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Zach Adam Zach Adam

Phone No: +972-8-948-9921

Fax: +972-8-948-9329

E-mail: zach.adam@mail.huji.ac.il






Research Interest

The proteolytic machinery of chloroplasts

Proteolysis in Chloroplasts

Proteolytic processes are involved in a wide range of functions throughout the life cycle of any cell. Chloroplast proteases are thus expected to 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. Gene expression within the chloroplast may require degradation of positive and negative regulators. Limited proteolytic processing is an essential step in the import and sorting of nuclear-encoded chloroplast proteins, and in the maturation of some chloroplast-encoded proteins. Proteases are likely to participate in the biogenesis of some protein complexes. 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. Using biochemical, molecular and genetic approaches, we have identified and characterized a number of chloroplast proteases in all major compartments of the organelle. In our current research we focus mainly on proteases of the FtsH and Deg families, and study their role in the biogenesis and maintenance of the photosynthetic apparatus.

Phenotypes of FtsH protease mutants

3D structure of Deg1 protease


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Selected Publications

  • Adam Z. (1995). A mutation in the small subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase that reduces the rate of its incorporation into holoenzyme. Photosynthesis Res. 43: 143-147. [Abstract]
  • Levy M. & Adam Z. (1995). Mutations in the processing site of the precursor of ribulose-1,5-bisphosphate carboxylase / oxygenase small subunit: effects on import, processing, assembly and stability. Plant Mol. Biol. 29: 53-61. [Abstract]
  • Halperin T. & Adam Z. (1996). Degradation of mistargeted OEE33 in the chloroplast stroma. Plant Mol. Biol. 30: 925-933. [Abstract]
  • Ostersetzer O., Tabak S., Yarden O., Shapira R. & Adam Z. (1996). Immunological detection of proteins similar to bacterial proteases in higher plant chloroplasts. Eur. J. Biochem. 236: 932-936. [Abstract]
  • Ostersetzer O. & Adam Z. (1996). Effects of light and temperature on expression of ClpC, the regulatory subunit of chloroplastic Clp protease, in pea seedlings. Plant Mol. Biol. 31: 673-676. [Abstract]
  • 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. [Abstract] [Full Text]
  • Adam Z. (1996). Protein stability and degradation in chloroplasts - a mini-review. Plant Mol. Biol. 32: 773-783.
  • Cook M. & Adam Z. (1997). Purification and characterization of an arginyl peptidase from the chloroplast stroma of pea seedlings. Plant Physiol. Biochem. 35: 163-168. [Abstract]
  • 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. [Abstract]
  • 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. [Abstract] [Full Text]
  • Ostersetzer O. & Adam Z. (1999). Construction of a vector for coupled in vitro transcription/translation. BioTechniques 27: 428-434.
  • Lindhal 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. [Abstract] [Full Text]
  • Adam Z. (2000). Chloroplast proteases: Possible regulators of gene expression? Biochimie 82: 647-654. [Abstract]
  • Halperin T., Zheng B., Itzhaki H., Clarke A.K. & Adam Z. (2001). Plant mitochondria contain proteolytic and regulatory subunits of the ATP-dependent Clp protease. Plant Mol. Biol. 45:461-468. [Abstract] [Full Text (PDF)]
  • 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. [Abstract] [Full Text (PDF)] [Table IV (revised)(DOC)]
  • Halperin T., Ostersetzer O. & Adam Z. (2001). ATP-dependent association between subunits of Clp protease in pea chloroplasts. Planta 213: 614-619. [Abstract] [Full Text (PDF)]
  • Zheng B., Halperin T., Hruskova-Heidingsfeldova O., Adam Z. & Clarke A.K. (2002). Characterization of chloroplast Clp proteins in Arabidopsis: localization, tissue specificity and stress responses. Physiol. Plant. 114: 92-101. [Full Text (PDF)]
