Prof. Zach Adam

The  Proteolytic  Machinery of Chloroplasts

chloroplast_proteases
 

Proteolytic processes are involved in a wide range of functions throughout the life cycle of any cell.  Chloroplast proteases thus affect photosynthesis at several different levels. The development of proplastids and etioplasts into chloroplasts involves not only the synthesis of a new set of proteins, but also massive degradation of the previous population. Limited proteolytic processing, for removal of targeting sequences, is an essential step in the import and sorting of nuclear-encoded chloroplast proteins, and in the maturation of some chloroplast-encoded proteins. Proteases participate in the biogenesis of some protein complexes, and in the recycling of proteins into free amino acids during senescence. Perhaps the most explored aspect of protein degradation in chloroplasts is its role in the response to changing environmental conditions. Increasing light intensities lead to photodamage, the repair of which requires accelerated removal of damaged proteins. Similarly, heat-denatured proteins that fail to refold properly are degraded.

Starting our lab in the 90’s, we have combined biochemical, molecular and genetic approaches, to identify and characterize the biochemical and physiological roles of a number of chloroplast proteases in all compartments of the organelle, with special emphasis on the thylakoid FtsH and Deg families, unraveling their role in the biogenesis and maintenance of the photosynthetic apparatus.

 

 

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Selected Publications

  •   Lindahl M., Tabak S., Cseke L, Pichersky E, Andersson B. & Adam Z. (1996). Identification, characterization, and molecular cloning of a homologue of the bacterial FtsH protease in chloroplasts of higher plants. J. Biol. Chem. 271: 29329-29334.

  • Adam Z. (1996). Protein stability and degradation in chloroplasts - a mini-review. Plant Mol. Biol. 32: 773-783.

  • Ostersetzer O. & Adam Z. (1997). Light-stimulated degradation of an unassembled Rieske FeS protein by a thylakoid-bound protease: the possible role of the FtsH protease. Plant Cell 9: 957-965.

  • Itzhaki H., Naveh L., Lindahl M., Cook M. & Adam Z. (1998). Identification and characterization of DegP, a serine protease associated with the lumenal side of the thylakoid membrane. J. Biol. Chem. 273: 7094-7098.

  • Lindahl M., Spetea C., Hundal T., Oppenheim A., Adam Z. & Andersson B. (2000). The Thylakoid FtsH protease plays a role in the light-induced turnover of the photosystem II D1 protein. Plant Cell 12: 419-431.

  • Adam Z., Adamska I., Nakabayashi K., Ostersetzer O., Haussuhl K., Manuell A., Zheng B., Vallon O., Rodermel S.R., Shinozaki K. & Clarke A.K. (2001). Chloroplast and Mitochondrial Proteases in Arabidopsis thaliana: A Proposed Nomenclature. Plant Physiol. 125:1912-1918.

  • Chassin Y., Kapri E., Sinvany G., Arad, T. & Adam Z. (2002). Expression and characterization of the thylakoid lumen protease DegP1 from Arabidopsis thaliana. Plant Physiol. 130: 857-864.

  • Adam Z. & Clarke A.K. (2002). Cutting edge of chloroplast proteolysis. Trends Plant Sci. 17: 451-456.

  • Sakamoto W., Zaltsman A., Adam Z. & Takahashi Y. (2003). Coordinated regulation and complex formation of YELLOW VARIEGATED1 and YELLOW VARIEGATED2, chloroplastic FtsH metalloproteases involved in the repair cycle of photosystem II in Arabidopsis thylakoid membranes. Plant Cell 15: 2843-2855.

  • Sinvany-Villalobo G., Davydov O., Ben-Ari G., Zaltsman A., Raskind A. & Adam Z. (2004). Expression in multi-gene families: Analysis of chloroplast and mitochondrial proteases. Plant Physiol. 135: 1336-1345.

  • Zaltsman A., Feder A. & Adam Z. (2005). Developmental and light effects on the accumulation of FtsH protease in Arabidopsis chloroplasts - implications for thylakoid formation and photosystem II maintenance. Plant J. 42: 609-617

  • Zaltsman A., Ori N. & Adam Z. (2005). Two types of FtsH protease subunits are required for chloroplast biogenesis and photosystem II repair in Arabidopsis. Plant Cell 17: 2782-2790.

  • Adam Z. , Rudella A. & van Wijk K. (2006). Recent advances in the study of Clp, FtsH and other proteases located in chloroplasts. Curr. Op. Plant Biol. 9: 234-240.

  • Kapri-Pardes E., Naveh L. & Adam Z. (2007). The thylakoid lumen protease Deg1 is involved in the repair of photosystem II from photoinhibition in Arabidospsis. Plant Cell 19: 1039-1047.

