxylase. Plant Physiol 115:41–50

    CAS  PubMed  Google Scholar 

  • Shen B, Li C, Tarczynski MC (2002) High free-methionine and decreased lignin content result from a mutation in the Arabidopsis S-adenosyl-l-methionine synthetase 3 gene. Plant J 29:371–380

    Article  CAS  PubMed  Google Scholar 

  • Stanley KK, Luzio JP (1984) Construction of a new family of high efficiency bacterial expression vectors: identification of cDNAs clones coding for human liver proteins. EMBO J 3:1329–1434

    Google Scholar 

  • Steudle E, Peterson CA (1998) How does water get through roots? J Exp Bot 49:775–788

    Article  CAS  Google Scholar 

  • Tabor CW, Tabor H (1984) Methionine adenosyl transferase (S-adenosylmethionine synthetase) and S-adenosylmethionine decarboxylase. Adv Enzymol 56:251–282

    CAS  PubMed  Google Scholar 

  • Tiburcio AF, Kaur-Sawhney R, Galston AW (1990) Polyamine metabolism. In: Miflin BJ, Lea PJ (eds) The biochemistry of plants: a comprehensive treatise, vol 16, Intermediary nitrogen metabolism. Academic Press, Orlando, FL, pp 283–325

  • Van Breusegem F, Dekeyser R, Gielen J, Van Montagu, Caplan A (1994) Characterization of a S-adenosylmethionine synthetase gene in rice. Plant Physiol 105:1463–1464

    Article  PubMed  Google Scholar 

  • Zhong R, Ripperger A, Ye ZH (2000) Ectopic deposition of lignin in the pith of stems of two Arabidopsis mutants. Plant Physiol 123:59–69

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by grant BIO2000-0938 from the Spanish Ministerio de Ciencia y Tecnología. Additional support was provided by Junta de Andalucía.

Author information

Authors and Affiliations

  1. Instituto de Recursos Naturales y Agrobiología, C.S.I.C., 41012, Sevilla, Spain

    José Manuel Rodríguez-Galán & José Manuel Pardo

  2. Departamento de Biología Celular, Facultad de Biología, Universidad de Sevilla, 41012, Sevilla, Spain

    Inmaculada Sánchez-Aguayo, Remedios García & José Torreblanca

Authors
  1. Inmaculada Sánchez-Aguayo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. José Manuel Rodríguez-Galán
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Remedios García
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. José Torreblanca
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. José Manuel Pardo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to José Manuel Pardo.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sánchez-Aguayo, I., Rodríguez-Galán, J.M., García, R. et al. Salt stress enhances xylem development and expression of S-adenosyl-l-methionine synthase in lignifying tissues of tomato plants. Planta 220, 278–285 (2004). https://doi.org/10.1007/s00425-004-1350-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-004-1350-2

Keywords

Search

Navigation