  • 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 [Full Text (PDF)]
  • 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.
  • Levy M. & Adam Z. (2004). A single recessive mutation in the proteolytic machinery of Arabidopsis chloroplasts impairs photoprotection and photosynthesis upon cold stress. Planta 218: 396-405.
  • 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.
  • Ostersetzer O., Kato, Y., Adam, Z. & Sakamoto, W. (2007). Multiple intracellular locations of lon protease in arabidopsis: evidence for the localization of AtLon4 to chloroplasts. Plant Cell Physiol. 48: 881-885.
  • Shen G., Adam Z., & Zhang H. (2007). The E3 ligase AtCHIP ubiquitylates FtsH1, a component of the chloroplast FtsH protease, and affects protein degradation in chloroplasts. Plant J. 52: 309-321.
  • Adam Z. (2007). Protein stability and degradation in plastids. In: Trends Curr. Genet., vol. 19, Cell and Molecular Biology of Plastids, pp 315-338 .
  • Dafny-Yelin M., Tzfira T., Vainstein A. & Adam Z. (2008). Non-redundant functions of sHSP-CIs in acquired thermotolerance and their role in early seed development in Arabidopsis. Plant Mol. Biol. 67: 363-373.
  • Sun X., Ouyang M., Guo J., Ma J., Lu C., Adam Z. & Zhang L. (2010). The thylakoid protease Deg1 is involved in photosystem II assembly in Arabidopsis thaliana. Plant J. 62: 240-249.
  • Adam Z., Charuvi D., Tsabari O., Rimon Knopf R. & Reich Z. (2011). Biogenesis of thylakoid networks in angiosperms: knowns and unknowns. Plant Mol. Biol. DOI: 76: 221-234.
  • Bienvenut W.V., Espagne C., Martinez A., Majeran W., Valot B., Zivy M., Vallon O., Adam Z., Meinnel T. & Giglione C. (2011). Dynamics of post-translational modifications and protein stability in the stroma of Chlamydomonas reinhardtii chloroplasts. Proteomics 11: 1734-1750.
  • 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.
  • Rimon Knopf R. & Adam Z. (2012). Rhomboid proteases in plants - still in square one? Physiol. Plant. 145:41-51.
  • 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 doi: 10.1111/j.1365-313X.2012.05090.x.
  • Adam Z. (2013). Emerging roles for diverse intramembrane proteases in plant biology. BBA-Biomembranes 1828: 2933-2936.
  • Adam Z. and Sakamoto W. (2014). Plastid Proteases. In: Plastid Biology, Advances in Plant Biology 5 (Eds., S.M. Theg, F.-A. Wollman). Springer, New York, pp. 359-389. (invited chapter).
  • Charuvi D., Nevo R., Shimoni E., Naveh L., Zia A., Adam Z., Farrant J.M., Kirchhoff H., & Reich, Z. (2015). Photoprotection conferred by changes in photosynthetic protein levels and organization during dehydration of a homoiochlorophyllous resurrection plant. Plant Physiol. 167: 1554-1565.
  • Adam Z. (2015). Plastid intramembrane proteolysis. Biochim. Biophys. Acta 1847:910-914. (invited review).
  • Ouyang M., Li X., Zhao S., Pu H., Shen J., Adam Z., Clausen T. & Zhang L.(2017). The crystal structure of Deg9 reveals a novel octameric-type HtrA protease. Nature Plants 3: 973-982.
  • 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.
  • Dalal V., Dagan S., Friedlander G., Aviv E., Bock R., Charuvi D., Reich Z. & Adam Z. (2018). Transcriptome analysis highlights nuclear control of chloroplast development in the shoot apex. Sci. Rep. 8:8881.
  • Swid N., Nevo R., Kiss V., Kapon R., Dagan S., Snir O., Adam Z., Falconet D., Reich Z. & Charuvi D. (2018). Differential impacts of FtsZ proteins on plastid division in the shoot apex of Arabidopsis. Dev. Biol. 441: 83-94.
  • 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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Current Members of the Group

Leah Naveh
Lab Technician

Yana Butenko

Eyal Tamary

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Former Lab Members

  • Elinor Aviv, M.Sc. (2018)
  • Eyal Tamary, Ph.D. (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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