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Taxonomically restricted genes of Craterostigma plantagineum are modulated in their expression during dehydration and rehydration

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Abstract

Main conclusion

Taxonomically restricted genes are known to contribute to the evolution of new traits. In Craterostigma plantagineum two of such genes are modulated during dehydration and rehydration and seem to contribute to a successful recovery after desiccation.

Abstract

The resurrection plant Craterostigma plantagineum can tolerate extreme water loss. Protective molecules linked to desiccation tolerance were identified in C. plantagineum but underlying mechanisms are far from being completely understood. A transcriptome analysis revealed several genes which could not be annotated and are, therefore, interesting candidates for understanding desiccation tolerance. Genes which occur only in some species are defined as orphan or taxonomically restricted genes (TRGs) and may be important for the evolution of new traits. Several of these TRGs are modulated in expression during dehydration/rehydration in C. plantagineum. Here we report the characterisation of two of these TRGs encoding a cysteine-rich rehydration-responsive protein 1 (CpCRP1) and an early dehydration-responsive protein 1 (CpEDR1). The involvement of CpCRP1 and CpEDR1 in different phases of the dehydration/rehydration cycle is shown by transcript and protein expression analysis. In silico sequence analyses predicted that both genes are likely to interact with other cellular components and are localised in two different cellular compartments. GFP fusion proteins demonstrated that CpCRP1 is secreted into the apoplasm, whereas CpEDR1 is imported into chloroplasts. Putative homologs of CpCRP1 and CpEDR1 were identified in Lindernia brevidens and Lindernia subracemosa which belong to the same family as C. plantagineum thus suggesting a recent evolution of the genes in this family. According to expression profiles, CpCRP1 may play a role in normal conditions and during rehydration, whereas CpEDR1 may be required for the acquisition of desiccation tolerance and protect photosynthetic structures during dehydration and rehydration.

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References

  • 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(4):1346–1353

    Article  CAS  PubMed Central  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(1):27–34

    Article  CAS  PubMed  Google Scholar 

  • Bartels D, Hanke C, Schneider K, Michel D, Salamini F (1992) A desiccation-related Elip-like gene from the resurrection plant Craterostigma plantagineum is regulated by light and ABA. EMBO J 11(8):2771–2778

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bartels D, Ditzer A, Furini A (2006) What can we learn from resurrection plants? In: Ribaut J (ed) Drought adaptation in cereals. Hayworth Publisher, Binghamton, pp 599–622

    Google Scholar 

  • Benson DA, Karsch-Mizrachi I, Clark K, Lipman DJ, Ostell J, Sayers EW (2012) GenBank. Nucleic Acids Res 40(D1):D48–D53

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bernacchia G, Salamini F, Bartels D (1996) Molecular characterization of the rehydration process in the resurrection plant Craterostigma plantagineum. Plant Physiol 111(4):1043–1050

    CAS  PubMed Central  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(2–3):158–166

    Article  CAS  Google Scholar 

  • Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden T (2009) BLAST+: architecture and applications. BMC Bioinformatics 10(1):421

    Article  PubMed Central  PubMed  Google Scholar 

  • de Castro E, Sigrist CJ, Gattiker A, Bulliard V, Langendijk-Genevaux PS, Gasteiger E, Bairoch A, Hulo N (2006) ScanProsite: detection of PROSITE signature matches and ProRule-associated functional and structural residues in proteins. Nucleic Acids Res 34:W362–W365

    Article  PubMed Central  PubMed  Google Scholar 

  • Denecke J, Botterman J, Deblaere R (1990) Protein secretion in plant cells can occur via a default pathway. Plant Cell 2(1):51–59

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Dinakar C, Bartels D (2012) Light response, oxidative stress management and nucleic acid stability in closely related Linderniaceae species differing in desiccation tolerance. Planta 236(2):541–555

    Article  CAS  PubMed  Google Scholar 

  • Dinakar C, Bartels D (2013) Desiccation tolerance in resurrection plants: new insights from transcriptome, proteome and metabolome analysis. Front Plant Sci 4:482

