Skip to main content

Advertisement

SpringerLink
Log in

Osmyb4 expression improves adaptive responses to drought and cold stress in transgenic apples

  • Biotic and Abiotic Stress
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Constitutive expression of the rice cold-inducible Osmyb4 gene in transgenic Arabidopsis (Arabidopsis thaliana) plants improves adaptive responses to cold and drought stress, most likely due to the constitutive activation of several stress-inducible pathways and to the accumulation of several compatible solutes (e.g., glucose, fructose, sucrose, proline, glycine betaine and some aromatic compounds). Although the Osmyb4 gene seems able to activate stress responsive pathways in different species, we previously reported that its specific effect on stress tolerance depends on the transformed species. In the present work, we report the effects of the Osmyb4 expression for improving the stress response in apple (Malus pumila Mill.) plants. Namely, we found that the ectopic expression of the Myb4 transcription factor improved physiological and biochemical adaptation to cold and drought stress and modified metabolite accumulation. Based on these results it may be of interest to use Osmyb4 as a tool for improving the productivity of woody perennials under environmental stress conditions.

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
Fig. 6

Similar content being viewed by others

Abbreviations

BAP:

N6-Benzyladenine

GA3 :

Gibberellic acid

IBA:

4-Indol-3-butyric acid

NAA:

1-Napthaleneacetic acid

TDZ:

1-Phenyl-3-(1,2,3-thiadiazol-5-yl)urea

References

  • An G, Watson BD, Stachel S, Gordon MP, Nester EW (1985) New cloning vehicles for transformation of higher plants. EMBO J 4:277–284

    PubMed  CAS  Google Scholar 

  • Bates LS, Waldren RP, Teare D (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207

    Article  CAS  Google Scholar 

  • Benedict C, Skinner JS, Meng R, Chang Y, Bhalerao R, Huner NPA, Finn CE, Chen THH, Hurry V (2006) The CBF1-dependent low temperature signaling pathway, regulon and increase in freeze tolerance are conserved in Populus spp. Plant Cell Environ 29:1259–1272

    Article  PubMed  CAS  Google Scholar 

  • Bhatnagar-Mathur P, Vadez V, Sharma KK (2008) Transgenic approaches for abiotic stress tolerance in plants: retrospect and prospects. Plant Cell Rep 27:411–424

    Article  PubMed  CAS  Google Scholar 

  • Bohnert HJ, Jensen RG (1996) Strategies for engineering water-stress tolerance in plants. Trends Biotechnol 14:89–97

    Article  CAS  Google Scholar 

  • Bohnert HJ, Nelson DE, Jensen RG (1995) Adaptations to environmental stresses. Plant Cell 7:1099–1111

    Article  PubMed  CAS  Google Scholar 

  • Bracale M, Coraggio I (2003) Chilling and freezing stresses in plants: cellular responses and molecular strategies for adaptation. In: Sanità di Toppi L, Pawlik-Skowronska B (eds) Abiotic stresses in plants. Kluwer Academic Publishers, Dordrecht, pp 36–53

    Google Scholar 

  • Bray EA (1997) Plant responses to water deficit. Trends Plant Sci 2:48–54

    Article  Google Scholar 

  • Coraggio I, Tuberosa R (2004) Molecular basis of plant adaptation to abiotic stresses and approaches to enhance tolerance to hostile environments. In: Christou P, Klee H (eds) Handbook of plant biotechnology. Wiley, Chichester, pp 413–468

    Google Scholar 

  • Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12:13–15

    Google Scholar 

  • Dubouzet JG, Sakuma Y, Ito Y, Kasuga M, Dubouzet EG, Miura S, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought-, high salt- and cold-responsive gene expression. Plant J 33:751–763

    Article  PubMed  CAS  Google Scholar 

  • Durrant WE, Rowland O, Piedras P, Hammond-Kosack KE, Jones JDJ (2000) cDNA-AFLP reveals a striking overlap in race-specific resistance and wound response gene expression profiles. Plant Cell 12:963–977

    Article  PubMed  CAS  Google Scholar 

  • Gilmour SJ, Sebolt AM, Salazar MP, Everard JD, Thomashow MF (2000) Overexpression of the Arabidopsis CBF3 transcriptional activator mimics multiple biochemical changes associated with cold acclimation. Plant Physiol 124:1854–1865

    Article  PubMed  CAS  Google Scholar 

  • Hare PD, Cress WA (1997) Metabolic implications of stress induced proline accumulation in plants. Plant Growth Regul 21:79–102

    Article  CAS  Google Scholar 

  • Hare PD, du Plessis S, Cress WA (1996) Stress-induced changes in plant gene expression: prospects for enhancing agricultural productivity in South Africa. S Afr J Sci 92:431–439

    CAS  Google Scholar 

  • Hare PD, Cress WA, Van Staden J (1998) Dissecting the roles of osmolytes accumulation during stress. Plant Cell Environ 21:535–553

    Article  CAS  Google Scholar 

  • Holefors A, Xue ZT, Welander M (1998) Transformation of the apple rootstock M26 with the rolA gene and its influence on growth. Plant Sci 136:69–78

