Plant Cell Reports

, Volume 26, Issue 1, pp 115–124 | Cite as

Enhanced stress tolerance in transgenic pine expressing the pepper CaPF1 gene is associated with the polyamine biosynthesis

Biotic and Abiotic Stress

Abstract

ERF/AP2 transcription factors play an important role in plant stress tolerance. However, little is known about the functional significance of ERF/AP2 genes in pine, compared to the model plant species Arabidopsis. Capsicum annuum pathogen and freezing tolerance-related protein 1 (CaPF1) is an ERF/AP2 transcription factor. We show here that overexpression of CaPF1 resulted in a dramatic increase in tolerance to drought, freezing, and salt stress in a gymnosperm species, eastern white pine (Pinus strobus L.). Measurement of polyamines demonstrated that the levels of putrescine (Put), spermidine (Spd), and spermine (Spm) did not increase but remain constant in CaPF1-overexpressed eastern white pine, whereas the levels decreased in the controls, probably increasing the ability of transgenic callus cultures and plants to stress tolerance. These results demonstrated that enhanced stress tolerance in transgenic pine expressing the pepper CaPF1 gene is associated with the polyamine biosynthesis and this pepper transcription factor may be used to engineer pine species for multiple stress tolerance.

Keywords

Pinus strobus L. Polyamines Stress tolerance Transcription factor 

References

  1. Apse MP, Aharon GS, Snedden WA, Blumwald E (1999) Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiporter in Arabidopsis. Science 285:1256–1258CrossRefPubMedGoogle Scholar
  2. Calkins JB, Swanson BT (1990) The distinction between living and dead plant tissue-viability tests in cold hardiness research. Cryobiology 27:194–211CrossRefGoogle Scholar
  3. Chaudhury AM, Letham S, Craig S, Dennis ES (1993) amp1—a mutant with high cytokinin levels and altered embryonic pattern, faster vegetative growth, constitutive photomorphogenesis and precocious flowering. Plant J 4:907–916CrossRefGoogle Scholar
  4. Chen W, Provart NJ, Glazebrook J et al (2002) Expression profile matrix of Arabidopsis transcription factor genes suggests their putative functions in response to environmental stresses. Plant Cell 14:559–574Google Scholar
  5. Desikan RAH, Mackerness S, Hancock JT, Neill SJ (2001) Regulation of the Arabidopsis transcriptome by oxidative stress. Plant Physiol 127:159–172CrossRefPubMedGoogle Scholar
  6. Flores HE, Galston AW (1982) Analysis of polyamines in higher plants by high performance liquid chromatography. Plant Physiol 69:701–706CrossRefGoogle Scholar
  7. Foyer CH, Deascouveries P, Kunert KJ (1994) Protection against oxygen radicals, important defense mechanism studied in transgenic plants. Plant Cell Environ 17:507–523CrossRefGoogle Scholar
  8. Gu YQ, Wildermuth MC, Chakravarthy S, Loh YT, Yang C, He X, Han Y, Martin GB (2002) Tomato transcription factors pti4, pti5, and pti6 activate defense responses when expressed in Arabidopsis. Plant Cell 14:817–831CrossRefPubMedGoogle Scholar
  9. Jaglo-Ottosen KR, Gilmour SJ, Zarka DG, Schabenberger O, Thomashow MF (1998) Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science 280:104–106CrossRefPubMedGoogle Scholar
  10. Kasuga M, Liu Q, Miura S, Yamaguchi-Shinnozaki K, Shinozaki K (1999) Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nat Biotechnol 17:287–291CrossRefPubMedGoogle Scholar
  11. Kim JB, Kang JY, Kim SY (2004) Over-expression of a transcription factor regulating ABA responsive gene expression confers multiple stress tolerance. Plant Biotechnol J 2:459–466CrossRefPubMedGoogle Scholar
