Dr. Marvin Edelman, The Sir Siegmund Warburg Chair of Agricultural Molecular Biology, Department of Plant Sciences, Weizmann Institute of Science, and Dr. Autar Mattoo, Research Leader; Vegetable Laboratory, Plant Sciences Institute; Henry A. Wallace Beltsville Agricultural Research Center; ARS; USDA, have worked as a synergistic team for the past two decades, discovering and unraveling the regulatory steps and mechanisms involved in the cycling of the PSII reaction center proteins, including the metabolism, intra-membrane mobility and reversible acylation and phosphorylation of the D1 protein.

A novel concept of regulation of protein degradation by light and herbicides. Drs. Edelman and Mattoo along with their collaborators uncovered the rapid, in vivo turnover of a major, photoinduced, chloroplast synthesis product, the 32-kDa thylakoid membrane protein, now known as the D1 protein. They determined that D1 is a key component of the photosynthetic electron transport chain acting at the reducing side of photosystem II. They showed that degradation of D1 in vivo is inhibited by diuron (DCMU) concomitant with the demonstration by C.J. Arntzen and collaborators of binding of atrazine to D1. These early, parallel studies established the rapidly-metabolized D1 protein as the in vivo target of photosystem II herbicides. The Edelman/Mattoo team demonstrated the phylogenetic conservation of the D1 protein in oxygenic photosyntates at several levels, including rapid synthesis, precursor maturation, membrane orientation and primary structure. They delineated the structural/functional architecture of the protein, including post-translational carboxy-terminal processing, a first in plants, and the in vivo catabolic site for the initial scission of the protein in the heart of the quinone B/herbicide binding region. This highly-quoted latter finding was seminal and laid the foundation for photosynthesis researchers throughout the world to incorporate degradation of D1 in their research to understand herbicide action in plants and how integral membrane proteins are degraded. Mattoo and collaborators applied these fundamental discoveries to develop a thermostable biosensor to enable rapid detection of environmentally unsafe photosystem II herbicide residues in soil and water. This biosensor is ultra-sensitive - its detection limits similar to the more complex, highly sensitive ELISA test, which is antibody-based. It has been patented with collaborators in Italy.

Intra-membrane mobility of the D1 protein, and protein acylation as a possible translocating signal. The Mattoo/Edelman teams elucidated the detailed metabolic life history of the D1 reaction center protein in vivo: that as a 33.5-kDa precursor it appears first in the unstacked stromal membranes, that following carboxy-terminal processing it is reversibly palmitoylated and translocated within the thylakoids to the topologically-distinct, stacked grana, that at this functional site it undergoes posttranslational, circadian-rhythmic phosphorylation and initial catabolic scission at the quinone B site. The novel demonstrations of intra-membrane mobility of proteins, and protein acylation as a possible translocating signal are the first of their kind in plant biology.

The photoreceptors for D1 degradation: physiological levels of UV-B radiation target the reaction center proteins of photosystem II. The Edelman/Mattoo teams demonstrated the involvement of two separate photoreceptors in D1 protein degradation: bulk photosynthetic pigments (chlorophyll) in the visible and far-red regions, and plastosemiquinone in the UV-B spectral region. Their research was the first to identify a protein target for UV-B damage in vivo. Activating both photoreceptors simultaneously, above a certain threshold of UV-B radiation, they demonstrated that both the D1 and D2 reaction center proteins degraded rapidly in vivo. They then went on to show that different cultivars of plants required different thresholds of UV-B radiation to activate rapid degradation of the photosystem II reaction center core. before These results have direct bearing on a plantıs adaptation to several environmental stresses, particularly in the areas of water deficiency, global climate change, and UV-B damage. The research of Drs. Edelman and Mattoo has advanced our knowledge about environmental stress damage of plants. Immediate application lies in selecting crop plants for UV-B resistant germplasm and/or engineering plants with built-in defense mechanisms. The identification of a novel UV-B radiation target has greater implications in view of the current depletion of stratospheric ozone and concomitant increase in the ambient levels of solar UV-B.

