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Plant thioredoxins: role of the French School
Plant Physiology and Biochemistry 41 (2003) 505–512 www.elsevier.com/locate/plaphy
Review
Plant thioredoxins: role of the French School Bob B. Buchanan *, Yves Balmer Department of Plant and Microbial Biology, University of California, 111 Koshland Hall, Berkeley, CA 94720, USA Received 20 November 2002; accepted 5 February 2003
Abstract A seminal discovery made by Pierre Gadal and his collaborators in Nancy, almost 30 years ago, has served as a nucleus for further development of research on plant thioredoxins. By attracting other investigators, research in the area has flourished and enabled France to assume a leadership position in the field. The chronology of development of this research is traced in the present review, from its origin in Nancy to its current distribution throughout France. A summary of the achievements of participating French scientists documents their influence on the field and the international thioredoxin community. The article closes with a personal perspective of Gadal’s scientific and professional contributions that was developed by the senior author during visits to Orsay over the past three decades. © 2003 Éditions scientifiques et médicales Elsevier SAS. All rights reserved. Keywords: Ferredoxin/thioredoxin system; NADP/thioredoxin system; Pierre Gadal; Plant thioredoxins
1. Introduction It is an honor to write an article that pays tribute to Pierre Gadal, on the occasion of his retirement from a distinguished university career that began in Nancy and culminated in Orsay. We approach this opportunity by describing how Gadal’s work in a particular area of photosynthesis research has served as the nucleus for the genesis of an effort that assumed national proportions and became part of an international effort. In this development, he and his colleagues have paved the way for France to become a leader in this research field. We begin by putting his work in a historical setting and then show how the initial embryonic efforts have developed and flourished.
2. Chronology 2.1. The beginning Research in photosynthesis in the late 1960s began to provide new clues on the way chloroplast enzymes are modu-
Abbreviations: DTT, dithiothreitol; FTR, ferredoxin-thioredoxin reductase; NTR, NADP-thioredoxin reductase. * Corresponding author. E-mail address: [email protected] (B.B. Buchanan). © 2003 Éditions scientifiques et médicales Elsevier SAS. All rights reserved. DOI: 10.1016/S0981-9428(03)00064-0
Pierre Gadal, 2000, the year he was selected as a Corresponding Member of the American Society of Plant Biologists. The senior author attended the ceremony at the annual meeting of the society in San Diego, where he received the award.
lated by light. Light was initially found to function via a ferredoxin-linked reductive reaction for the activation of fructose-1,6-bisphosphatase [13], although later, it was known to act through several other mechanisms (e.g., changes in pH, Mg2+, effectors rubisco activase). It later became evident that ferredoxin did not interact directly with the target enzyme to achieve activation, but required a protein factor [14], which was later resolved into two components [64]. The two required proteins were soon identified as ferredoxin-thioredoxin reductase (FTR) and a thioredoxin [16,67]. The thioredoxin fraction, itself, was then resolved into two components— thioredoxins f and m—with specificity for different target enzymes [17,68]. Together with ferre-
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doxin, these three proteins were later found to effect the regulation of a spectrum of enzymes via the mechanism that became known as the ferredoxin/thioredoxin system [9–11,15,63]. The system, present in chloroplasts and oxygenic photosynthetic prokaryotes, worked, in effect, by using photons and electrons (from water) to reduce disulfide bonds on target enzymes. In this way, thioredoxin acted as “eye” by which biochemical processes of chloroplasts distinguished light from dark and adjusted their rates accordingly [9–11,15]. While the fructose bisphosphatase work was in progress, Pierre Gadal and his colleagues, Jean Vidal and Jean-Pierre Jacquot, then in Nancy, described a protein factor that was needed in the presence of dithiothreitol (DTT), for the activation of another chloroplast enzyme, NADP-malate dehydrogenase [43]. Soon thereafter, experiments carried out in Nancy led to the identification of the protein factor as thioredoxin m and showed the f-counterpart to be a separate protein [44]. The f- and m-type thioredoxins were named for their respective ability to activate fructose-1,6-bisphosphatase and NADP-malate dehydrogenase [17]. Peter Schürmann in Neuchâtel who had earlier worked in Berkeley on the fructose bisphosphatase protein factor, collaborated with the Nancy group in identifying the NADP-malate dehydrogenase counterpart. Interestingly, the active components of the protein factor faction were found to be identical to thioredoxins f and m in the bisphosphatase and dehydrogenase assays. Jacquot’s postdoctoral visit to Buchanan’s laboratory in Berkeley in the early 1980s confirmed and extended the original Nancy experiments and led to the purification and characterization of NADP-dependent malate dehydrogenase. Later in the decade, the Berkeley group also benefited from the short-term visits of Gadal, Myroslawa Miginiac-Maslow and Jacquot. The latter investigators by then were working as a team in Orsay. Impressive advances were made at this time on FTR in experiments, which were carried out by Michel Droux, initially as a graduate student in Orsay and later as a postdoctoral scholar in Berkeley. The collaboration led to the publication of several papers [26–28,36,39,40,54]. As a result of this longstanding association, joint articles continue to be published [15]. During the 1980s, Tom Johnson and Heather Huppe visited Orsay after completing their doctoral studies in Berkeley. As described later, dramatic progress has been made in the 25 years since the discovery of the ferredoxin/thioredoxin system: elucidation of the function, structure, physical properties, mechanism and genes of its protein members [3,9– 11,15,41,61,63]. Much of the progress has been due to the achievements of scientists actively working on plant thioredoxins in France, subsequently referred to as the “French School.” 2.2. The field expands Following the lead of Gadal and his collaborators, several groups started to investigate plant thioredoxins in the 1980s, thereby advancing the French School to a leading position in
Fig. 1. Chronological development of plant thioredoxins in laboratories of the French School. Plant thioredoxin research in France was initiated in Nancy by Gadal, Vidal and Jacquot. The major laboratories stemming from this origin (Orsay and later again Nancy) and those developed independently in Montpellier, Perpignan and Lyon are identified by the year in which research was initiated on thioredoxins.
