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The novel gene CpEdi-9 from the resurrection plant C. plantagineum encodes a hydrophilic protein and is expressed in mature seeds as well as in response to dehydration in leaf phloem tissues

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Abstract

The resurrection plant Craterostigma plantagineum Hochst. is used as an experimental system to investigate desiccation tolerance in higher plants. A search for genes activated during early stages of dehydration identified the gene CpEdi-9, which is expressed in mature seeds and in response to dehydration in the phloem cells of vascular tissues of leaves. Elements for the tissue-specific expression pattern reside in the isolated promoter of the CpEdi-9 gene, as shown through the analysis of transgenic plants. The CpEdi-9 promoter could be a suitable tool for expressing genes in the vascular system of dehydrated plants. CpEdi-9 encodes a small (10 kDa) hydrophilic protein, which does not have significant sequence homologies to known genes. The predicted protein CpEDI-9 shares some physicochemical features with LEA proteins from plants and a nematode. Based on the unique expression pattern and on the nucleotide sequence we propose that CpEdi-9 defines a new class of hydrophilic proteins that are supposed to contribute to cellular protection during dehydration. This group of proteins may have evolved because desiccation tolerance requires the abundant expression of protective proteins during early stages of dehydration in all tissues.

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Abbreviations

ABA :

Abscisic acid

ABRE :

ABA-responsive element

Edi :

Early dehydration induced

GUS :

Glucuronidase

LEA :

Late embryogenesis abundant

MU :

Methylumbelliferone

References

  • Alamillo J, Almoguera C, Bartels D, Jordano J (1995) Constitutive expression of small heat shock proteins in vegetative tissues of the resurrection plant Craterostigma plantagineum. Plant Mol Biol 29:1093–1099

    CAS  PubMed  Google Scholar 

  • Bartels D (1999) Late embryogenesis abundant (LEA) proteins: expression and regulation in the resurrection plant Craterostigma plantagineum, Chapter 19. In: MF Smallwood MF, Clavert CM, Bowles DJ (eds) Plant responses to environmental stress. BIOS, Oxford, pp 143–160

  • Bartels D, Salamini F (2001) Desiccation tolerance in the resurrection plant Craterostigma plantagineum. A contribution to the study of drought tolerance at the molecular level. Plant Physiol 127:1346–1353

    CAS  PubMed  Google Scholar 

  • Bartels D, Schneider K, Terstappen G, Piatkowski D, Salamini F (1990) Molecular cloning of abscisic acid modulated genes which are induced during desiccation of the resurrection plant Craterostigma plantagineum. Planta 181:27–34

    CAS  Google Scholar 

  • Bartels D, Furini A, Ingram J, Salamini F (1996) Responses of plants to dehydration stress: a molecular analysis. Plant Growth Regul 20:111–118

    CAS  Google Scholar 

  • Bechtold N, Ellis J, Pelletier G (1993) In planta Agrobacterium mediated gene transfer by infiltration of adult Arabidopsis thaliana plants. CR Acad Sci Paris Life Sci 316:1194–1196.

    CAS  Google Scholar 

  • Bhattacharyya-Pakrasi M, Peng J, Elmer JS, Laco G, Shen P, Kaniewska MB, Kononowicz H, Wen F, Hodges TK, Beachy RN (1993) Specificity of a promoter from the rice tungro bacilliform virus for expression in phloem tissues. Plant J 4:71–79

    Article  CAS  PubMed  Google Scholar 

  • Bockel C, Salamini F, Bartels D (1998) Isolation and characterization of genes expressed during early events of the dehydration process in the resurrection plant Craterostigma plantagineum. J Plant Physiol 152:158–166

    CAS  Google Scholar 

  • Bravo LA, Gallardo J, Navarrete A, Olave N, Martinez J, Alberdi M, Close TJ. Corcuera LJ (2003) Cryoprotective activity of a cold-induced dehydrin purified from barley. Physiol Plant 118:262–269

    Article  CAS  Google Scholar 

  • Brears T, Walker EL, Coruzzi GM (1991) A promoter sequence involved in cell-specific expression of the pea glutamine synthetase GS3A gene in organs of transgenic tobacco and alfalfa. Plant J 1:235–244

