Skip to main content
SpringerLink
Log in

Proline biosynthetic gene expression in tissue cultures of rice (Oryza sativa L.) in response to saline treatment

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

Abstract

The regulation of proline biosynthesis has been examined in callus and cell cultures of the indica-type rice cultivar Khao Dawk Mali 105 (KDML105) in response to a saline treatment (250 mM NaCl) in terms of the expression of Δ1-pyrroline-5-carboxylate reductase (OsP5CR) and members of the gene family encoding the rate-determining enzyme, Δ1-pyrroline-5-carboxylate synthase (designated OsP5CS1 and OsP5CS2). Using friable callus, growth was retarded by treatment with 250 mM NaCl within 4 days, with a significant increase in the expression of OsP5CS2 by 24 h, and a less marked induction in OsP5CS1 and OsP5CR over the same time-course. Cell suspension cultures derived from the friable callus were also treated with 250 mM NaCl and an induction in OsP5CS2 was again observed, although this was not as marked as in the friable callus, and there was no significant change in OsP5CS1 and OsP5CR expression. This is the first report that details the expression of OsP5CS1 and OsP5CS2 in tissue culture and the results show that, in common with whole plants, OsP5CS2 displays a primacy of response to saline treatment. However, this response may require a community of communicating cells, as occurs in callus tissue, rather than cell suspension cultures. This difference has implications both in terms of the biology of signaling in response to increased salinity and in the use of tissue culture to screen for saline-tolerant germplasm.

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

Similar content being viewed by others

References

  • Ahmad MSA, Javed F, Ashraf M (2007) Iso-osmotic effect of NaCl and PEG on growth, cations and free proline accumulation in callus tissue of two indica rice (Oryza sativa L.) genotypes. Plant Growth Regul 53:53–63

    Article  Google Scholar 

  • AliaSaradhi PP (1993) Suppression in mitochondrial electron transport is the prime cause behind stress induced proline accumulation. Biochem Biophys Res Commun 193:54–58

    Article  Google Scholar 

  • Armengaud P, Thiery L, Buhot N, Grenier-de March G, Savoure A (2004) Transcriptional regulation of proline biosynthesis in Medicago truncatula reveals developmental and environmental specific features. Physiol Plant 120:442–450

    Article  CAS  PubMed  Google Scholar 

  • Bohnert HJ, Shen B (1999) Transformation and compatible solutes. Sci Hortic 78:237–260

    Article  CAS  Google Scholar 

  • Delauney AJ, Verma DPS (1990) A soybean gene encoding Δ1-pyrroline-5-carboxylate reductase was isolated by functional complementation in Escherichia coli and is found to be osmoregulated. Mol Gen Genet 221:299–305

    Article  CAS  PubMed  Google Scholar 

  • Delauney AJ, Verma DPS (1993) Proline biosynthesis and osmoregulation in plants. Plant J 4:215–223

    Article  CAS  Google Scholar 

  • Fujita Y, Maggio A, Garcia-Rios M, Bressan RA, Csonka LN (1998) Comparative analysis of the regulation of expression and structures of two evolutionarily divergent genes for Δ1-pyrroline-5-carboxylate synthetase from tomato. Plant Physiol 118:661–674

    Article  CAS  PubMed  Google Scholar 

  • Garcia AB, Engler JdA, Iyer S, Gerats T, Van Montagu M, Caplan B (1997) Effects of osmoprotectants upon NaCl stress in rice. Plant Physiol 115:159–169

    CAS  PubMed  Google Scholar 

  • Ginzberg I, Stein H, Kapulnik Y, Szabados N, Schell J, Koncz C, Zilberstein A (1998) Isolation and characterization of two different cDNAs of Δ1-pyrroline-5-carboxylate synthetase in alfalfa, transcriptionally induced upon salt stress. Plant Mol Biol 38:755–764

    Article  CAS  PubMed  Google Scholar 

  • Hien DT, Jacobs M, Angenon G, Hermans C, Thu TT, Son LV, Roosens NH (2003) Proline accumulation and Δ′-pyrroline-5-carboxylate synthetase gene properties in three rice cultivars differing in salinity and drought tolerance. Plant Sci 165:1059–1068

    Article  CAS  Google Scholar 

  • Hu C-AA, Delauney AJ, Verma DPS (1992) A bifunctional enzyme (Δ′-pyrroline-5-carboxylate synthetase) catalyzes the first two steps in proline biosynthesis in plants. Proc Natl Acad Sci USA 89:9354–9358

    Article  CAS  PubMed  Google Scholar 

  • Hunter DA, Reid MS (2001) A simple and rapid method for isolating high quality RNA from flower petals. Acta Hortic 543:147–152

    CAS  Google Scholar 

  • Hur J, Jung K-H, Lee C-H, An G (2004) Stress-inducible OsP5CS2 gene is essential for salt and cold tolerance in rice. Plant Sci 167:417–426

    Article  CAS  Google Scholar 

  • Igarashi Y, Yoshiba Y, Sanada Y, Yamaguchi-Shinozaki K, Wada K, Shinozaki K (1997) Characterization of the gene for Δ1-pyrroline-5-carboxylate synthetase and correlation between the expression of the gene and salt tolerance in Oryza sativa L. Plant Mol Biol 33:857–865

    Article  CAS  PubMed  Google Scholar 

  • Kant S, Kant P, Raveh E, Barak S (2006) Evidence that differential gene expression between the halophyte Thellungiella halophila and Arabidopsis thaliana is responsible for higher levels of the compatible osmolyte proline and tight control of Na+ uptake in T. halophila. Plant Cell Environ 29:1220–1234