Light dependent reversible phosphorylation of the D1 protein. The Mattoo/Edelman teams discovered a novel in vivo-generated electrophoretic variant of D1, designated 32*, in higher plants which they showed was the phosphorylated form of the D1 protein. They demonstrated that phosphorylated D1 is generated solely in active, grana-localized reaction centers, that its formation is light dependent, its appearance correlates with the onset of D1 degradation and it is inhibited by DCMU under conditions that inhibit light-dependent degradation of D1. They also discovered that light was a mediator in dephosphorylation of photosystem II proteins, a novel finding. As to the D1 protein, they showed that photosystem I-excitation regulates its dephosphorylation. Both processes were biochemically characterized. These studies produced high-impact articles, changed the previous dogma that phosphatases are not light regulated, and identified propyl gallate as a specific inhibitor of protein phosphorylation in vivo. These discoveries have advanced scientific knowledge, opened new research worldwide into the role of phosphorylation and dephosphorylation in photosynthesis, and have become the basis of the current, novel possibility that phosphorylation and dephosphorylation of photosystem II reaction center proteins may mediate chromatic adaptation of plants to light/dark cycles, offering a mechanism by which different metabolic processes are regulated in response to internal and environmental cues. Finally, these studies offer new avenues to modulate plant growth and influence crop productivity.

Joint journal publications:
Mattoo AK, Pick U, Hoffman-Falk H, Edelman M (1981) The rapidly metabolized 32kDa polypeptide of the chloroplast is the "proteinaceous shield" regulating photosystem II electron transport and mediating diuron herbicide sensitivity. Proc. Natl. Acad. Sci. USA 78, 1572-1576.

Nachustai R, Nelson N, Mattoo AK, Edelman M (1981) Site of synthesis of subunits to photosystem I reaction center and the proton-ATPase in Spirodela. FEBS Lett. 125, 115-119.

Hoffman-Falk H, Mattoo AK, Marder JB, Edelman M, Ellis RJ (1982) General occurrence and structural similarity of the rapidly synthesized, 32kDa of the chloroplast membrane. J. Biol. Chem. 257, 4583-4587.

Mattoo AK, Marder JB, Gressel J, Edelman M (1982) Presence of the rapidly-labeled 32kDa chloroplast membrane protein in triazine resistant biotypes. FEBS Lett. 140, 36-40.

Reisfeld A, Mattoo AK, Edelman M (1982) Processing of a chloroplast-translated membrane protein in vivo: Analysis of the rapidly synthesized 32kDa shield protein and its precursor in Spirodela oligorrhiza. Eur. J. Biochem. 124, 125-129.

Goloubinoff P, Edelman M, Hallick, RB (1984) Chloroplast-coded atrazine resistance in Solanum nigrum: psbA loci from susceptible and resistant biotypes are isogenic except for a single codon change . Nucl. Acids Res. 12, 9489-9496.

Marder JB, Goloubinoff P, Edelman M (1984) Molecular architecture of the rapidly metabolized 32kDa protein of photosystem II. J. Biol. Chem. 259, 3900-3908.

Mattoo AK, Hoffman-Falk H, Marder JB, Edelman, M (1984) Regulation of protein metabolism: Coupling of photosynthetic electron transport to in vivo degradation of the rapidly-metabolized 32kDa protein of the chloroplast membranes. Proc. Natl. Acad. Sci. USA 81, 1380-1384.

Mattoo AK, St.John JB, Wergin WP (1984) Adaptive reorganization of protein and lipid components in chloroplast membranes as associated with herbicide binding. J. Cell. Biochem. 24, 163-175.

Fromm H, Devic M, Fluhr R, Edelman M (1985) Control of psbA gene expression: In mature Spirodela chloroplasts: Light regulation of 32kDa protein synthesis is independant of transcript level. EMBO J. 4, 291-295.

Eyal Y,. Goloubinoff P, Edelman. M (1987) The amino terminal region delimited by Met1 and Met37 is an integral part of the 32kDa herbicide binding protein. Plant Mol. Biol. 8, 337-343.

Gaba V, Marder JB, Greenberg B, Mattoo AK, Edelman M (1987) Degradation of the 32kDa herbicide binding protein in far-red light. Plant Physiol. 84:348-352.

Greenberg BM, Gaba V, Mattoo AK, Edelman M (1987) Identification of a primary in vivo degradation product of the rapidly-turning-over 32kDa protein of photosystem II. EMBO J. 6, 2865-2869.

Mattoo AK, Edelman M (1987) Intra-membrane translocation and post-translational palmitoylation of the chloroplast 32kDa herbicide binding protein. Proc. Nat. Acad. Sci. USA 84, 1497-1501.

Goloubinoff P, Brusslan J, Golden SS, Hasselkorn R, Edelman M (1988) Characterization of the photosystem II 32kDa-protein in Synechococcus PCC7942. Plant Mol. Biol 11, 441-447.

Callahan FE, Wergin WP, Nelson N, Edelman M, Mattoo AK (1989) Distribution of thylakoid proteins between stromal and granal lamellae in Spirodela: dual location of photosystem II components. Plant Physiol. 91, 629-635.