    CAS  PubMed  Google Scholar 

  • Busk PK, Pages M (1998) Regulation of abscisic acid-induced transcription. Plant Mol Biol 37:425–435

    CAS  PubMed  Google Scholar 

  • Bustos MB, Guiltinan J, Jordano J, Begum D, Kalkan FA, Hall TC (1989) Regulation of beta-glucuronidase expression in transgenic tobacco plants by an A/T rich, cis-acting sequence found upstream of a french bean beta-phaseolin gene. Plant Cell 1:839–853

    Article  CAS  PubMed  Google Scholar 

  • Close TJ (1997) Dehydrins: a commonalty in the response of plants to dehydration at low temperature. Physiol Plant 100:291–296

    Article  Google Scholar 

  • Colmenero-Flores JM, Campos F, Garciarrubio A, Covarrubias AA (1997) Characterization of Phaseolus vulgaris cDNA clones responsive to water deficit—identification of a novel late embryogenesis abundant-like protein. Plant Mol Biol 35:393–405

    CAS  PubMed  Google Scholar 

  • Cuming A (1999) LEA proteins. In: Shewry P, Casey R (eds) Seed proteins. Kluwer, Dordrecht, pp 753–780

  • Devereux J, Haerberli P, Smithies O (1984) A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res 12:387–395

    PubMed  Google Scholar 

  • DeWitt ND, Harper JF, Sussman MR (1991) Evidence for a plasma membrane proton pump in phloem cells of higher plants. Plant J 1:121–128

    CAS  PubMed  Google Scholar 

  • Ditzer A, Kirch HH, Nair A, Bartels D (2001) Molecular characterization of two alanine-rich Lea genes abundantly expressed in the resurrection plant C. plantagineum in response to osmotic stress and ABA. J Plant Physiol 158:623–633

    CAS  Google Scholar 

  • Dure III L (1993) Structural motifs in Lea proteins. In: Plant responses to cellular dehydration during environmental stress. Close T, Bray EA (eds) Current topics in plant physiology, vol 10. The American Society of Plant Physiologists, Rockville, MD, pp 91–103

  • Dure III L, Crouch M, Harada J, Ho T-H, Mundy J, Quatrano R, Thomas T, Sung ZR (1989) Common amino acid sequence domains among the Lea proteins of higher plants. Plant Mol Biol 12:475–486

    CAS  Google Scholar 

  • Feinberg AP, Vogelstein B (1984) A technique for radiolabelling DNA restrcition endonuclease fragments to high specific activity. Anal Biochem 137:266–267

    CAS  PubMed  Google Scholar 

  • Furini A, Parcy F, Salamini F, Bartels D (1996) Differential regulation of two aba-inducibie genes from Craterostigma plantagineum in transgenic Arabidopsis plants. Plant Mol Biol 30:343–349

    CAS  PubMed  Google Scholar 

  • Gaff DF (1971) Desiccation-tolerant plants in southern Africa. Science 174:209–224

    Google Scholar 

  • Galau GA, Hughes DW, Dure III L (1986) Abscisic acid induction of clones cotton late embryogenesis abundant (Lea) mRNA. Plant Mol Biol 7:155–170

    CAS  Google Scholar 

  • Goyal K, Tisi L, Basran A, Browne J, Burnell A, Zurdo J, Tunnacliffe A (2003) Transition from natively unfolded to folded state induced by desiccation in an anhydrobiotic nematode protein. J Biol Chem 278:12977–12984

    Article  CAS  PubMed  Google Scholar 

  • Guevara-Garcia A, Mosqueda-Cano G, Argüello-Astorga G, Simpson J, Herrera-Estrella L (1993) Tissue-specific and wound-inducible pattern of expression of the mannopine synthase promoter is determined by the interaction between positive and negative cis-regulatory elements. Plant J 4:495–505

    Article  CAS  PubMed  Google Scholar 

  • Hara M, Terashima S, Kuboi T (2001) Characterization and cryoprotective activity of cold-responsive dehydrin from Citrus unshiu. J Plant Physiol 158:1333–1339

    CAS  Google Scholar 

  • Hara M, Terashima S, Fukaya T, Kuboi T (2003) Enhancement of cold tolerance and inhibition of lipid peroxidation by citrus dehydrin in transgenic tobacco. Planta 217:290–298