  12. Kishitani S, Takanami T, Suzuki M, Oikawa M, Yokoi S, Ishitani M, Alvarez-Nakase AM, Takabe T (2000) Compatibility of glycinebetaine in rice plants, evaluation using transgenic rice plants with a gene for peroxisomal betaine aldehyde dehydrogenase from barley. Plant Cell Environ 23:107–114CrossRefGoogle Scholar
  13. Klee H, Romano CP (1994) The roles of phytohormones in development as studied in transgenic plants. Crit Rev Plant Sci 13:311–324Google Scholar
  14. Knight H, Knight MR (2001) Abiotic stress signalling pathways, specificity and cross-talk. Trends Plant Sci 6:262–267CrossRefPubMedGoogle Scholar
  15. Kovtun Y, Chiu WL, Tena G, Sheen J (2000) Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. Proc Natl Acad Sci USA 97:2940–2945CrossRefPubMedGoogle Scholar
  16. Leon-Kloosterziel KM, Gil MA, Ruijs GJ, Jacobsen SE, Olszewski NE, Schwartz SH, Zeevaart JA, Koornneef M (1996) Isolation and characterization of abscisic acid-deficient Arabidopsis mutants at two new loci. Plant J 10:655–661CrossRefPubMedGoogle Scholar
  17. 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 10:1391–1406CrossRefPubMedGoogle Scholar
  18. Moon H, Lee B, Choi G, Shin D, Prasad DT, Lee O, Kwak SS, Kim DH, Nam J, Bahk J, Hong JC, Lee SY, Cho MJ, Lim CO, Yun DJ (2003) NDP kinase 2 interacts with two oxidative stress-activated MAPKs to regulate cellular redox state and enhances multiple stress tolerance in transgenic plants. Proc Natl Acad Sci USA 100:358–363CrossRefPubMedGoogle Scholar
  19. Murata N, Ishizaki-Nishizawa O, Higashi S, Hayashi H, Tasaka Y, Nishida I (1992) Genetically engineered alteration in the chilling sensitivity of plants. Nature 356:710–713CrossRefGoogle Scholar
  20. Nakagawa H, Jiang CJ, Sakakibara H, Kojima M, Honda I, Ajisaka H, Nishijima T, Koshioka M, Homma T, Mander LN, Takatsuji H (2005) Overexpression of a petunia zinc-finger gene alters cytokinin metabolism and plant forms. Plant J 41:512–523CrossRefPubMedGoogle Scholar
  21. Nakamura T, Yokota S, Muramoto Y, Tsutsui K, Oguri Y, Fukui K, Takabe T (1997) Expression of a betaine aldehyde dehydrogenase gene in rice, a glycinebetaine nonaccumulator, and possible localization of its protein in peroxisomes. Plant J 11:1115–1120CrossRefPubMedGoogle Scholar
  22. Otegui MS, Capp R, Staehelin LA (2002) Developing seeds of Arabidopsis store different minerals in two types of vacuoles and in the endoplasmic reticulum. Plant Cell 14:1311–1327CrossRefPubMedGoogle Scholar
  23. Romano CP, Hein MB, Klee HJ (1991) Inactivation of auxin in tobacco transformed with the indoleacetic acid-lysine synthetase gene of Pseudomonas savastanoi. Genes Dev 5:438–446PubMedGoogle Scholar
  24. Roxas VP, Smith RK Jr, Allen ER, Allen RD (1997) Overexpression of glutathione S-transferase/glutathione peroxidase enhances the growth of transgenic tobacco seedlings during stress. Nat Biotechnol 15:988–991CrossRefPubMedGoogle Scholar
  25. Sakamoto A, Murata N (2002) The role of glycine betaine in the protection of plants from stress, clues from transgenic plants. Plant Cell Environ 25:163–171CrossRefPubMedGoogle Scholar
  26. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning, a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, New YorkGoogle Scholar
  27. Sanders D, Pelloux J, Brownlee C, Harper JF (2002) Calcium at the crossroads of signaling. Plant Cell 14:S401–S417PubMedGoogle Scholar
  28. Seki M, Kamei A, Yamaguchi-Shinozaki K, Shinozaki K (2003) Molecular responses to drought, salinity and frost, common and different paths for plant protection. Curr Opin Biotechnol 14:194–199CrossRefPubMedGoogle Scholar