    Article  CAS  PubMed  Google Scholar 

  • Kavi Kishor PB, Sangam S, Amrutha RN, Laxmi PS, Naidu KR, Rao KRSS, Rao S, Reddy KJ, Theriappan P, Sreenivasulu N (2005) Regulation of proline biosynthesis, degradation, uptake and transport in higher plants: its implications in plant growth and abiotic stress tolerance. Curr Sci 88:424–438

    Google Scholar 

  • Lee TJ, Shultz RW, Hanley-Bowdoin L, Thompson W (2004) Establishment of rapidly proliferating rice cell suspension culture and its characterization by fluorescence-activated cell sorting analysis. Plant Mol Biol Rep 22:259–267

    Article  CAS  Google Scholar 

  • Liu K, Wang L, Xu Y, Chen N, Ma Q, Li F, Chong K (2007) Overexpression of OsCOIN, a putative cold inducible zinc finger protein, increased tolerance to chilling, salt and drought, and enhanced proline level in rice. Planta 226:1007–1016

    Article  CAS  PubMed  Google Scholar 

  • Lutts S, Kinet JM, Bouharmont J (1996) Effects of various salts and of mannitol on ion and proline accumulation in relation to osmotic adjustment in rice (Oryza sativa L.) callus cultures. J Plant Physiol 149:186–195

    CAS  Google Scholar 

  • Lutts S, Majerus V, Kinet J-M (1999) NaCl effects on proline metabolism in rice (Oryza sativa) seedlings. Physiol Plant 105:450–458

    Article  CAS  Google Scholar 

  • Lutts S, Almansouri M, Kinet JM (2004) Salinity and water stress have contrasting effects on the relationship between growth and cell viability during and after stress exposure in durum wheat callus. Plant Sci 167:9–18

    Article  CAS  Google Scholar 

  • Magne C, Larher F (1992) High sugar content of extracts interferes with colorimetric determination of amino acids and free proline. Anal Biochem 200:115–118

    Article  CAS  PubMed  Google Scholar 

  • Mali PC, Mehta SL (1977) Effect of drought on enzymes and free proline in rice varieties. Phytochemistry 16:1355–1357

    Article  CAS  Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681

    Article  CAS  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 

  • Raff JW, Hutchinson JF, Knox RB, Clarke AE (1979) Cell recognition: antigenic determinants of plant organs and their cultured callus cells. Differentiation 12:179–186

    Article  Google Scholar 

  • Schat H, Sharma SS, Vooijs R (1997) Heavy metal induced accumulation of free proline in a metal-tolerant and a non-tolerant ecotype of Silene vulgaris. Physiol Plant 101:477–482

    Article  CAS  Google Scholar 

  • Strizhov N, Abraham E, Okresz L, Blickling S, Zilberstein A, Schell J, Koncz C, Szabador L (1997) Differential expression of two P5CS genes controlling proline accumulation during salt stress requires ABA and is regulated by ABA1, ABI1 and AXR2 in Arabidopsis. Plant J 12:557–569

    Article  CAS  PubMed  Google Scholar 

  • Summart J, Thanonkeo P, Panichajakul S, Prathepha P, McManus MT (2010) Effect of salt stress on growth, inorganic ion and proline accumulation in Thai aromatic rice, Khao Dawk Mali 105, callus culture. Afr J Biotechnol 9:145–152

    CAS  Google Scholar 

  • Trotel P, Bouchereau A, Niogret MF, Larher F (1996) The fate of osmo-regulated proline in leaf discs of rape (Brassica napus L.) incubated in a medium of low osmolarity. Plant Sci 118:31–45

    Article  CAS  Google Scholar 

  • Vanrensburg L, Kruger GHJ, Kruger RH (1993) Proline accumulation as drought tolerance selection criterion: its relationship to membrane integrity and chloroplast ultra structure in Nicotiana tabacum L. J Plant Physiol 141:188–194

    CAS  Google Scholar 

  • Yoshiba Y, Kiyosue T, Katagiri T, Ueda H, Mizoguchi T, Yamaguchi-Shinozaki K, Wada K, Harada Y, Shinozaki K (1995) Correlation between the induction of a gene for Δ1-pyrroline-5-carboxylate synthetase and the accumulation of proline in Arabidopsis thaliana under osmotic stress. Plant J 7:751–760

    Article  CAS  PubMed  Google Scholar 

  • Zhu B, Su J, Chang M, Verma DPS, Fan Y-L, Wu R (1998) Overexpression of a Δ1-pyrroline-5-carboxylate synthetase gene and analysis of tolerance to water- and salt-stress in transgenic rice. Plant Sci 139:41–48

    Article  CAS  Google Scholar 

Download references

Acknowledgment

This work was supported by a PhD study grant to JS from the Agro-industry Consortium of Thailand.

Author information

Author notes

  1. I. Somboonwatthanaku

    Present address: Department of Biotechnology, Faculty of Technology, Mahasarakham University, Mahasarakham, 44000, Thailand

Authors and Affiliations

  1. Department of Biotechnology, Faculty of Technology, Khon Kaen University, Khon Kaen, 40002, Thailand

    I. Somboonwatthanaku

  2. Institute of Molecular BioSciences, Massey University, Private Bag 11222, Palmerston North, New Zealand

    S. Dorling, S. Leung & M. T. McManus

Authors
  1. I. Somboonwatthanaku
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. Dorling
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. S. Leung
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. M. T. McManus
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M. T. McManus.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Somboonwatthanaku, I., Dorling, S., Leung, S. et al. Proline biosynthetic gene expression in tissue cultures of rice (Oryza sativa L.) in response to saline treatment. Plant Cell Tiss Organ Cult 103, 369–376 (2010). https://doi.org/10.1007/s11240-010-9790-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11240-010-9790-9

Keywords

Search

Navigation