    CAS  PubMed  Google Scholar 

  • Hattori T, Vasil V, Rosenkrans L, Hannah LC, McCarty DR, Vasil IK (1992) The Viviparous-1 gene and abscisic acid activate the C1 regulatory gene or anthocyanin biosynthesis during seed maturation in maize. Genes Devel 6:609–618

    CAS  PubMed  Google Scholar 

  • Hedley PE, Maddison AL, Davidson D, Machray GC (2000) Differential expression of invertase genes in internal and external phloem tissues of potato (Solanum tuberosum L.) J Exp Bot 51:817–821

    Google Scholar 

  • Hehn A, Rohde W (1998) Characterization of cis-acting elements affecting strength and phloem specificity of the coconut foliar decay virus promoter. J Gen Virol 79:1495–1499

    CAS  PubMed  Google Scholar 

  • Horsch RB, Frey J, Hoffmann N, Eichholtz D, Rogers S, Fraley R (1985) A simple method for transferring genes into plants. Science 227:1229–1231

    CAS  Google Scholar 

  • Hull GA, Bies N, Twell D, Delseny M (1996) Analysis of a promoter of an abscisic acid responsive late embryogenesis abundant gene of Arabidopsis thaliana. Plant Sci 114:181–192

    Google Scholar 

  • Imai R, Chang L, Ohta A, Bray EA, Takagi M (1996) A lea-class gene of tomato confers salt and freezing tolerance when expressed in Saccharomyces cerevisae. Gene 170:243–248

    Article  CAS  PubMed  Google Scholar 

  • Ingram J, Bartels D (1996) The molecular basis of dehydration tolerance in plants. Annu Rev Plant Physiol Plant Mol Biol 47:377–403

    CAS  Google Scholar 

  • Ismail AM, Hall AE, Close TJ (1999) Allelic variation of a dehydrin gene cosegregates with chilling tolerance during seedling emergence. Proc Natl Acad Sci USA 96:13566–13570

    CAS  PubMed  Google Scholar 

  • Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusion: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901–3907

    CAS  PubMed  Google Scholar 

  • Kirch HH, Nair A, Bartels D (2001) Novel ABA- and dehydration-inducible aldehyde dehydrogenase genes isolated from the resurrection plants Craterostigma plantagineum and Arabidopsis thaliana. Plant J 28:555–567

    Article  CAS  PubMed  Google Scholar 

  • Leopold AC, Bruni F, Williams RJ (1992) Water in dry organisms. In: Somero GN, Osmond CB, Bolos CL (eds) Water and life. Springer, Berlin Heidelberg New York, pp 161–169

  • Leung J, Giraudat J (1998) Abscisic acid signal transduction. Annu Rev Plant Physiol Plant Mol Biol 49:199–222

    CAS  Google Scholar 

  • Lescot M, Dehais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouze P, Rombauts S (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res. 30:325–327

    Google Scholar 

  • Lisse T, Bartels D, Kalbitzer HR, Jaenicke R (1996) The recombinant dehydrin-like desiccation stress protein from the resurrection plant Craterostigma plantagineum displays no defined three-dimensional structure in its native state. Biol Chem 377:555–561

    CAS  PubMed  Google Scholar 

  • Michel D, Salamini F, Bartels D, Dale P, Baga M, Szalay A (1993) Analysis of a desiccation and ABA-responsive promoter isolated from de resurrection plant Craterostigma plantagineum. Plant J 4:29–40

    Article  CAS  PubMed  Google Scholar 

  • Michel D, Furini A, Salamini F, Bartels D (1994) Structure and regulation of an ABA- and desiccation-responsive gene from the resurrection plant Craterostigma plantagineum. Plant Mol Biol 24:549–560

    CAS  PubMed  Google Scholar 

  • Phillips JR, Hilbricht T, Salamini F, Bartels D (2002) A novel abscisic acid- and dehydration-responsive gene family from the resurrection plant Craterostigma plantagineum encodes a plastid-targeted protein with DNA-binding activity. Planta 215:258–266

