Professor Bob Buchanan
Bob B. Buchanan
Redox Regulation in Microorganisms, Cereal Improvement
Professor, Executive Associate Dean College of Natural Resources
411 Koshland Hall
Berkeley, California 94720-3102
Phone 510.642.3590
Lab Phone 510.642.9799

Ph.D.  Microbiology    Duke University, 1962
B.A.  Emory and Henry College, 1958

CV

My current research focuses on thioredoxin and is carried out collaboratively. We study (1) The diversity of thioredoxin and its role in redox regulation, emphasizing anaerobic archaea and bacteria as well as oxygenic photosynthetic prokaryotes, and (2) Applying thioredoxin to improve the quality and yield of cereals.

Thioredoxin (Trx) is a disulfide protein found in all types of living cells. Discovered as an electron donor for ribonucleotide reductase, Trx has since been found to play a regulatory role in a spectrum of processes throughout biology. The protein is also finding a place in medicine and biotechnology.

My Main Projects:
  • Diversity of Trx systems with an emphasis on their role in anaerobic archaea and bacteria and oxygenic photosynthetic prokaryotes. 

            Biswarup Mukhopadhyay (Virginia Tech)
                    www.vbi.vt.edu/faculty/personal/Biswarup_Mukhopadhyay

            Monica Balsera (CSIC, Salamanca, Spain) 
                    www.irnasa.csic.es

            Peter Schürmann (Université de Neuchâtel)
  • Improvement in cereal quality and yield by Trx:
    Peggy G. Lemaux (UC Berkeley)
 
My long-term collaborator, Joshua Wong, is a mainstay in both of the projects. William H. Vensel of the Western Regional Research Center, Albany, CA, is also a longstanding collaborator.
 
I have also recently collaborated with Professor Andrew Benson on producing a video on the historic photosynthesis experiments he carried out in Berkeley in the 1940's and 50's with the late Melvin Calvin. Link to Andrew Benson Video.

Research

Evolution of Redox Regulation
 
As our most recent research has been in this area, we will highlight this aspect of the work.
 
Background. The regulatory role of Trx was uncovered in studies on photosynthesis initiated 45 years ago in our laboratory (Buchanan et al., 1967). Trx was found to function as a part of a multiprotein regulatory mechanism (ferredoxin/thioredoxin system) that links light to the activity of enzymes central to the Calvin-Benson cycle in chloroplasts (Figure 1) (Wolosiuk and Buchanan, 1977).
Ferredoxin/Thioredoxin System of Oxygenic Photosynthesis
Trx acts via thiol/disulfide exchange (Holmgren, 1979). Trx reduced in the light via ferredoxin and ferredoxin-thioredoxin reductase (FTR), in turn, reduces target enzymes, leading to their activation of biosynthetic enzymes (Figure 1). Enzymes of degradation behave in the opposite manner and are deactivated by reduced Trx. Although the reductant and nature of Trx reductase can differ, this type of regulation (known as redox regulation) takes place in all types of living cells.
 
Recent work. We have obtained evidence on how Trx-linked redox regulation evolved—a longstanding question in photosynthesis and other fields (Balsera et al., 2013). It came as a surprise when genome analyses revealed that the enzyme FTR is not ubiquitous in oxygenic photosynthetic organisms. Certain early-evolving cyanobacteria appear to lack this key enzyme (Figure 2).
Evolutionary Development of Redox Regulation In Oxygenic Photosynthesis
Interestingly, an oxidative type of regulation (Balmer et al., 2003) appears to have evolved first, as a repair mechanism (Figure 3). It seems likely that oxidants other than oxygen play a role in this type of regulation. The classical light/dark type originally observed with chloroplasts developed later. Regulation by change in redox status increased in complexity as evolution progressed.
Light/Dark vs. Oxidative Regulation in Oxygenic Photosynthesis
Because FTR was long thought to be restricted to oxygenic photosynthetic cells, it came as a surprise that the enzyme also occurs in nonphotosynthetic microorganisms, bacteria and archaea (FTRc-like 2 organisms in Figure 4). For the complete list of organisms shown in Figure 4 see Balsera et al. (2013).
Aximum Likelihood Unrooted Phylogenetic Tree Showing the Evolutionary Development of Chloroplast FTR
Many of the bacteria and archaea containing FTR are deeply rooted and grow in extreme environments such as hydrothermal vents (Figure 5).
A Hydrothermal Vent: Habitat of Bacteria with FTR and the Reverse Citric Acid Cycle
Our studies suggest that the catalytic subunit of FTR (FTRc) originated in microaerophilic autotrophs and was then appeared in oxygen-evolving photosynthetic organisms, initially the prokaryotic cyanobacteria and later algae and land plants (Figure 6).
Evolutionary Development of FTR
With time the variable subunit (FTRv) was incorporated seemingly to protect the iron-sulfur cluster of FTRc against oxygen.
 