the field (Fig. 1). During this period, the highly successful collaboration between Jacquot and Miginiac-Maslow referred to the above-produced outstanding contributions on NADP-malate dehydrogenase and related problems. P. Decottignies, P. Le Maréchal, E. Issakidis-Bourguet and M. Stein were an integral part of this Orsay effort. Since his return to Nancy 5 years ago, Jacquot has started a collaboration with E. Gelhaye and C. Corbier, and he and MiginiacMaslow have pursued separate thioredoxin projects. Nevertheless, the scientific success of their programs has continued unabated. Some of their achievements have been recently summarized [41,61,63]. The next development of the French School stemmed from Karoly Kobrehel’s sabbatical visit to Buchanan’s laboratory in Berkeley in the early 1990s. At that time, evidence was obtained for a function for the then-recently-identified plant cytosolic thioredoxin h [29 and references therein]. Biochemical experiments suggested that thioredoxin h reduced critical disulfide groups of proteins of the endosperm of wheat seeds and, in effect, acted as a wakeup call in the germination process [10,11,47]. Recent experiments with barley seeds, which overexpressed thioredoxin h, have confirmed and extended these results in new directions [21,69]. While in Berkeley, Kobrehel and Buchanan also designed experiments, since successfully completed, to test the concept that treatment by reduced thioredoxin could lead to the improvement of foods. Following his return to Montpellier, Kobrehel continued this line of research and observed positive effects of thioredoxin on dough improvement, in addition to providing new information on grain proteins [46]. In related research, P. Joudrier, M.-F. Gautier, F. de Lamotte and colleagues have successfully pursued the cloning of the wheat thioredoxin h gene and characterized its protein product [32]. During the same period, a team led by Y. Meyer in Perpignan initiated a comprehensive study of plant thioredoxins at both the gene and protein levels. Their work has given insight into the structure and evolution of plant thioredoxin genes
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and into the function of thioredoxin h [7,52,55,57,58,62,66]. The Meyer group has also characterized the mitochondrial thioredoxin system [5,49]. Data made available through the sequencing of the Arabidopsis thaliana genome have been a great asset in their studies. Starting in the early 1990s, J.M. Lancelin in Lyon applied NMR technology to elucidate the structure of thioredoxins m and h and their associated enzymes [48,50,53]. His contributions have been central to our understanding not only of the structure, but also the mechanism of action of thioredoxins and NADP-thioredoxin reductase (NTR), the flavin enzyme catalyzing the reduction of thioredoxin h by NADPH. Not shown in Fig. 1 are the French scientists who have made important contributions on thioredoxin in investigations that initially were not directed to thioredoxin. The pursuits of C. Dumas and T. Gaude (Lyon) on fertilization in Brassica gave new insight on how thioredoxin of the stigma acts to control self-incompatibility via a protein kinase [18]. Similarly, Rey et al. (Cadarache) [56] recently uncovered a thioredoxin-like protein that acts in drought stress. Also not shown in Fig. 1 are contributing French scientists, who are no longer working in the thioredoxin field or whose projects have a different focus. These include the groups of J. Ricard and his collaborator J.-C. Meunier in Marseilles, who added information on chloroplast thioredoxins and target enzymes [65]; Clément-Métral et al. (Compiègne) [22], who laid the foundation for thioredoxin occurrence and function in photosynthetic bacteria; Balangé and Lambert (Rouen) [2], who followed a similar path and studied heme biosynthesis in these organisms; and finally G. Girault and J.M. Galmiche (Saclay), who studied the thioredoxin-linked activation of chloroplast CF1 [31]. B. Gontero, who worked earlier in Ricard’s group, has continued this line of research in Paris, where she currently investigates enzyme complexes of the Calvin cycle, including components linked to thioredoxin [1]. 3. Research contributions 3.1. Chloroplast ferredoxin/thioredoxin system Important contributions of the French school on plant thioredoxins are summarized in Table 1. Earlier results by Gadal and colleagues are reproduced in Fig. 2, which shows the purification of a protein factor required for the activation of NADP-malate dehydrogenase by DTT [43]. The identification of the protein factor as thioredoxin m is illustrated in Fig. 3, which also documents the presence of thioredoxin f in the preparation [44]. This study of thioredoxin-linked redox regulation in chloroplasts initiated by Gadal and his colleagues in Nancy in the mid 1970s, broke new ground on chloroplast thioredoxin m and set the stage for others in France and elsewhere to pursue related studies, initially on the ferredoxin/thioredoxin system and later on other problems, such as the NADP/thioredoxin counterpart and the target enzymes of both systems.
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Fig. 2. Purification of the protein factor found by Jacquot, Vidal and Gadal to be required for the activation of NADP-malate dehydrogenase by DTT. The factor was purified from a DEAE-cellulose column by applying an NaCl gradient. The experiments were carried with extracts prepared from French bean leaves (adapted from [43]). Activity of NADP-malate dehydrogenase is shown on the ordinate. The protein factor activating the enzyme peaked at fractions 10 and 11.
