A “mille-feuilles” of stress tolerance in the desert plant Zygophyllum dumosum Boiss.: Highlighting epigenetics

in Israel Journal of Plant Sciences

Plants thriving in harsh desert environments provide a suitable bio-system for unraveling novel mechanisms for survival under seasonal climate change and combination of temperature extremes, low water and nutrient availability and high salinity and radiation levels. The study of the desert plant Zygophyllum dumosum Boiss in its the natural habitat of the Negev desert revealed that stress tolerance is achieved by a plethora of mechanisms (e.g. morphological, molecular and developmental mechanisms), which are probably regulated by multiple genes that act together to bring about tolerance. Of particular interest is the finding that Z. dumosum like other Zygophyllaceae species, most of which inhabit dry and semidry regions of the world, do not possess the repressive epigenetic markers of histone H3 di- and tri-methylated at lysine 9; yet they possess mono methyl H3K9. We discuss the adaptive value of lessening epigenetic constraints with regard to the opportunistic behavior that makes plants most adaptable to change.

  • Arents G. Moudrianakis E.N. (1995). The histone fold: a ubiquitous architectural motif utilized in DNA compaction and protein dimerization. Proc. Natl. Acad. Sci. USA . 92: 1117011174.

    • Über Google Scholar suchen
    • Zitierung exportieren
  • Bailey H.P. (1979). Semi-arid climates: their definition and distribution. In: Hall A.E. Cannell G.H. and Lawton H.W. eds. Agriculture in Semiarid Environments. New York: Springer-Verlag pp. 7396.

    • Über Google Scholar suchen
    • Zitierung exportieren
  • Bartee L. Malagnac F. Bender J. (2001). Arabidopsis cmt3 chromomethylase mutations block non-CG methylation and silencing of an endogenous gene. Genes Dev. 15: 17531758.

  • Cao X. Jacobsen S.E. (2002). Role of the arabidopsis DRM methyltransferases in de novo DNA methylation and gene silencing. Curr. Biol. 12: 11381144.

  • Chen X. Hu Y. Zhou D.X. (2011). Epigenetic gene regulation by plant Jumonji group of histone demethylase. Biochim. Biophys. Acta. 1809: 421426.

  • Choi S.M. Song H.R. Han S.K. Han M. Kim C.Y. Park J. Lee Y.H. Jeon J.S. Noh Y.S. Noh B. (2012). HDA19 is required for the repression of salicylic acid biosynthesis and salicylic acid-mediated defense responses in Arabidopsis. Plant J. 71: 135146.

    • Über Google Scholar suchen
    • Zitierung exportieren
  • Danin A. (1983). Desert Vegetation of Israel and Sinai. Jerusalem: Cana Publishing House.

  • Dimitrova E. Turberfield A.H. Klose R.J. (2015). Histone demethylases in chromatin biology and beyond. EMBO Rep. 16: 16201639.

  • Dowen R.H. Pelizzola M. Schmitz R.J. Lister R. Dowen J.M. Nery J.R. Dixon J.E. Ecker J.R. (2012). Widespread dynamic DNA methylation in response to biotic stress. Proc. Natl. Acad. Sci. USA . 109: E218391.

    • Über Google Scholar suchen
    • Zitierung exportieren
  • Eberharter A. Becker P.B. (2002). Histone acetylation: a switch between repressive and permissive chromatin. Second in review series on chromatin dynamics. EMBO Rep . 3: 224229.

  • Eissenberg J.C. Shilatifard A. (2010). Histone H3 lysine 4 (H3K4) methylation in development and differentiation. Dev. Biol. 339: 240249.

  • Finnegan E.J. Kovac K.A. (2000). Plant DNA methyltransferases. Plant Mol. Biol . 43: 189201.

  • Granot G. Sikron-Persi N. Gaspan O. Florentin A. Talwara S. Paul L.K. Morgenstern Y. Granot Y. Grafi G. (2009). Histone modifications associated with drought tolerance in the desert plant Zygophyllum dumosum Boiss. Planta 231: 2734.

    • Über Google Scholar suchen
    • Zitierung exportieren
  • Granot G. Grafi G. (2014). Epigenetic information can reveal phylogenetic relationships within Zygophyllales. Plant Syst. Evol. 300: 18191824.

  • Hollósy F. (2002). Effects of ultraviolet radiation on plant cells. Micron. 33: 179197.

  • Hunter R.G. Gagnidze K. McEwen B.S. Pfaff D.W. (2015). Stress and the dynamic genome: steroids, epigenetics, and the transposome. Proc. Natl. Acad. Sci. USA . 112: 68286833.

  • Jeltsch A. (2002). Beyond Watson and Crick: DNA methylation and molecular enzymology of DNA methyltransferases. Chembiochem. 3: 274293.

  • Johnson L.M. Bostick M. Zhang X. Kraft E. Henderson I. Callis J. Jacobsen S.E. (2007). The SRA methyl-cytosine-binding domain links DNA and histone methylation. Curr. Biol. 17: 379384.

    • Über Google Scholar suchen
    • Zitierung exportieren
  • Khadka J. Yadav N.S. Granot G. Grafi G. (2018) Seasonal growth of Zygophyllum dumosum Boiss.: summer dormancy is associated with loss of the permissive epigenetic marker dimethyl H3K4 and extensive reduction in proteins involved in basic cell functions. Plants 7: pii: E59.