Greenberg BM, Gaba V, Canaani O, Malkin S, Mattoo AK, Edelman M (1989) Separate photosensitizers mediate degradation of the 32kDa photosystem II reaction center protein in the visible and UV spectral regions. Proc. Natl. Acad. Sci. USA 86, 6617-6620.

Mattoo AK, Callahan FE, Mehta RA, Ohlrogge JB (1989) Rapid in vivo acylation of acyl carrier protein with exogenous fatty acids in Spirodela oligorrhiza. Plant Physiol. 89, 707-711.

Mattoo AK, Marder JB, Edelman M (1989) Dynamics of the photosystem II reaction center. Cell 56, 241-146.

Greenberg BM, Gaba V, Mattoo AK, Edelman M (1989) Degradation of the 32kDa photosystem II reaction center protein in UV, visible and far-red light occurs through a common 23.5 kDa intermediate. Z. Naturforsch. 44c, 450-452.

Jansen MAK, Malkin S, Edelman M (1990) Differential sensitivity of 32 kDa-D1 protein degradation and photosynthetic electron flow to photosystem II herbicides. Z. Naturforsch. 45c, 408-411.

Sopory SK, Greenberg BM, Mehta RA, Edelman M, Mattoo AK (1990) Free radical scavengers inhibit light-dependent degradation of the 32kDa photosystem II reaction center protein. Z. Naturforsch. 45c, 412-417

Callahan FE, Ghirardi ML, Sopory SK, Mehta AM, Edelman M, Mattoo AK (1990) A novel metabolic form of the 32kDa-D1 protein in the grana-localized reaction center of photosystem II. J. Biol. Chem. 265, 15357-15360.

Avni A, Mehta RA, Mattoo AK, Greenberg BM, Chattoo BB, Heller D, Edelman M (1991) Nucleotide sequence of the Spirodela oligorrhiza chloroplast psbA gene coding for the D1 (32kDa) photosystem II protein. Plant Mol. Biol. 17, 919-921.

Elich T, Edelman M, Mattoo AK (1992) Identification, characterization and resolution of the in vivo phosphorylated form of the D1 photosystem II reaction center protein. J. Biol. Chem. 267, 3523-3529.

Kless H, Vermaas WFJ, Edelman M (1992) Photosystem II function and integrity in spite of drastic changes in a conserved region of the D2 protein. Biochemistry 31, 11065-11071.

Kless H, Oren-Shamir M, Ohad I, Edelman M, Vermaas W (1993) Protein modifications in the D2 protein of photosystem II affect properties of the QB/herbicide binding environment. Z. Naturforsch. 48c, 185-190.

Jansen MAK, Mattoo AK, Malkin S, Edelman M (1993) Direct demonstration of binding site competition in vivo between photosystem-II-inhibitors at the QB niche of the D1 protein. Pesticide Biochem. Physiol 46, 78-83.

Jansen MAK, Depka B, Trebst A, Edelman M (1993) Degradation of the D1 protein in photosystem II is regulated by engagement of specific sites in the plastoquinone niche. J. Biol. Chem. 268, 21246-21253.

Ghirardi ML, Mahajan S, Sopory SK, Edelman M, Mattoo AK (1993) Photosystem II reaction center particles from Spirodela stroma lamellae. J. Biol. Chem. 268, 5357-5360.

Elich,T, Edelman M, Mattoo AK (1993) Dephosphorylation of photosystem II core proteins is light-regulated in vivo. EMBO J. 12, 4857-4862.

Kless H, Oren-Shamir M, Malkin S, McIntosh L, Edelman M (1994) The D-E region of the D1 protein is involved in multiple quinone and herbicide interactions in photosystem II. Biochemistry 33, 10501-10507.

Sobolev V, Edelman M (1995) Modeling the quinone-B site of the photosystem II reaction center using notions of complementarity and contact surface between atoms. Proteins 21, 214-225.

Oren-Shamir M, Maruthi S, Edelman M Scherz A (1995) Isolation and spectroscopic characterization of a plantlike photosystem II reaction center from the cyanobacterium Synechocystis Sp. 6803. Biochemistry 34, 5523-5526.

Jansen, MAK, Babu TS, Heller D, Gaba V, Mattoo AK, Edelman M (1996) Ultraviolet-B effects on Spirodela oligorrhiza: induction of different protection mechanisms. Plant Sci. 115, 217-223.

Jansen MAK, Gaba V, Greenberg BM, Mattoo AK, Edelman M (1996) Low threshold levels of ultraviolet-B in a background of photosynthetically active radiation trigger rapid degradation of the D2 protein of photosystem-II. Plant J. 9, 693-699.