    Article  PubMed Central  PubMed  Google Scholar 

  • Domingo C, Gomez MD, Canas L, Hernandez-Yago J, Conejero V, Vera P (1994) A novel extracellular matrix protein from tomato associated with lignified secondary cell walls. Plant Cell 6(8):1035–1047

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Domingo C, Saurí A, Mansilla E, Conejero V, Vera P (1999) Identification of a novel peptide motif that mediates cross-linking of proteins to cell walls. Plant J 20(5):563–570

    Article  CAS  PubMed  Google Scholar 

  • Drin G, Antonny B (2010) Amphipathic helices and membrane curvature. FEBS Lett 584(9):1840–1847

    Article  CAS  PubMed  Google Scholar 

  • Emanuelsson O, Nielsen H, Heijne GV (1999) ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites. Protein Sci 8(5):978–984

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Farrant JM (2000) A comparison of mechanisms of desiccation tolerance among three angiosperm resurrection plant species. Plant Ecol 151(1):29–39

    Article  Google Scholar 

  • Farrant JM, Vander Willigen C, Loffell DA, Bartsch S, Whittaker A (2003) An investigation into the role of light during desiccation of three angiosperm resurrection plants. Plant, Cell Environ 26(8):1275–1286

    Article  CAS  Google Scholar 

  • Farrant JM, Brandt W, Lindsey GG (2007) An overview of mechanisms of desiccation tolerance in selected angiosperm resurrection plants. Plant Stress 1(1):72–84

    Google Scholar 

  • Feiz L, Irshad M, Pont-Lezica RF, Canut H, Jamet E (2006) Evaluation of cell wall preparations for proteomics: a new procedure for purifying cell walls from Arabidopsis hypocotyls. Plant Methods 2(1):10

    Article  PubMed Central  PubMed  Google Scholar 

  • Furini A, Koncz C, Salamini F, Bartels D (1997) High level transcription of a member of a repeated gene family confers dehydration tolerance to callus tissue of Craterostigma plantagineum. EMBO J 16(12):3599–3608

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gaff DF (1989) Responses of desiccation-tolerant “resurrection” plants to water stress. In: Kreeb KH, Richter H, Hinckley TM (eds) Structural and functional responses to environmental stresses: water shortages. SPB Academic, The Hague, pp 264–311

    Google Scholar 

  • Gautier R, Douguet D, Antonny B, Drin G (2008) HELIQUEST: a web server to screen sequences with specific α-helical properties. Bioinformatics 24(18):2101–2102

    Article  CAS  PubMed  Google Scholar 

  • Gechev T, Benina M, Obata T, Tohge T, Sujeeth N, Minkov I, Hille J, Temanni M-R, Marriott A, Bergström E, Thomas-Oates J, Antonio C, Mueller-Roeber B, Schippers J, Fernie A, Toneva V (2013) Molecular mechanisms of desiccation tolerance in the resurrection glacial relic Haberlea rhodopensis. Cell Mol Life Sci 70(40):689–709

  • Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD, Fazo J, Mitros T, Dirks W, Hellsten U, Putnam N, Rokhsar DS (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 40(D1):D1178–D1186

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Höfler K, Migsch H, Rottenburg W (1941) Über die Austrocknungresistenz landwirtschaftlicher Kulturpflanzen. Forschungsdienst 12:50–61

    Google Scholar 

  • Horton P, Park KJ, Obayashi T, Fujita N, Harada H, Adams-Collier CJ, Nakai K (2007) WoLF PSORT: protein localization predictor. Nucleic Acids Res 35:W585–W587

    Article  PubMed Central  PubMed  Google Scholar 

  • Ingram J, Bartels D (1996) The molecular basis of dehydration tolerance in plants. Annu Rev Plant Biol 47(1):377–403

    Article  CAS  Google Scholar 

  • Khalturin K, Hemmrich G, Fraune S, Augustin R, Bosch TCG (2009) More than just orphans: are taxonomically-restricted genes important in evolution? Trends Genet 25(9):404–413

    Article  CAS  PubMed  Google Scholar 

  • Kirch H-H, Röhrig H (2010) Affinity purification and determination of enzymatic activity of recombinantly expressed aldehyde dehydrogenases. In: Sunkar R (ed) Plant stress tolerance, vol 639., Methods in molecular biologyHumana Press, New York, pp 281–290