    Article  CAS  PubMed  Google Scholar 

  • Piatkowski D, Schneider K, Salamini F, Bartels D (1990) Characterization of five abscisic acid-responsive cDNA clones isolated from the desiccation-tolerant plant Craterostigma plantagineum and their relationship to other water-stress genes. Plant Physiol 94:1682–1688

    CAS  Google Scholar 

  • Rinne PLH, Kaikuranta PLM, van der Plas LHW, van der Schoot C (1999) Dehydrins in cold-acclimated apices of birch (Betula pubescens Ehrh.): production, localization and potential role in rescuing enzyme function during dehydration. Planta 209:377–388

    Article  CAS  PubMed  Google Scholar 

  • Rock CD (2000) Pathways to abscisic acid-regulated gene expression. New Phytol 148:357–396

    Article  CAS  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY

    Google Scholar 

  • Schneider K, Wells B, Schmelzer E, Salamini F, Bartels D (1993) Desiccation leads to the rapid accumulation of both cytosolic and chloroplastic proteins in the resurrection plant Craterostigma plantagineum Hochst. Planta 189:120–131

    CAS  Google Scholar 

  • Smith-Espinoza CJ, Richter A, Salamini F, Bartels D (2003) Dissecting the response to dehydration and salt (NaCl) in the resurrection plant Craterostigma plantagineum. Plant Cell Environ 26:1307–1315

    Article  CAS  Google Scholar 

  • Sunkar R, Bartels D, Kirch HH (2003) Overexpression of a stress-inducible aldehyde dehydrogenase gene from Arabidopsis thaliana in transgenic plants improves stress tolerance. Plant J 35:452–464

    Article  CAS  PubMed  Google Scholar 

  • Twell D, Yamaguchi J, Wing RA, Ushiba J, McCormick S (1991) Promoter analysis of genes that are coordinately expressed during pollen development reveals pollen-specific enhancer sequences and shred regulatory elements. Genes Dev 5:496–507

    CAS  PubMed  Google Scholar 

  • Velasco R, Salamini F, Bartels D (1998) Gene structure and expression analysis of the drought-and abscisic acid-responsive cdet11-24 gene family from the resurrection plant Craterostigma plantagineum Hochst. Planta 204:459–471

    Article  CAS  PubMed  Google Scholar 

  • Xu D, Duan X, Wang B, Hong B, Ho T-HD, Wu R (1996) Expression of a late embryogenesis abundant protein gene, HVA1, from barley confers tolerance to water deficit and salt stress in transgenic rice. Plant Physiol 110:249–257

    CAS  Google Scholar 

  • Yin Y, Zhu Q, Dai S, lamb C, Beachy R (1997) RF2a, a bzip transcriptional activator of the phloem-specific rice tungro bacilliform virus promoter, functions in vascular development. EMBO J 16:5247–5259

    Google Scholar 

  • Yoshida K, Mohri T, Nishiguchi M, Tazaki K (2002) Robinia pseudoacacia inner-bark lactin promoter expresses GUS also predominantly in phloem of transgenic tobacco. J Plant Physiol 159:757–764

    CAS  Google Scholar 

  • Zhang L, Ohta A, Takagi M, Imai R (2000) Expression of plant group 2 and group 3 lea genes in Saccharomyces cerevisiae revealed functional divergence among LEA proteins. J Biochem 127:611–616

    CAS  PubMed  Google Scholar 

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Acknowledgments

We thank F. Salamini for advice during the work and critically reading the manuscript, B. Eilts for technical assistance, S. Berger for help with preparing the manuscript and C.J. Smith-Espinoza for performing the C. plantagineum salt treatments. M.-J.R. was supported by a postdoctoral fellowship from the Spanish Ministry of Science and Technology and a research contract from the EU Biotech Programme (BIO-CT98-5006).

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Correspondence to Dorothea Bartels.

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This article is dedicated to Prof. Dr. Francesco Salamini on the occasion of his 65th birthday and his departure from the Max Planck Institute in Köln

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Rodrigo, M.J., Bockel, C., Blervacq, AS. et al. The novel gene CpEdi-9 from the resurrection plant C. plantagineum encodes a hydrophilic protein and is expressed in mature seeds as well as in response to dehydration in leaf phloem tissues. Planta 219, 579–589 (2004). https://doi.org/10.1007/s00425-004-1264-z

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