Jansen MAK, Greenberg BM, Edelman M, Mattoo AK, Gaba V (1996) Accelerated degradation of the D2 protein of photosystem II under ultraviolet radiation. Photochem. Photobiol. 63, 814-817.

Giardi MT, Cona A, Geiken B, Kucera T, Masojidek J, Mattoo AK (1996) Long-term drought stress induces structural and functional reorganization of Photosystem II. Planta 199, 118-125.

Elich TD, Edelman M, Mattoo AK (1997) Evidence for light-dependent and light-independent protein dephosphorylation in chloroplasts. FEBS Lett. 411, 236-238.

Koblizek M, Masojidek J, Komenda J, Kucera T, Pilloton R, Mattoo AK, Giardi MT (1998) A sensitive photosystem II-based biosensor for detection of a class of herbicides. Biotechnol. Bioeng. 60, 664-669.

Lardens A, Forster B, Prasil O, Falkowski PG, Sobolev V, Edelman M, Osmond CB, Gilham NW and Boynton JE (1998) Biophysical, biochemical and physiological characterization of Chlamydomonas reinhardtii mutants with amino acid substitutions at the Ala251 residue of the D1 protein that results in varying levels of photosynthetic competence. J.Biol. Chem. 273, 11082-11091.

Janse MAK, Mattoo AK, Edelman M (1999) Photodynamics of D1-D2 protein catabolism in the chloroplast. Eur. J. Biochem. 260, 527-532.

Babu TS, Jansen MAK, Greenberg BM, Gaba, V, Malkin S, Mattoo AK, Edelman M (1999) Amplified degradation of the photosystem II D1 and D2 proteins under a mixture of PAR and UV-B: Dependence on photosystem II electron transport. Photochem Photobiol. 69, 553-559.

Mattoo AK, Giardi M-T, Raskind A, Edelman M (1999) Dynamic metabolism of photosystem II reaction center proteins and pigments. Physiol. Plant. 107, 454-461.

Booij-James IS, Dube SK, Jansen MAK, Edelman M, Mattoo AK (2000) Ultraviolet-B radiation impacts light-mediated turnover of the photosystem II reaction center heterodimer in Arabidopsis mutants altered in phenolic metabolism. Plant Physiol. 124, 1275-1283.

Mattoo AK, et al. (2000) Invention Report No. 0154.00, Photosystem II-based biosensor for detection and environmental monitoring of photosynthesis-inhibiting herbicides (triazines, phenylureas). Accepted by Biotechnology Patent Committee, 12-10-00.

Koblizek M, Maly J, Masojidek J, Komenda J, Kucera T, Giardi MT, Mattoo AK, Pilloton R (2002) A biosensor for the detection of triazine and phenylurea herbicides designed using Photosystem II coupled to a screen-printed electrode. Biotechnol. Bioeng. In Press.

Booij-James IS, Swegle M, Edelman M, Mattoo AK (2002) Phosphorylation of the D1 photosystem II reaction center protein is controlled by an endogenous circadian rhythm. In Review.

Book Chapters:
Edelman M, Marder JB, Mattoo AK (1983) A compendium of characteristics for the rapidly metabolized 32 kd protein of the chloroplast membrane. In: Structure and function of plant genomes. Ciferri O, Dure L, Eds. Plenum, New York pp. 187-192.

Edelman M, Mattoo AK, Marder JB (1984) Three hats of the rapidly metabolized 32 kD protein of thylakoids. In: Chloroplast biogenesis. Ellis RJ, Ed. Cambridge University Press. pp. 283-302.

Marder JB, Mattoo AK, Goloubinoff P, Edelman M (1984) Structure and physiological control of the rapidly-metabolized 32kDa chloroplast membrane protein. In: Biosynthesis of the photosynthetic apparatus: molecular biology, development and regulation. Eds. Thornber P, Staehelin A, Hallick RB. Liss Inc., New York pp. 309-311.

Edelman M, Goloubinoff P, Marder JB, Fromm, H, Devic M, Fluhr R, Mattoo AK (1985) Structure-function relationships and regulation of the 32kDa protein of the photosynthetic membranes. In: Molecular form and function of the plant genome. eds. van Vloten-Doting L, Groot, GSP, Hall TC, Plenum, New York. pp. 291-300.

Mattoo AK, Edelman M (1985) Photoregulation and metabolism of a thylakoidal herbicide-receptor protein. In: Frontiers of membrane research in agriculture. St.John JB, Berlin E, Jackson PC, Eds. Rowman & Allanheld, Totowa. pp 23-34.

Marder JB, Mattoo AK, Edelman M (1986) Identification and characterization of the psbA gene product: the 32kDa chloroplast membrane protein. Meth. Enzymol. 118, 384-396.

