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

in Israel Journal of Plant Sciences
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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.

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References
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

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

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

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

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

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • Granot G. Grafi G. (2014). Epigenetic information can reveal phylogenetic relationships within Zygophyllales. Plant Syst. Evol. 300: 18191824.

    • Search Google Scholar
    • Export Citation
  • 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.

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

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

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

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

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

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
Figures
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    Phenology of Zygophyllum dumosum Boiss on a southeast-facing slope at Sede Boqer research area (30o 51’ N 34o 46’ E; elevation 498 m). A. A typical Zygophyllum plant during the wet season (March 2008). B. A Zygophyllum branch with new compound leaves each composed of two leaflets (L) carried on a thick, fleshy new petiole (NP). 1-YOP, 1-year-old petiole. C. A typical Z. dumosum branch during the dry season carrying petioles (P). D. A dual appearance of Z. dumosum plant showing healthy branches carrying new leaves and flowers (below the broken line) and unhealthy branches (above the broken line). E. A Z. dumosum plant with the main trunk divided into several distinct units. F. A cross section in petiole collected during the summer highlighting the bilayer epidermis (blep) and sunken stomata (st). G-I. Epidermis morphology during the wet and the dry season. Cross sections of petioles collected on March (G), July (H) and October (I) demonstrating the occurrence of bilayer epidermis on entry into the summer. cut, cuticle; ep, epidermis; st, stomata; blep, bilayer epidermis.

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    Daily temperature (years 2009–2012) is highly fluctuated during the winter month (March). Note that during the summer month of August, the temperature is high and stable and not fluctuating as during the rainy month of March (data obtained from the Israel Metorological database https://ims.data.gov.il/).

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    Distribution of rainfall in Sede Boqer area during the indicated winters of 2008–2012. Blue dotted line indicates the 2 mm rainfall. Note that most rainfall events during the winters are below 2 mm. Rich, well distributed rainfall events (>4 mm, green dotted line) are characteristic of the winter of 2009–2010. A special rainfall event (62 mm) during January 2010 is indicated. The yearly precipitation (mm) is given in brackets.

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