    Article  CAS  Google Scholar 

  • Hood EE, Helmer GL, Fraley RT, Chilton MD (1986) The hypervirulence of Agrobacterium tumefaciens A281 is encoded in a region of pTiBo542 outside of T-DNA. J Bacteriol 168:1291–1301

    PubMed  CAS  Google Scholar 

  • Hsieh TH, Lee JT, Yang PT, Chiu LH, Charng YY, Wang YC, Chan MT (2002) Heterologous expression of the Arabidopsis CBF1 gene confers elevated tolerance to chilling and oxidative stresses in transgenic tomato. Plant Physiol 129:1086–1094

    Article  PubMed  CAS  Google Scholar 

  • Hsu SY, Hsu YT, Kao CH (2003) The effect of polyethylene glycol on proline accumulation in rice leaves. Biol Plant 46:73–78

    Article  CAS  Google Scholar 

  • Ito Y, Katsura K, Maruyama K, Taji T, Kobayashi M, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2006) Functional analysis of rice DREB1/CBF-type transcription factors involved in cold-responsive gene expression in transgenic rice. Plant Cell Physiol 47:141–153

    Article  PubMed  CAS  Google Scholar 

  • Jaglo KR, Kleff S, Amundsen K, Zhang X, Haake V, Zhang J, Deits T, Thomashow MF (2001) Components of the Arabidopsis CBF cold response pathway are conserved in Brassica napus and other plant species. Plant Physiol 127:910–917

    Article  PubMed  CAS  Google Scholar 

  • James DJ, Dandekar AM (1991) Regeneration and transformation of apple (Malus pumila Mill.). In: Plant tissue culture manual, vol B-8. Kluwer Academic Publishers, Dordrecht, pp 1–18

  • Kasuga M, Liu Q, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1999) Improving plant drought, salt and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nat Biotechnol 17:287–291

    Article  PubMed  CAS  Google Scholar 

  • Kavi Kishore 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 

  • Knight H, Knight MR (2001) Abiotic stress signaling pathways: specificity and cross-talk. Trends Plant Sci 6:262–267

    Article  PubMed  CAS  Google Scholar 

  • Lee JT, Prasad V, Yang PT, WU JF, Ho THD, Charng YY, Chan MT (2003) Expression of Arabidopsis CBF1 regulated by an ABA/stress inducible promoter in transgenic tomato confers stress tolerance without affecting yield. Plant Cell Environ 26:1181–1190

    Article  CAS  Google Scholar 

  • Lee SC, Huh KW, An K, An G, Kim SR (2004) Ectopic expression of a cold-inducible transcription factor, CBF1/DREB1b, in transgenic rice (Oryza sativa L.). Mol Cells 18:107–114

    PubMed  CAS  Google Scholar 

  • Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1998) Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA-binding domain separate two cellular signal transduction pathways in drought- and low temperature—responsive gene expression, respectively in Arabidopsis. Plant Cell 10:1391–1406

    Article  PubMed  CAS  Google Scholar 

  • Mancuso S (2000) Electrical resistance changes during exposure to low temperature measure chilling and freezing tolerance in olive tree (Olea europaea L.) plants. Plant Cell Environ 23:291–299

    Article  Google Scholar 

  • Mata CG, Lamattina L (2001) Nitric oxide induces stomatal closure and enhances the adaptive plant responses against drought stress. Plant Physiol 126:1196–1204

    Article  PubMed  CAS  Google Scholar 

  • Mattana M, Biazzi E, Consonni R, Locatelli F, Vannini C, Provera S, Coraggio I (2005) Overexpression of Osmyb4 enhances compatible solute accumulation and increases stress tolerance of Arabidopsis thaliana. Physiol Plant 125:212–223

    Article  CAS  Google Scholar 

  • Moore S (1968) Amino acid analysis: aqueous dimethyl sulfoxide as solvent for the ninhydrin reaction. J Biol Chem 243:6281–6283

    PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Murata N, Ishizakinis Hizawa Q, Higashi S, Hayashi H, Tasaka Y, Nishida I (1992) Genetically engineered alteration in the chilling sensitivity of plants. Nature 356:710–713

    Article  CAS  Google Scholar 

  • Pandolfi D, Solinas G, Valle G, Coraggio I (1997) Cloning of a cDNA encoding a novel myb gene (accession no. Y11414) highly expressed in cold stressed rice coleoptiles (PGR PGR97–079). Plant Physiol 114:747

    Article  Google Scholar 

  • Pino MT, Skinner JS, Park EJ, Jeknic Z, Hayes PM, Thomashow MF, Chen TH (2007) Use of a stress inducible promoter to drive ectopic AtCBF expression improves potato freezing tolerance while minimizing negative effects on tuber yield. Plant Biotechnol J 5:591–604

    Article  PubMed  CAS  Google Scholar 

  • Rhodes D, Verslues PE, Sharp RE (1999) Role of amino acids in abiotic stress resistance. In: Singh BK (ed) Plant amino acids: biochemistry and biotechnology. Marcel Dekker, New York, pp 319–356