Mattoo AK, Marder JB, Gaba V, Edelman M (1986) Control of 32kDa thylakoid protein degradation as a consequence of herbicide binding to its receptor. In: Regulation of Chloroplast Differentiation Akoyunoglou G, Senger H, Eds. Plant Biology Series, Alan R. Liss Inc., Pub., New York. pp. 607-613.

Callahan FE, Edelman M, Mattoo AK (1987) Post-translational acylation and intra-thylakoid translocation of specific chloroplast proteins. In: Progress in Photosynthesis Research. Vol III. Biggens J, Ed. Martinus Nijhoff, Dordrecht. pp. 702-799.

Norman HA, St. John JB, Callahan FE, Mattoo AK, Wergin JP (1987) Lipid molecular species composition of granal and stromal lamellae. In: The Metabolism, Structure and Function of Plant Lipids. Stumpf PK, Mudd JB, Nes WD, Eds. Plenum, New York. pp. 193-195.

Mattoo AK, Callahan FE, Greenberg BM, Goloubinoff P, Edelman M (1989) Molecular dynamics of the 32kDa photosystem II herbicide binding protein. In: Biotechnology for Crop Protection Hedin P, Menn J, Hollingsworth R., Eds. American Chem. Soc. Symp. Series, ACS Books, Washington. pp. 248-257.

Mattoo AK, Callahan FE, Sopory SK, Edelman M (1989) Trafficking and distribution of the photosynthesic reaction center proteins in the chloroplast membranes. In: Photosynthesis: molecular biology and bioenergetics. Singhal G, Ed. Narosa Pub. House, New Dehli. pp. 189-191.

Mattoo AK, Norman HA, Callahan FE, St. John JB, Edelman M (1989) Plant protein acylation: Identification of the modified proteins and analysis of the bound fatty acid ligand. In: Post-Translational Modification of Proteins by Lipids. Brolbeck U, Bordier C, Eds, Springer-Verlag, Berlin. pp. 82-87.

Greenberg BM, Sopory S, Gaba V, Mattoo AK, Edelman M (1990) Photoregulation of protein turnover in the PSII reaction center. In: Current Research in Photosynthesis. Vol. I. Baltscheffsky M, Ed. Kluwer Acad Publ., Dordrecht. 209-216.

Ghirardi ML, Callahan FE, Sopory SK, Elich T, Edelman M, Mattoo AK (1990) Cycling of the photosystem II reaction center core between grana and stroma lamellae. In: Current Research in Photosynthesis Vol. II. Baltscheffsky M, Ed., Kluwer Acad. Pub., Holland. pp. 733-738.

Ghirardi ML, Sopory SK, Elich T, Greenberg BM, Edelman M, Mattoo AK (1991) Light-induced degradation of the D1photosystem II reaction center protein. In: Recent advances in Bioeinergetic Processes. Singhal GS, Ed. Today & Tomorrow Publ. New Dehli. pp.57-63.

Sopory SK, Ghirardi ML, Greenberg BM, T Elich, Edelman M, Mattoo AK (1992) Regulation of the 32kDa-D1 photosystem II reaction center protein. In: Photosynthesis: photoreactions to plant productivity. Abrol YP, Mohanty P, Govindjee, Eds. Oxford & IBH Publ. New Delhi. pp. 132-156.

Elich T, Edelman M, Mattoo AK (1992) Redox-regulated protein phosphosphorylation and photosystem II function. In: Regulation of chloroplast biogenesis. Argyroudi-Akoyunoglou JH, Ed. Plenum, New York. pp. 533-537.

Jansen MAK, Driesenaar ARJ, Kless H, Malkin S, Mattoo AK, Edelman M (1992) PSII inhibitor binding, QB-mediated electron flow and rapid degradation are separable properties of the D1 reaction center protein. In: Regulation of chloroplast biogenesis..Argyroudi-Akoyunoglou JH Ed., Plenum, New York. 303-311.

Jansen MAK, Gaba V, Greenberg BM, Mattoo AK, Edelman M (1993) UV-B driven degradation of the D1 reaction-center of photosystem II proceeds via plastosemiquinone. In: Photosynthetic responses to the environment. Yamamoto HY, Smith CM, Eds. Amer. Soc. Plant Physiol. Washington. pp. 142-149.

Mattoo AK, Elich T, Ghirardi ML, Callahan FE, Edelman M (1993) Post-translational modification of chloroplast proteins and the regulation of protein turnover. In Post-Translational Modifications in Plants. Battey NH, Dickinson HG, Hetherington AM, Eds. SEB Seminar series 53, Cambridge U. Press. pp. 65-78.