Fig. 3. Identification of thioredoxin m as the protein factor required for the DTT-dependent NADP-malate dehydrogenase activation. The presence of thioredoxin f was also demonstrated through its activation of fructose bisphosphatase by DTT. (C—C), NADP-malate dehydrogenase (thioredoxin m activity); (•—•), fructose bisphosphatase (thioredoxin f activity) (adapted from [44]).
The mechanism of regulation of chloroplast NADPmalate dehydrogenase has been studied extensively during the last 15 years by biochemical, genetic and structural approaches [19,25,37,45,48]. Taken together, the data explain the step-by-step activation of the enzyme. The mechanism entails the sequential reduction of the two disulfide bonds that occur in extensions at the C- and N-termini specific to the chloroplast isoform. The N-terminal disulfide helps to stabilize the inactive form of the dimer, whereas the C-terminal disulfide controls substrate access by fixing the enzyme in a position that blocks the active site. The reduction of the two regulatory disulfides thus facilitates a structural change that yields a fully active enzyme with ready substrate access to its binding site [61]. Fructose bisphosphatase, another model enzyme of thioredoxin regulation, has also been studied extensively. Amino acid sequence alignment of the enzyme from the cytosol and chloroplast showed that plastid isoforms contain an internal insertion of about 20 amino acids with three conserved cysteines. Site-directed mutagenesis experiments demonstrated that the replacement of one of these cysteines (Cys153 in pea) by a serine yielded a constitutively fully active enzyme, whereas the mutation of either one of the two
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other cysteines resulted in partial activity [42,59]. These findings led to the conclusion that the regulatory disulfide could be formed between Cys153 and either one of the two remaining cysteines (Cys173 or Cys178). However, the elucidation of the structure of pea chloroplast fructose-1,6-bisphosphatase clearly showed that a single disulfide (formed between Cys153 and Cys 173) is involved in the redox regulation of the enzyme [20]. Thus, the third conserved cysteine located near the regulatory site seems to form a bond that is an artifact associated with the mutant enzyme [4,20]. Biochemical studies mentioned above laid the foundation for the characterization of FTR, a unique type of iron-sulfur enzyme that, through its reduction of thioredoxins links light to enzyme activity [26,27]. The enzyme, whose structure and reaction mechanism have recently been solved [24], composed of two heterosubunits and was able to accept electrons from two ferredoxins via a disulfide group that, in turn, reduces the disulfide of chloroplast thioredoxins. Finally, the screening of a cDNA library of A. thaliana led to the identification of four genes coding for chloroplast thioredoxins m, and a new type of thioredoxin, x [52]. This multiplicity of proteins raises the question of their distribution and expression as well as their function. Subsequent yeast complementation experiments revealed a new putative function for m-type thioredoxin [38]. The recent work of Rey et al. [56] has uncovered a chloroplast thioredoxin-like protein (CDSP32), which was expressed in response to drought stress. Subsequent study shows that CDSPS32 together with a 2Cys peroxiredoxin functions in protection against oxidative damage [8,56].
thioredoxin h and NTR has been achieved [23,51,53]. Thioredoxin h specificity has also been characterized by using yeast complementation [7] and more recently, by linking the promoters of different thioredoxin h genes to the GUS reporter and analyzing individual plant tissues [55]. In a similar line of experiments, a new family of peroxiredoxins has been isolated in yeast two hybrid experiments [66]. Application of a procedure based on the use of a thioredoxin h mutant, in which the buried cysteine of the active site was replaced by a serine, bound a protein identified as chloroplast peroxiredoxin [34]. Using EST sequence data, Rouhier et al. [60] cloned and characterized a novel type of peroxiredoxin from poplar. The study of thioredoxin h of wheat [32] is of particular interest, owing to its potential application in the improvement of foods by lowering allergenicity [12] and enhancing dough quality [46]. Recently, the role of thioredoxin h has been extended by Dumas and Gaude in a new direction, from new data on how its earlier-observed link to a protein kinase [6] controls self-incompatibility during fertilization [18]. This work opens a new door to investigate the fertilization process. 3.3. Mitochondrial thioredoxin system Meyer and his group have identified and characterized the NTR and yet another type of thioredoxin, thioredoxin o, of plant mitochondria [3,49]. This work makes it possible to elucidate the role of thioredoxin in these organelles—a problem that surfaced when Follmann and his collaborators demonstrated that mitochondria contain a thioredoxin [5].
3.2. Cytosolic NADP/thioredoxin system Several French research groups have actively studied plant cytosolic thioredoxin h and NTR. Their efforts have resulted in the cloning of several thioredoxin h genes and the characterization of their protein products [7,33,55,57,58,62]. The resolution of the three-dimensional structure of both
4. Influence The influence of the French School, during the past 25 years, has had a profound effect on the thioredoxin field. As apparent from Table 1, French scientists have contributed
Table 1 Pathbreaking contributions on plant thioredoxins by the French School. Most of the below contributions were made by established laboratories of the French School. The findings on CDSP32 (by P. Rey) and self-incompatibility (by T. Gaude and C. Dumas) were made in research not initially directed toward thioredoxin Chloroplast ferredoxin/thioredoxin system • Early studies on thioredoxin m • Genetic and functional analysis of thioredoxin m • Characterization of ferredoxin-thioredoxin reductase • Mechanism of regulation and structure of fructose-1,6-bisphosphate phosphatase • Mechanism of regulation and structure of NADP-malate dehydrogenase • Identification of CDSP32, a thioredoxin-like chloroplastic protein, in drought stress Cytosolic NADP/thioredoxin system • Cloning, characterization and structure of thioredoxin h • Genetic, evolutionary and functional properties of thioredoxin h • Importance of thioredoxin h in cereals and its applications in biotechnology • Role of thioredoxin h in self-incompatibility in Brassica Mitochondrial NADP/thioredoxin system • Identification and characterization of NADP-thioredoxin reductase and thioredoxin o from plant mitochondria
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Table 2 Long-term international collaborations with the French School Collaborator Bob B. Buchanan (Berkeley)
Ana Chueca Julio Lopez-Gorge (Granada)
French counterparts P. Gadal J.-P. Jacquot M. Miginiac-Maslow P. Decottignies M. Droux K. Kobrehel J.-P. Jacquot M. Miginiac-Maslow
Cooperative research Properties of members of the ferredoxin/thioredoxin system and target enzymes Thioredoxin biotechnology Properties of target enzymes Fig. 4. Current research on plant thioredoxins by the French School.