    • Über Google Scholar suchen
    • Zitierung exportieren
  • Lämke J. Bäurle I. (2017). Epigenetic and chromatin-based mechanisms in environmental stress adaptation and stress memory in plants. Genome Biol. 18: 124.

  • Laude H.M. (1953). The nature of summer dormancy in perennial grasses. Bot. Gaz. 114: 284292.

  • Lee K.K. Workman J.L. (2007). Histone acetyltransferase complexes: one size doesn’t fit all. Nat. Rev. Mol. Cell Biol. 8: 284295.

  • Li T. Chen X. Zhong X. Zhao Y. Liu X. Zhou S. Cheng S. Zhou D.X. (2013). Jumonji C domain protein JMJ705-mediated removal of histone H3 lysine 27 trimethylation is involved in defense-related gene activation in rice. Plant Cell 25: 47254736.

    • Über Google Scholar suchen
    • Zitierung exportieren
  • Lindroth A.M. Cao X. Jackson J.P. Zilberman D. McCallum C.M. Henikoff S. Jacobsen S.E. (2001). Requirement of CHROMOMETHYLASE3 for maintenance of CpXpG methylation. Science 292: 207720780.

    • Über Google Scholar suchen
    • Zitierung exportieren
  • Luger K. Mäder A.W. Richmond R.K. Sargent D.F. Richmond T.J. (1997). Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389: 251260.

  • March-Díaz R. García-Domínguez M. Lozano-Juste J. León J. Florencio F.J. Reyes J.C. (2008). Histone H2A.Z and homologues of components of the SWR1 complex are required to control immunity in Arabidopsis. Plant J . 53: 475487.

    • Über Google Scholar suchen
    • Zitierung exportieren
  • McClintock B. (1984) The significance of responses of the genome to challenge. Science 226: 792801.

  • Negi P. Rai A.N. Suprasanna P. (2016). Moving through the stressed genome: emerging regulatory roles for transposons in plant stress response. Front. Plant Sci. 7: 1448.

  • Noy-Meir I. (1973). Desert ecosystems: environment and producers. Annu. Rev. Ecol. Syst. 4: 2551.

  • Ofir M. Kerem D. (1982). The effects of temperature and photoperiod on the onset of summer-dormancy in Poa bulbosa L. Ann. Bot. 50: 259264.

  • Ofir M. Kigel J. (2007). Regulation of summer dormancy by water deficit and ABA in Poa bulbosa ecotypes. Ann. Bot. 99: 293299.

  • Petrie M.D. S.L. Collins M.E. Litvak (2015). The ecological role of small rainfall events in a desert grassland. Ecohydrol. 8: 16141622.

  • Sala O.E. Lauenroth W.K. (1982). Small rainfall events: an ecological role in semiarid regionsOecologia 53: 301304.

  • Shaimi N. Kallida R. Volaire F. Saidi N. Al Faiz C. (2009). Summer dormancy and drought survival of Moroccan ecotypes of orchardgrass. Crop Sci. 49: 14161424.

  • Soen Y. Knafo M. Elgart M. (2015). A principle of organization which facilitates broad Lamarckian-like adaptations by improvisation. Biol. Direct. 10: 68.

  • Takata H. Hanafusa T. Mori T. Shimura M. Iida Y. Ishikawa K. Yoshikawa K. Yoshikawa Y. Maeshima K. (2013). Chromatin compaction protects genomic DNA from radiation damage. PLoS One 8: e75622.

    • Über Google Scholar suchen
    • Zitierung exportieren
  • Terwilliger V.J. Zeroni M. (1994). Gas exchange of a desert shrub (Zygophyllum dumosum Boiss.) under different soil moisture regimes during summer drought. J. Plant Ecol . 115: 133144.

    • Über Google Scholar suchen
    • Zitierung exportieren
  • Thorstensen T. Grini P.E. Aalen R.B. (2011). SET domain proteins in plant development. Biochim. Biophys. Acta. 1809: 407420.

  • Tyrrell R.M. (1994). The molecular and cellular pathology of solar ultraviolet radiation. Mol. Aspects Med. 15: 177.

  • van Zanten M. Koini M.A. Geyer R. Liu Y. Brambilla V. Bartels D. Koornneef M. Fransz P. Soppe W.J. (2011). Seed maturation in Arabidopsis thaliana is characterized by nuclear size reduction and increased chromatin condensation. Proc. Natl. Acad. Sci. USA . 108: 2021920224.

    • Über Google Scholar suchen
    • Zitierung exportieren
  • Volaire F. Norton M. (2006). Summer dormancy in perennial temperate grasses. Ann. Bot. 98: 927933.

  • Waisel Y. Liphschitz N. Fahn A. (1970). Cambial activity in Zygophyllum dumosum Boiss. Ann. Bot. 34: 409414.

  • Wessler S.R. (1996) Plant retrotransposons: Turned on by stress. Curr. Biol. 6: 959961.

  • Zheng Y. Ding Y. Sun X. Xie S. Wang D. Liu X. Su L. Wei W. Pan L. Zhou D.X. (2016). Histone deacetylase HDA9 negatively regulates salt and drought stress responsiveness in Arabidopsis. J. Exp. Bot. 67: 17031713.

    • Über Google Scholar suchen
    • Zitierung exportieren

Kennzahlen

Insgesamt Im letzten Jahr In den letzten 30 Tagen
Aufrufe von Kurzbeschreibungen 112 112 10
Gesamttextansichten 9 9 1
PDF-Downloads 10 10 3