  • Kley J., Schmidt B., Boyanov B., Stolt-Bergner P.C., Kirk R., Ehrmann M., Knopf R.R., Naveh L., Adam Z. & Clausen T. (2011). Structural adaptation of the plant protease Deg1 to repair photosystem II during light exposure. Nature Struct. Mol. Biol. 18: 728-731

  • Adam Z., Frottin F., Espagne C., Meinnel T. & Giglione C. (2011). Interplay between N-terminal methionine excision and FtsH protease is essential for normal chloroplast development and function. Plant Cell 23: 3745-3760.

  • Charuvi D., Kiss V., Nevo R., Shimoni E., Adam Z. & Reich Z. (2012). Gain and loss of photosynthetic membranes during plastid differentiation in the shoot apex of Arabidopsis. Plant Cell 24: 1143-1157.

  • Moldavski O., Levin-Kravets O., Ziv T., Adam Z. & Prag G. (2012). The hetero-hexameric nature of a chloroplast AAA+ FtsH protease contributes to its thermodynamic stability. PLoS ONE 7 (4): e36008.

  • Rimon Knopf R., Feder A., Mayer K., Lin A., Rozenberg M., Schaller A., & Adam Z. (2012). Rhomboid proteins in the chloroplast envelope affect the level of allene oxide synthase in Arabidopsis thaliana. Plant J. 72: 559-571.

  • Adam Z. (2013). Emerging roles for diverse intramembrane proteases in plant biology. BBA-Biomembranes 1828: 2933-2936.

  • Adam Z. (2015). Plastid intramembrane proteolysis. Biochim. Biophys. Acta 1847:910-914.

  • Knopf R.R. & Adam Z. (2018). Lumenal exposed regions of the D1 protein of PSII are long enough to be degraded by the chloroplast Deg1 protease. Sci. Rep. 8:5230.

  • Butenko Y., Lin A., Naveh L., Kupervaser M., Levin Y., Reich Z. & Adam Z. (2018). Differential roles of the thylakoid lumenal Deg protease homologs in chloroplast proteostasis. Plant Physiol. 178: 1065-1080.

  • Tamary E., Nevo R., Naveh L., Levin-Zaidman S., Kiss V., Savidor A., Levin Y., Eyal Y., Reich Z. & Adam Z. (2019). Chlorophyll catabolism precedes changes in chloroplast structure and proteome during leaf senescence. Plant Direct 3: 1-18.

  • Adam Z., Aviv-Sharon E., Keren-Paz A., Naveh L., Rozenberg M., Savidor A. & Chen J. (2019). The chloroplast envelope protease FTSH11 - interaction with CPN60 and identification of potential substrates. Front. Plant Sci. 10: 428.

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Former Lab Members

  • Leah Naveh  Lab Technician
  • Laure Sultan  Postdoctoral Fellow (2022)
  • Tiru Malavath  Postdoctoral Fellow (2021)
  • Yana Butenko  Postdoc (2020)
  • Eyal Tamary, Ph.D. (2019)
  • Elinor Aviv, M.Sc. (2018)
  • Hadar Lecker, M.Sc (2017)
  • Vijay Dalal, Postdoc (2017)
  • Albina Lin, M.Sc. (2012)
  • Ronit Rimon-Knopf, Ph.D. (2012)
  • Dana Charuvi, Ph.D. (2011)
  • Alona Keren-Paz, Postdoc (2010)
  • Mazal Ish-Shalom, Ph.D. (2009)
  • Ofer Moldavski, M.Sc. (2009)
  • Michal Eldar, M.Sc. (2009)
  • Yifat Lascar, M.Sc. (2009)
  • Einat Kapri Pardes, Ph.D. (2007)
  • Yonatan Gross, M.Sc (2007)
  • Ari Feder, M.Sc. (2007) 
  • Mery Dafni-Yelin, Ph.D. (2006)
  • Galit Sinvany Villalobo, Ph.D. (2006)
  • Adi Zaltsman, Ph.D. (2005) 
  • Ora Podlyas, M.Sc. (2005) 
  • Alexander Raskin, Postdoc (2004)
  • Yael Chasin, M.Sc. (2002)
  • Tal Arad, M.Sc. (2002)
  • Ifat Matityahu, M.Sc. (2002)
  • Maggie Levy, M.Sc. (1995) , Ph.D. (2001)
  • Oren Ostersetzer-Biran, M.Sc. (1995), Ph.D (2001)
  • Marika Lindahl, Postdoc (2001)
  • Tamar Halperin, Ph.D. (2000)
  • Hanan Itzhaki, Postdoc (1998)
  • Sarit Tabak, M.Sc. (1997)
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