Hans Eklund (Uppsala) J.-P. Jacquot M. Miginiac-Maslow E. Issakidis-Bourguet David B. Knaff J.-P. Jacquot (Lubbock) M. Miginiac-Maslow Y. Meyer Peter Schürmann (Neuchâtel)
P. Gadal J. Vidal J.-P. Jacquot
Structure of NTR and NADP-MDH Physical characterization of proteins associated with the ferredoxin/thioredoxin system Functional properties of thioredoxin and target enzymes; key review article
seminal information on the ferredoxin/thioredoxin system (thioredoxin m, FTR) and target enzymes (NADP-malate dehydrogenase, fructose bisphosphatase). Similar advances have been made with the NADP/thioredoxin system, including key contributions not only on the structure and function of thioredoxin h and NTR, but also on the novel system recently identified in mitochondria. These achievements have been amplified by conferences hosted or co-hosted by the French School—first the International Conference on Thioredoxin held in Berkeley in 1981 (followed up with a book of the proceedings edited by Gadal [30]), and later, the 1990 Jacques Monod Conference on Thioredoxins and Glutaredoxins held in Roscoff. The contributions in Table 1 and the conferences, however, tell only part of the story. Results obtained in long-term international collaborations (Table 2) have extended the findings made in France and moved the field in decisive new directions. In addition to promoting science, these collaborations have led to countless exchange visits and lasting friendships between French scientists and the international thioredoxin community. 5. Future prospects Patrick Henry, an illustrious Virginian and an ardent supporter of independence, made reference to the future of the colonies in a well-known speech, given at the dawn of the American Revolution: “I have but one lamp by which my feet are guided, and that is the lamp of experience. I know no way of judging the future but by the past.” [35]
From this perspective, it is appropriate to examine the research on plant thioredoxins that has been or is being carried out in France. Past research is summarized above and ongoing work is identified in Fig. 4. The projects cover a broad range, including the studies of both the ferredoxin/ thioredoxin and NADP/thioredoxin systems as well as pertinent target enzymes. Furthermore, the laboratories continue to apply approaches based on biochemistry, physiology, genetics, structure, biotechnology and agronomy that span the biological spectrum. Past experience coupled with the new talent entering the field bode well for a rich future for thioredoxin research in France. 6. Reflections It seems fitting to close this tribute on a personal note. One of us (B.B.B.) has interacted closely with Pierre Gadal for 25 years on both a personal and scientific basis. This association was enriched by B.B.B.’s spending a part of two sabbatical leaves (1984, 1991) in Orsay and, during most of this period, by annual visits to his laboratory. In 1984, he was accompanied by his wife, Melinda, and four daughters, who had a truly memorable visit as a result of the gracious hospitality of the members of the Orsay laboratory and the Gadal family. Ferried by a new Peugeot 505 wagon (now in Berkeley), the Buchanans enjoyed guided trips to historic French sites and a long weekend at the Gadal’s home in Brittany. It was a pleasure during these visits to witness Pierre, in collaboration with Francis Quétier, turn what initially was a dream into a grand structure that today houses the Institut de Biotechnologie des Plantes—a leading group in plant biology research. The trips to Orsay were also often associated with gratifying academic activities—e.g., seminars either in-house or at neighboring laboratories and service as an external examiner on doctoral thesis committees, such as the one for Akira Suzuki, whose research dealt with nitrogen metabolism, another of Gadal’s long-term interests. Invariably provided were opportunities to meet and interact with foreign visitors, including North American colleagues, such as Ann Oaks, Ray Chollet and David Knaff. As noted above, the transatlantic trips from California were complemented by reciprocal visits to Berkeley by Pierre and members of his
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laboratory. Pierre’s visits stand out as being particularly pleasant and productive: one of his longer stays resulted in a paper on glutamine synthetase—a favorite topic [28]—and provided an opportunity for him to attend the US Japan Seminar on Environmental Plant Stress in Fairbanks, Alaska. Finally, a traditional part of B.B.B.’s trips to Orsay included social activities integrated into each visit, irrespective of its duration. In addition to daily swims in the Orsay pool and countless activities arranged by different members of the laboratory, the visits included the incomparable dinners hosted at the Gadal home and the memorable tea held religiously each afternoon around four o’clock that was attended by all the members of the laboratory. On special occasions, everyone enjoyed delectable pastries available only in France, including for one celebration of American Independence (July 4), cakes from Lenôtre in Paris. The informal atmosphere at these gatherings encouraged lively discussions on topics that ranged from science to contemporary American television soap operas. Congeniality combined with exciting science made visits to Orsay unforgettable.
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The authors wish to thank the Federation of the European Biochemical Societies for permission to reprint Figs. 2 and 3 (Jacquot et al. “Identification of a Protein....”, FEBS Lett. 71 (1976) 223-246 and Jacquot et al. “Evidence for several enzyme...”, FEBS Lett. 96 (1978) 243-246).