    Google Scholar 

  • Saxe H, Cannell MGR, Johnsen O, Ryan MG, Vourlitis G (2001) Tree and forest functioning in response to global warming. New Phytol 149:369–400

    Article  CAS  Google Scholar 

  • Schenk PM, Kazan K, Wilson I, Anderson JP, Richmond T, Somerville SC, Manners JM (2000) Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proc Natl Acad Sci USA 97:11655–11660

    Article  PubMed  CAS  Google Scholar 

  • Sedira M, Holefors A, Welander M (2001) Protocol for transformation of apple rootstock Jork 9 with the rolB gene and its influence on rooting. Plant Cell Rep 20:517–524

    Article  CAS  Google Scholar 

  • Seki M, Narusaka M, Abe H, Kasuga M, Yamaguchi-Shinozaki K, Carnici P, Hayashizaki Y, Shinozaki K (2001) Monitoring the expression pattern of 1300 Arabidopsis genes under drought and cold stresses by using a full-length cDNA microarray. Plant Cell 13:61–72

    Article  PubMed  CAS  Google Scholar 

  • Selas V, Piovesan G, Adams JM, Bernabei M (2002) Climatic factors controlling reproduction and growth of Norway spruce in southern Norway. Can J For Res 32:217–225

    Article  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K (1997) Gene expression and signal transduction in water-stress response. Plant Physiol 115:327–334

    Article  PubMed  CAS  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K (2000) Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways. Curr Opin Plant Biol 3:217–233

    PubMed  CAS  Google Scholar 

  • Smirnoff N (1998) Plant resistance to environmental stress. Curr Opin Biotechnol 9:214–219

    Article  PubMed  CAS  Google Scholar 

  • Thomashow MF (1998) Role of cold-responsive genes in plant freezing tolerance. Plant Physiol 118:1–8

    Article  PubMed  CAS  Google Scholar 

  • Thomashow MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol 50:571–599

    Article  CAS  Google Scholar 

  • Vannini C, Locatelli F, Bracale M, Magnani E, Marsoni M, Osnato M, Mattana M, Baldoni E, Coraggio I (2004) Overexpression of the rice Osmyb4 gene increases chilling and freezing tolerance of Arabidopsis thaliana plants. Plant J 37:115–127

    Article  PubMed  CAS  Google Scholar 

  • Vannini C, Iriti M, Bracale M, Locatelli F, Faoro F, Croce P, Pirona R, Di Maro A, Coraggio I, Genga A (2006) The ectopic expression of the rice Osmyb4 gene in Arabidopsis increases tolerance to abiotic, environmental and biotic stresses. Physiol Mol Plant Pathol 69:26–42

    Article  CAS  Google Scholar 

  • Vannini C, Campa M, Iriti M, Genga A, Faoro F, Carravieri S, Rotino GL, Rossoni M, Spinardi A, Bracale M (2007) Evaluation of transgenic tomato plants ectopically expressing the rice Osmyb4 gene. Plant Sci 173:231–239

    Article  CAS  Google Scholar 

  • Xing W, Rajashekar CB (2001) Glycine betaine involvement in freezing tolerance and water stress in Arabidopsis thaliana. Environ Exp Bot 46:21–28

    Article  PubMed  CAS  Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki K (1994) A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low temperature or high salt stress. Plant Cell 6:251–264

    Article  PubMed  CAS  Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803

    Article  PubMed  CAS  Google Scholar 

  • Zhang X, Fowler SG, Cheng H, Lou Y, Rhee SY, Stockinger EJ, Tomashow MF (2004) Freezing-sensitive tomato has a functional CBF cold response pathway, but a CBF regulon that differs from that of freezing-tolerant Arabidopsis. Plant J 39:905–919

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Dr. D. J. James for providing the GS92 apple clone. This work was partially supported by the FIRB-strategic project postgenome, Program of the Italian Ministry of University and Scientific Research (code RBNE01LAC).

Author information

Authors and Affiliations

  1. Dipartimento di Ortoflorofrutticoltura, Università di Firenze, Viale delle Idee, 30, 50019, Sesto Fiorentino, Firenze, Italy

    Gemma Pasquali & Stefano Biricolti

  2. Istituto di Biologia e Biotecnologia Agraria, CNR, Via Bassini, 15, 20133, Milan, Italy

    Franca Locatelli, Elena Baldoni & Monica Mattana

Authors
  1. Gemma Pasquali
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Stefano Biricolti
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Franca Locatelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Elena Baldoni
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Monica Mattana
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Monica Mattana.

Additional information

Communicated by J.C. Register.

Gemma Pasquali and Stefano Biricolti have contributed equally to this work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Material (DOC 110 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pasquali, G., Biricolti, S., Locatelli, F. et al. Osmyb4 expression improves adaptive responses to drought and cold stress in transgenic apples. Plant Cell Rep 27, 1677–1686 (2008). https://doi.org/10.1007/s00299-008-0587-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-008-0587-9

Keywords

Search

Navigation