  29. Seki M, Narusaka M, Ishida J et al (2002) Monitoring the expression profiles of 7000 Arabidopsis genes under drought cold and high-salinity stresses using a full-length cDNA, microarray. Plant J 31:279–292CrossRefPubMedGoogle Scholar
  30. Sheveleva E, Chmara W, Bohnert HJ, Jensen RG (1997) Increased salt and drought tolerance by D-ononitol production in transgenic Nicotiana tabacum L. Plant Physiol 115:1211–1219PubMedGoogle Scholar
  31. Shi H, Lee BH, Wu SJ, Zhu JK (2003) Overexpression of a plasma membrane Na+/H+ antiporter gene improves salt tolerance in Arabidopsis thaliana. Nature Biotechnol 21:81–85CrossRefGoogle Scholar
  32. Stockinger EJ, Gilmour SJ, Thomashow MF (1997) Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the C-repeat/DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. Proc Natl Acad Sci USA 94:1035–1040CrossRefPubMedGoogle Scholar
  33. Sugano S, Kaminaka H, Rybka Z, Catala R, Salinas J, Matsui K, Ohme-Takagi M, Takatsuji H (2003) Stress-responsive zinc finger gene ZPT2-3 plays a role in drought tolerance in petunia. Plant J 36:830–841CrossRefPubMedGoogle Scholar
  34. Tang W, Newton RJ (2005) Plant regeneration from callus cultures derived from mature zygotic embryos in white pine (Pinus strobus L.). Plant Cell Rep 24:1–9CrossRefPubMedGoogle Scholar
  35. Tang W, Charles TM, Newton RJ (2005a) Overexpression of the pepper transcription factor CaPF1 in transgenic Virginia pine (Pinus virginiana Mill.) confers multiple stress tolerance and enhances organ growth. Plant Mol Biol 59:603–617CrossRefPubMedGoogle Scholar
  36. Tang W, Newton RJ, Charles TM (2005b) High efficiency inducible gene expression system based on activation of a chimeric transcription factor in transgenic pine. Plant Cell Rep 24:619–628CrossRefPubMedGoogle Scholar
  37. Tantikanjana T, Yong JW, Letham DS, Griffith M, Hussain M, Ljung K, Sandberg G, Sundaresan V (2001) Control of axillary bud initiation and shoot architecture in Arabidopsis through the SUPERSHOOT gene. Genes Dev 15:1577–1588CrossRefPubMedGoogle Scholar
  38. Tarczynski MC, Jensen RG, Bohnert HJ (1993) Stress protection of transgenic tobacco by production of the osmolyte mannitol. Science 259:508–510CrossRefPubMedGoogle Scholar
  39. Warren G, McKown R, Marin AL, Teutonico R (1996) Isolation of mutations affecting the development of freezing tolerance in Arabidopsis thaliana (L.) Heynh. Plant Physiol 111:1011–1019CrossRefPubMedGoogle Scholar
  40. Welin BV, Olson A, Nylander M, Palva ET (1994) Characterization and differential expression of dhn/lea/rab-like genes during cold acclimation and drought stress in Arabidopsis thaliana. Plant Mol Biol 26:131–144CrossRefPubMedGoogle Scholar
  41. Xiong L, Schumaker KS, Zhu JK (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14(Suppl.):S165–S183PubMedGoogle Scholar
  42. Yi SY, Kim JH, Joung YH, Lee S, Kim WT, Yu SH, Choi D (2004) The pepper transcription factor CaPF1 confers pathogen and freezing tolerance in arabidopsis. Plant Physiol 136:2862–2874CrossRefPubMedGoogle Scholar
  43. Zhu JK (2002) Salt and drought stress signal transduction in plants. Ann Rev Plant Biol 53:247–273CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Wei Tang
    • 1
  • R. J. Newton
    • 1
  • C. Li
    • 2
  • T. M. Charles
    • 1
  1. 1.Department of Biology, Howell Science ComplexEast Carolina UniversityGreenvilleUSA
  2. 2.Department of Chemistry, Science and Technology BuildingEast Carolina UniversityGreenvilleUSA

Personalised recommendations