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Review
Plant thioredoxins: role of the French School Bob B. Buchanan *, Yves Balmer Department of Plant and Microbial Biology, University of California, 111 Koshland Hall, Berkeley, CA 94720, USA Received 20 November 2002; accepted 5 February 2003
Abstract A seminal discovery made by Pierre Gadal and his collaborators in Nancy, almost 30 years ago, has served as a nucleus for further development of research on plant thioredoxins. By attracting other investigators, research in the area has flourished and enabled France to assume a leadership position in the field. The chronology of development of this research is traced in the present review, from its origin in Nancy to its current distribution throughout France. A summary of the achievements of participating French scientists documents their influence on the field and the international thioredoxin community. The article closes with a personal perspective of Gadal’s scientific and professional contributions that was developed by the senior author during visits to Orsay over the past three decades. © 2003 Éditions scientifiques et médicales Elsevier SAS. All rights reserved. Keywords: Ferredoxin/thioredoxin system; NADP/thioredoxin system; Pierre Gadal; Plant thioredoxins
1. Introduction It is an honor to write an article that pays tribute to Pierre Gadal, on the occasion of his retirement from a distinguished university career that began in Nancy and culminated in Orsay. We approach this opportunity by describing how Gadal’s work in a particular area of photosynthesis research has served as the nucleus for the genesis of an effort that assumed national proportions and became part of an international effort. In this development, he and his colleagues have paved the way for France to become a leader in this research field. We begin by putting his work in a historical setting and then show how the initial embryonic efforts have developed and flourished.
2. Chronology 2.1. The beginning Research in photosynthesis in the late 1960s began to provide new clues on the way chloroplast enzymes are modu-
Abbreviations: DTT, dithiothreitol; FTR, ferredoxin-thioredoxin reductase; NTR, NADP-thioredoxin reductase. * Corresponding author. E-mail address: [email protected] (B.B. Buchanan). © 2003 Éditions scientifiques et médicales Elsevier SAS. All rights reserved. DOI: 10.1016/S0981-9428(03)00064-0
Pierre Gadal, 2000, the year he was selected as a Corresponding Member of the American Society of Plant Biologists. The senior author attended the ceremony at the annual meeting of the society in San Diego, where he received the award.
lated by light. Light was initially found to function via a ferredoxin-linked reductive reaction for the activation of fructose-1,6-bisphosphatase [13], although later, it was known to act through several other mechanisms (e.g., changes in pH, Mg2+, effectors rubisco activase). It later became evident that ferredoxin did not interact directly with the target enzyme to achieve activation, but required a protein factor [14], which was later resolved into two components [64]. The two required proteins were soon identified as ferredoxin-thioredoxin reductase (FTR) and a thioredoxin [16,67]. The thioredoxin fraction, itself, was then resolved into two components— thioredoxins f and m—with specificity for different target enzymes [17,68]. Together with ferre-
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doxin, these three proteins were later found to effect the regulation of a spectrum of enzymes via the mechanism that became known as the ferredoxin/thioredoxin system [9–11,15,63]. The system, present in chloroplasts and oxygenic photosynthetic prokaryotes, worked, in effect, by using photons and electrons (from water) to reduce disulfide bonds on target enzymes. In this way, thioredoxin acted as “eye” by which biochemical processes of chloroplasts distinguished light from dark and adjusted their rates accordingly [9–11,15]. While the fructose bisphosphatase work was in progress, Pierre Gadal and his colleagues, Jean Vidal and Jean-Pierre Jacquot, then in Nancy, described a protein factor that was needed in the presence of dithiothreitol (DTT), for the activation of another chloroplast enzyme, NADP-malate dehydrogenase [43]. Soon thereafter, experiments carried out in Nancy led to the identification of the protein factor as thioredoxin m and showed the f-counterpart to be a separate protein [44]. The f- and m-type thioredoxins were named for their respective ability to activate fructose-1,6-bisphosphatase and NADP-malate dehydrogenase [17]. Peter Schürmann in Neuchâtel who had earlier worked in Berkeley on the fructose bisphosphatase protein factor, collaborated with the Nancy group in identifying the NADP-malate dehydrogenase counterpart. Interestingly, the active components of the protein factor faction were found to be identical to thioredoxins f and m in the bisphosphatase and dehydrogenase assays. Jacquot’s postdoctoral visit to Buchanan’s laboratory in Berkeley in the early 1980s confirmed and extended the original Nancy experiments and led to the purification and characterization of NADP-dependent malate dehydrogenase. Later in the decade, the Berkeley group also benefited from the short-term visits of Gadal, Myroslawa Miginiac-Maslow and Jacquot. The latter investigators by then were working as a team in Orsay. Impressive advances were made at this time on FTR in experiments, which were carried out by Michel Droux, initially as a graduate student in Orsay and later as a postdoctoral scholar in Berkeley. The collaboration led to the publication of several papers [26–28,36,39,40,54]. As a result of this longstanding association, joint articles continue to be published [15]. During the 1980s, Tom Johnson and Heather Huppe visited Orsay after completing their doctoral studies in Berkeley. As described later, dramatic progress has been made in the 25 years since the discovery of the ferredoxin/thioredoxin system: elucidation of the function, structure, physical properties, mechanism and genes of its protein members [3,9– 11,15,41,61,63]. Much of the progress has been due to the achievements of scientists actively working on plant thioredoxins in France, subsequently referred to as the “French School.” 2.2. The field expands Following the lead of Gadal and his collaborators, several groups started to investigate plant thioredoxins in the 1980s, thereby advancing the French School to a leading position in
Fig. 1. Chronological development of plant thioredoxins in laboratories of the French School. Plant thioredoxin research in France was initiated in Nancy by Gadal, Vidal and Jacquot. The major laboratories stemming from this origin (Orsay and later again Nancy) and those developed independently in Montpellier, Perpignan and Lyon are identified by the year in which research was initiated on thioredoxins.