    Chapter  Google Scholar 

  • Laemmli UKU (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227(5259):680–685

    Article  CAS  PubMed  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23(21):2947–2948

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Lupas A (1996) Coiled coils: new structures and new functions. Trends Biochem Sci 21(10):375–382

    Article  CAS  PubMed  Google Scholar 

  • Lupas A, Van Dyke M, Stock J (1991) Predicting coiled coils from protein sequences. Science 252(5009):1162–1164

    Article  CAS  PubMed  Google Scholar 

  • Moore JP, Le NT, Brandt WF, Driouich A, Farrant JM (2009) Towards a systems-based understanding of plant desiccation tolerance. Trends Plant Sci 14(2):110–117

    Article  CAS  PubMed  Google Scholar 

  • Moore JP, Nguema-Ona EE, Vicré-Gibouin M, Sørensen I, Willats WG, Driouich A, Farrant JM (2013) Arabinose-rich polymers as an evolutionary strategy to plasticize resurrection plant cell walls against desiccation. Planta 237(3):739–754

    Article  CAS  PubMed  Google Scholar 

  • Ohno S (1970) Evolution by gene duplication. Springer-Verlag, Heidelberg and New York

    Book  Google Scholar 

  • Oliver MJ, O’Mahony P, Wood AJ (1998) “To dryness and beyond”: preparation for the dried state and rehydration in vegetative desiccation-tolerant plants. Plant Growth Regul 24(3):193–201

    Article  CAS  Google Scholar 

  • Oliver M, Tuba Z, Mishler B (2000) The evolution of vegetative desiccation tolerance in land plants. Plant Ecol 151(1):85–100

    Article  Google Scholar 

  • Petersen J, Eriksson SK, Harryson P, Pierog S, Colby T, Bartels D, Röhrig H (2012) The lysine-rich motif of intrinsically disordered stress protein CDeT11-24 from Craterostigma plantagineum is responsible for phosphatidic acid binding and protection of enzymes from damaging effects caused by desiccation. J Exp Bot 63(13):4919–4929

    Article  CAS  PubMed Central  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(2):258–266

    Article  CAS  PubMed  Google Scholar 

  • Proost S, Van Bel M, Sterck L, Billiau K, Van Parys T, Van de Peer Y, Vandepoele K (2009) PLAZA: a comparative genomics resource to study gene and genome evolution in plants. Plant Cell 21(12):3718–3731

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Prud’homme B, Gompel N, Carroll SB (2007) Emerging principles of regulatory evolution. Proc Natl Acad Sci USA 104(suppl 1):8605–8612

    Article  PubMed Central  PubMed  Google Scholar 

  • Rodrigo MJ, Bockel C, Blervacq AS, Bartels D (2004) 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(4):579–589

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez MC, Edsgärd D, Hussain SS, Alquezar D, Rasmussen M, Gilbert T, Nielsen BH, Bartels D, Mundy J (2010) Transcriptomes of the desiccation-tolerant resurrection plant Craterostigma plantagineum. Plant J 63(2):212–228

    Article  CAS  PubMed  Google Scholar 

  • Röhrig H, Schmidt J, Colby T, Bräutigam A, Hufnagel P, Bartels D (2006) Desiccation of the resurrection plant Craterostigma plantagineum induces dynamic changes in protein phosphorylation. Plant, Cell Environ 29(8):1606–1617

    Article  Google Scholar 

  • Roy A, Kucukural A, Zhang Y (2010) I-TASSER: a unified platform for automated protein structure and function prediction. Nat Protoc 5(4):725–738

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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

    Google Scholar 

  • Scheibe R, Beck E (2011) Drought, desiccation, and oxidative stress. In: Lüttge U, Beck E, Bartels D (eds) Plant desiccation tolerance, vol 215., Ecological studiesSpringer, Berlin Heidelberg, pp 209–231

    Chapter  Google Scholar 

  • Schmidt J, John M, Wieneke U, Krüssmann H-D, Schell J (1986) Expression of the nodulation gene nodA in Rhizobium meliloti and localization of the gene product in the cytosol. Proc Natl Acad Sci USA 83(24):9581–9585