the field (Fig. 1). During this period, the highly successful collaboration between Jacquot and Miginiac-Maslow referred to the above-produced outstanding contributions on NADP-malate dehydrogenase and related problems. P. Decottignies, P. Le Maréchal, E. Issakidis-Bourguet and M. Stein were an integral part of this Orsay effort. Since his return to Nancy 5 years ago, Jacquot has started a collaboration with E. Gelhaye and C. Corbier, and he and MiginiacMaslow have pursued separate thioredoxin projects. Nevertheless, the scientific success of their programs has continued unabated. Some of their achievements have been recently summarized [41,61,63]. The next development of the French School stemmed from Karoly Kobrehel’s sabbatical visit to Buchanan’s laboratory in Berkeley in the early 1990s. At that time, evidence was obtained for a function for the then-recently-identified plant cytosolic thioredoxin h [29 and references therein]. Biochemical experiments suggested that thioredoxin h reduced critical disulfide groups of proteins of the endosperm of wheat seeds and, in effect, acted as a wakeup call in the germination process [10,11,47]. Recent experiments with barley seeds, which overexpressed thioredoxin h, have confirmed and extended these results in new directions [21,69]. While in Berkeley, Kobrehel and Buchanan also designed experiments, since successfully completed, to test the concept that treatment by reduced thioredoxin could lead to the improvement of foods. Following his return to Montpellier, Kobrehel continued this line of research and observed positive effects of thioredoxin on dough improvement, in addition to providing new information on grain proteins [46]. In related research, P. Joudrier, M.-F. Gautier, F. de Lamotte and colleagues have successfully pursued the cloning of the wheat thioredoxin h gene and characterized its protein product [32]. During the same period, a team led by Y. Meyer in Perpignan initiated a comprehensive study of plant thioredoxins at both the gene and protein levels. Their work has given insight into the structure and evolution of plant thioredoxin genes
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and into the function of thioredoxin h [7,52,55,57,58,62,66]. The Meyer group has also characterized the mitochondrial thioredoxin system [5,49]. Data made available through the sequencing of the Arabidopsis thaliana genome have been a great asset in their studies. Starting in the early 1990s, J.M. Lancelin in Lyon applied NMR technology to elucidate the structure of thioredoxins m and h and their associated enzymes [48,50,53]. His contributions have been central to our understanding not only of the structure, but also the mechanism of action of thioredoxins and NADP-thioredoxin reductase (NTR), the flavin enzyme catalyzing the reduction of thioredoxin h by NADPH. Not shown in Fig. 1 are the French scientists who have made important contributions on thioredoxin in investigations that initially were not directed to thioredoxin. The pursuits of C. Dumas and T. Gaude (Lyon) on fertilization in Brassica gave new insight on how thioredoxin of the stigma acts to control self-incompatibility via a protein kinase [18]. Similarly, Rey et al. (Cadarache) [56] recently uncovered a thioredoxin-like protein that acts in drought stress. Also not shown in Fig. 1 are contributing French scientists, who are no longer working in the thioredoxin field or whose projects have a different focus. These include the groups of J. Ricard and his collaborator J.-C. Meunier in Marseilles, who added information on chloroplast thioredoxins and target enzymes [65]; Clément-Métral et al. (Compiègne) [22], who laid the foundation for thioredoxin occurrence and function in photosynthetic bacteria; Balangé and Lambert (Rouen) [2], who followed a similar path and studied heme biosynthesis in these organisms; and finally G. Girault and J.M. Galmiche (Saclay), who studied the thioredoxin-linked activation of chloroplast CF1 [31]. B. Gontero, who worked earlier in Ricard’s group, has continued this line of research in Paris, where she currently investigates enzyme complexes of the Calvin cycle, including components linked to thioredoxin [1]. 3. Research contributions 3.1. Chloroplast ferredoxin/thioredoxin system Important contributions of the French school on plant thioredoxins are summarized in Table 1. Earlier results by Gadal and colleagues are reproduced in Fig. 2, which shows the purification of a protein factor required for the activation of NADP-malate dehydrogenase by DTT [43]. The identification of the protein factor as thioredoxin m is illustrated in Fig. 3, which also documents the presence of thioredoxin f in the preparation [44]. This study of thioredoxin-linked redox regulation in chloroplasts initiated by Gadal and his colleagues in Nancy in the mid 1970s, broke new ground on chloroplast thioredoxin m and set the stage for others in France and elsewhere to pursue related studies, initially on the ferredoxin/thioredoxin system and later on other problems, such as the NADP/thioredoxin counterpart and the target enzymes of both systems.
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Fig. 2. Purification of the protein factor found by Jacquot, Vidal and Gadal to be required for the activation of NADP-malate dehydrogenase by DTT. The factor was purified from a DEAE-cellulose column by applying an NaCl gradient. The experiments were carried with extracts prepared from French bean leaves (adapted from [43]). Activity of NADP-malate dehydrogenase is shown on the ordinate. The protein factor activating the enzyme peaked at fractions 10 and 11.
Fig. 3. Identification of thioredoxin m as the protein factor required for the DTT-dependent NADP-malate dehydrogenase activation. The presence of thioredoxin f was also demonstrated through its activation of fructose bisphosphatase by DTT. (C—C), NADP-malate dehydrogenase (thioredoxin m activity); (•—•), fructose bisphosphatase (thioredoxin f activity) (adapted from [44]).
The mechanism of regulation of chloroplast NADPmalate dehydrogenase has been studied extensively during the last 15 years by biochemical, genetic and structural approaches [19,25,37,45,48]. Taken together, the data explain the step-by-step activation of the enzyme. The mechanism entails the sequential reduction of the two disulfide bonds that occur in extensions at the C- and N-termini specific to the chloroplast isoform. The N-terminal disulfide helps to stabilize the inactive form of the dimer, whereas the C-terminal disulfide controls substrate access by fixing the enzyme in a position that blocks the active site. The reduction of the two regulatory disulfides thus facilitates a structural change that yields a fully active enzyme with ready substrate access to its binding site [61]. Fructose bisphosphatase, another model enzyme of thioredoxin regulation, has also been studied extensively. Amino acid sequence alignment of the enzyme from the cytosol and chloroplast showed that plastid isoforms contain an internal insertion of about 20 amino acids with three conserved cysteines. Site-directed mutagenesis experiments demonstrated that the replacement of one of these cysteines (Cys153 in pea) by a serine yielded a constitutively fully active enzyme, whereas the mutation of either one of the two
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other cysteines resulted in partial activity [42,59]. These findings led to the conclusion that the regulatory disulfide could be formed between Cys153 and either one of the two remaining cysteines (Cys173 or Cys178). However, the elucidation of the structure of pea chloroplast fructose-1,6-bisphosphatase clearly showed that a single disulfide (formed between Cys153 and Cys 173) is involved in the redox regulation of the enzyme [20]. Thus, the third conserved cysteine located near the regulatory site seems to form a bond that is an artifact associated with the mutant enzyme [4,20]. Biochemical studies mentioned above laid the foundation for the characterization of FTR, a unique type of iron-sulfur enzyme that, through its reduction of thioredoxins links light to enzyme activity [26,27]. The enzyme, whose structure and reaction mechanism have recently been solved [24], composed of two heterosubunits and was able to accept electrons from two ferredoxins via a disulfide group that, in turn, reduces the disulfide of chloroplast thioredoxins. Finally, the screening of a cDNA library of A. thaliana led to the identification of four genes coding for chloroplast thioredoxins m, and a new type of thioredoxin, x [52]. This multiplicity of proteins raises the question of their distribution and expression as well as their function. Subsequent yeast complementation experiments revealed a new putative function for m-type thioredoxin [38]. The recent work of Rey et al. [56] has uncovered a chloroplast thioredoxin-like protein (CDSP32), which was expressed in response to drought stress. Subsequent study shows that CDSPS32 together with a 2Cys peroxiredoxin functions in protection against oxidative damage [8,56].
thioredoxin h and NTR has been achieved [23,51,53]. Thioredoxin h specificity has also been characterized by using yeast complementation [7] and more recently, by linking the promoters of different thioredoxin h genes to the GUS reporter and analyzing individual plant tissues [55]. In a similar line of experiments, a new family of peroxiredoxins has been isolated in yeast two hybrid experiments [66]. Application of a procedure based on the use of a thioredoxin h mutant, in which the buried cysteine of the active site was replaced by a serine, bound a protein identified as chloroplast peroxiredoxin [34]. Using EST sequence data, Rouhier et al. [60] cloned and characterized a novel type of peroxiredoxin from poplar. The study of thioredoxin h of wheat [32] is of particular interest, owing to its potential application in the improvement of foods by lowering allergenicity [12] and enhancing dough quality [46]. Recently, the role of thioredoxin h has been extended by Dumas and Gaude in a new direction, from new data on how its earlier-observed link to a protein kinase [6] controls self-incompatibility during fertilization [18]. This work opens a new door to investigate the fertilization process. 3.3. Mitochondrial thioredoxin system Meyer and his group have identified and characterized the NTR and yet another type of thioredoxin, thioredoxin o, of plant mitochondria [3,49]. This work makes it possible to elucidate the role of thioredoxin in these organelles—a problem that surfaced when Follmann and his collaborators demonstrated that mitochondria contain a thioredoxin [5].
3.2. Cytosolic NADP/thioredoxin system Several French research groups have actively studied plant cytosolic thioredoxin h and NTR. Their efforts have resulted in the cloning of several thioredoxin h genes and the characterization of their protein products [7,33,55,57,58,62]. The resolution of the three-dimensional structure of both
4. Influence The influence of the French School, during the past 25 years, has had a profound effect on the thioredoxin field. As apparent from Table 1, French scientists have contributed
Table 1 Pathbreaking contributions on plant thioredoxins by the French School. Most of the below contributions were made by established laboratories of the French School. The findings on CDSP32 (by P. Rey) and self-incompatibility (by T. Gaude and C. Dumas) were made in research not initially directed toward thioredoxin Chloroplast ferredoxin/thioredoxin system • Early studies on thioredoxin m • Genetic and functional analysis of thioredoxin m • Characterization of ferredoxin-thioredoxin reductase • Mechanism of regulation and structure of fructose-1,6-bisphosphate phosphatase • Mechanism of regulation and structure of NADP-malate dehydrogenase • Identification of CDSP32, a thioredoxin-like chloroplastic protein, in drought stress Cytosolic NADP/thioredoxin system • Cloning, characterization and structure of thioredoxin h • Genetic, evolutionary and functional properties of thioredoxin h • Importance of thioredoxin h in cereals and its applications in biotechnology • Role of thioredoxin h in self-incompatibility in Brassica Mitochondrial NADP/thioredoxin system • Identification and characterization of NADP-thioredoxin reductase and thioredoxin o from plant mitochondria
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509
Table 2 Long-term international collaborations with the French School Collaborator Bob B. Buchanan (Berkeley)
Ana Chueca Julio Lopez-Gorge (Granada)
French counterparts P. Gadal J.-P. Jacquot M. Miginiac-Maslow P. Decottignies M. Droux K. Kobrehel J.-P. Jacquot M. Miginiac-Maslow
Cooperative research Properties of members of the ferredoxin/thioredoxin system and target enzymes Thioredoxin biotechnology Properties of target enzymes Fig. 4. Current research on plant thioredoxins by the French School.