    Article  CAS  PubMed Central  PubMed  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(1):120–131

    Article  CAS  Google Scholar 

  • Sherwin H, Farrant J (1998) Protection mechanisms against excess light in the resurrection plants Craterostigma wilmsii and Xerophyta viscosa. Plant Growth Regul 24(3):203–210

    Article  CAS  Google Scholar 

  • Towbin H, Staehelin T, Gordon J (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 76(9):4350–4354

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Valenzuela-Avendaño JP, Mota IAE, Uc GL, Perera RS, Valenzuela-Soto EM, Aguilar JJZ (2005) Use of a simple method to isolate intact RNA from partially hydrated Selaginella lepidophylla plants. Plant Mol Biol Rep 23(2):199–200

    Article  Google Scholar 

  • van den Dries N, Facchinelli F, Giarola V, Phillips JR, Bartels D (2011) Comparative analysis of LEA-like 11-24 gene expression and regulation in related plant species within the Linderniaceae that differ in desiccation tolerance. New Phytol 190(1):75–88

    Article  PubMed  Google Scholar 

  • Wang WX, Pelah D, Alergand T, Shoseyov O, Altman A (2002) Characterization of SP1, a stress-responsive, boiling-soluble, homo-oligomeric protein from aspen. Plant Physiol 130(2):865–875

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wang W, Scali M, Vignani R, Spadafora A, Sensi E, Mazzuca S, Cresti M (2003) Protein extraction for two-dimensional electrophoresis from olive leaf, a plant tissue containing high levels of interfering compounds. Electrophoresis 24(14):2369–2375

    Article  CAS  PubMed  Google Scholar 

  • Willige BC, Kutzer M, Tebartz F, Bartels D (2009) Subcellular localization and enzymatic properties of differentially expressed transketolase genes isolated from the desiccation tolerant resurrection plant Craterostigma plantagineum. Planta 229(3):659–666

    Article  CAS  PubMed  Google Scholar 

  • Willigen CV, Pammenter NW, Jaffer MA, Mundree SG, Farrant JM (2003) An ultrastructural study using anhydrous fixation of Eragrostis nindensis, a resurrection grass with both desiccation-tolerant and -sensitive tissues. Funct Plant Biol 30(3):281

    Article  Google Scholar 

  • Wilson GA, Bertrand N, Patel Y, Hughes JB, Feil EJ, Field D (2005) Orphans as taxonomically restricted and ecologically important genes. Microbiology 151(8):2499–2501

    Article  CAS  PubMed  Google Scholar 

  • Xue B, Dunbrack RL, Williams RW, Dunker AK, Uversky VN (2010) PONDR-FIT: a meta-predictor of intrinsically disordered amino acids. Biochim Biophys Acta 1804(4):996–1010

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

We thank C. Buchholz for providing plant material, N. Jung and H. Bertram for help with some PCR experiments, A. Sergeeva for the immunoblot analysis of cell wall proteins and B. Buchen for critically reading the manuscript. Part of the work was supported by the Deutsche Forschungsgemeinschaft grant BA 712/9-2.

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The authors declare that they have no conflict of interest.

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Author notes

  1. Stephanie Krey

    Present address: Botanical Institute, Cologne Biocenter, University of Cologne, Zülpicherstraße 47b, 50674, Cologne, Germany

  2. Anneke Frerichs

    Present address: Institute of Developmental Biology, Cologne Biocenter, University of Cologne, Zülpicherstraße 47b, 50674, Cologne, Germany

Authors and Affiliations

  1. Institute of Molecular Physiology and Biotechnology of Plants (IMBIO), University of Bonn, Kirschallee 1, 53115, Bonn, Germany

    Valentino Giarola & Dorothea Bartels

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  1. Valentino Giarola
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Giarola, V., Krey, S., Frerichs, A. et al. Taxonomically restricted genes of Craterostigma plantagineum are modulated in their expression during dehydration and rehydration. Planta 241, 193–208 (2015). https://doi.org/10.1007/s00425-014-2175-2

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