Hans Eklund (Uppsala) J.-P. Jacquot M. Miginiac-Maslow E. Issakidis-Bourguet David B. Knaff J.-P. Jacquot (Lubbock) M. Miginiac-Maslow Y. Meyer Peter Schürmann (Neuchâtel)
P. Gadal J. Vidal J.-P. Jacquot
Structure of NTR and NADP-MDH Physical characterization of proteins associated with the ferredoxin/thioredoxin system Functional properties of thioredoxin and target enzymes; key review article
seminal information on the ferredoxin/thioredoxin system (thioredoxin m, FTR) and target enzymes (NADP-malate dehydrogenase, fructose bisphosphatase). Similar advances have been made with the NADP/thioredoxin system, including key contributions not only on the structure and function of thioredoxin h and NTR, but also on the novel system recently identified in mitochondria. These achievements have been amplified by conferences hosted or co-hosted by the French School—first the International Conference on Thioredoxin held in Berkeley in 1981 (followed up with a book of the proceedings edited by Gadal [30]), and later, the 1990 Jacques Monod Conference on Thioredoxins and Glutaredoxins held in Roscoff. The contributions in Table 1 and the conferences, however, tell only part of the story. Results obtained in long-term international collaborations (Table 2) have extended the findings made in France and moved the field in decisive new directions. In addition to promoting science, these collaborations have led to countless exchange visits and lasting friendships between French scientists and the international thioredoxin community. 5. Future prospects Patrick Henry, an illustrious Virginian and an ardent supporter of independence, made reference to the future of the colonies in a well-known speech, given at the dawn of the American Revolution: “I have but one lamp by which my feet are guided, and that is the lamp of experience. I know no way of judging the future but by the past.” [35]
From this perspective, it is appropriate to examine the research on plant thioredoxins that has been or is being carried out in France. Past research is summarized above and ongoing work is identified in Fig. 4. The projects cover a broad range, including the studies of both the ferredoxin/ thioredoxin and NADP/thioredoxin systems as well as pertinent target enzymes. Furthermore, the laboratories continue to apply approaches based on biochemistry, physiology, genetics, structure, biotechnology and agronomy that span the biological spectrum. Past experience coupled with the new talent entering the field bode well for a rich future for thioredoxin research in France. 6. Reflections It seems fitting to close this tribute on a personal note. One of us (B.B.B.) has interacted closely with Pierre Gadal for 25 years on both a personal and scientific basis. This association was enriched by B.B.B.’s spending a part of two sabbatical leaves (1984, 1991) in Orsay and, during most of this period, by annual visits to his laboratory. In 1984, he was accompanied by his wife, Melinda, and four daughters, who had a truly memorable visit as a result of the gracious hospitality of the members of the Orsay laboratory and the Gadal family. Ferried by a new Peugeot 505 wagon (now in Berkeley), the Buchanans enjoyed guided trips to historic French sites and a long weekend at the Gadal’s home in Brittany. It was a pleasure during these visits to witness Pierre, in collaboration with Francis Quétier, turn what initially was a dream into a grand structure that today houses the Institut de Biotechnologie des Plantes—a leading group in plant biology research. The trips to Orsay were also often associated with gratifying academic activities—e.g., seminars either in-house or at neighboring laboratories and service as an external examiner on doctoral thesis committees, such as the one for Akira Suzuki, whose research dealt with nitrogen metabolism, another of Gadal’s long-term interests. Invariably provided were opportunities to meet and interact with foreign visitors, including North American colleagues, such as Ann Oaks, Ray Chollet and David Knaff. As noted above, the transatlantic trips from California were complemented by reciprocal visits to Berkeley by Pierre and members of his
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laboratory. Pierre’s visits stand out as being particularly pleasant and productive: one of his longer stays resulted in a paper on glutamine synthetase—a favorite topic [28]—and provided an opportunity for him to attend the US Japan Seminar on Environmental Plant Stress in Fairbanks, Alaska. Finally, a traditional part of B.B.B.’s trips to Orsay included social activities integrated into each visit, irrespective of its duration. In addition to daily swims in the Orsay pool and countless activities arranged by different members of the laboratory, the visits included the incomparable dinners hosted at the Gadal home and the memorable tea held religiously each afternoon around four o’clock that was attended by all the members of the laboratory. On special occasions, everyone enjoyed delectable pastries available only in France, including for one celebration of American Independence (July 4), cakes from Lenôtre in Paris. The informal atmosphere at these gatherings encouraged lively discussions on topics that ranged from science to contemporary American television soap operas. Congeniality combined with exciting science made visits to Orsay unforgettable.
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The authors wish to thank the Federation of the European Biochemical Societies for permission to reprint Figs. 2 and 3 (Jacquot et al. “Identification of a Protein....”, FEBS Lett. 71 (1976) 223-246 and Jacquot et al. “Evidence for several enzyme...”, FEBS Lett. 96 (1978) 243-246).
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