These deeply rooted microaerophiles lack the Calvin-Benson cycle and assimilate CO2 by other pathways. Organisms with FTRc utilize the reverse citric acid cycle that we originally described for photosynthetic green sulfur bacteria (Evans et al., 1966). Organisms with the reverse citric acid cycle are identified in red in Figure 6. Organisms shown in green use the Calvin-Benson cycle that is typical of oxygenic photosynthesis. As far as is known, early microaerophiles regulate the Calvin-Benson cycle allosterically independently of FTRc.
 
FTR and Trx appear to regulate the reverse citric acid cycle via the oxidative type of regulation described for chloroplasts. Evidence for a role for Trx in regulating the reverse citric acid cycle has been obtained with the green photosynthetic sulfur bacteria (Hosoya-Matsude et al., 2009). Enzymes linked to Trx are identified with a black dot in Figure 7.

TRX - Activated Enzymes of the Reverse Citric Acid Cycle
References

Balmer, Y., Koller, A., del Val, G., Manieri, W., Schürmann, P., Buchanan, B.B. (2003) Proteomics gives insight into the regulatory function of chloroplast thioredoxins. Proc. Natl. Acad. Sci. USA 100, 370-375.

Balsera, M., Uberegui, E., Susanti, D., Schmitz, R.A., Mukhopadhyay, B., Schürmann, P. and Buchanan, B.B. (2012) Ferredoxin:thioredoxin reductase (FTR) links the regulation of oxygenic photosynthesis to deeply rooted bacteria. Planta Epub before print.

Buchanan, B.B., Kalberer, P.P. and Arnon, D.I. (1967) Ferredoxin-activated fructose diphosphatase in isolated chloroplasts. Biochem. Biophys. Res. Commun. 29, 74-79.

Evans, M.C.W., Buchanan, B.B. and Arnon, D.I. (1966) A new ferredoxin-dependent carbon reduction cycle in a photosynthetic bacterium. Proc. Natl. Acad. Sci. USA 55, 928-934.

Holmgren, A. (1979) Thioredoxin catalyzes the reduction of insulin by dithiothreitol and dihydrolipoamide. J. Biol. Chem. 254, 9627-9632.

Hosoya-Matsuda N, Inoue, K and Hisabori T. (2009) Roles of thioredoxin in the obligate anaerobic green sulfur photosynthetic bacterium Chlorobaculum tepidum. Mol. Plant 2, 336-343.

Wolosiuk, R.A. and Buchanan, B.B. (1977) Thioredoxin and glutathione regulate photosynthesis in chloroplasts. Nature 266, 565-567.

Recent publications

Peer Reviewed
Hajheidari, M., Eivazi, A., Buchanan, B.B., Wong, J.H., Majidi, I. and Salekdeh, G.H. (2007) Proteomics uncovers a role for redox in drought tolerance in wheat. J. Proteome Res. 6, 1451-1460. 
 
Alkhalfioui, F., Renard, M., Vensel, W.H., Wong, J., Tanaka, C.K., Hurkman, W.J., Buchanan, B.B. and Montrichard, F. (2007) Thioredoxin-linked proteins are reduced during germination of Medicago truncatula seeds. Plant Physiol. 144, 1559-1579. 

Buchanan BB. (2007) Thioredoxin: an unexpected meeting place. Photosynth Res. 92:145-148. 

Lee SC, Lan WZ, Kim BG, Li L, Cheong YH, Pandey GK, Lu G, Buchanan BB, Luan S. (2007) A protein phosphorylation/dephosphorylation network regulates a plant potassium channel. Proc Natl Acad Sci U S A. 104:15959-15964. 

Fu A, He Z, Cho HS, Lima A, Buchanan BB, Luan S. (2007) A chloroplast cyclophilin functions in the assembly and maintenance of photosystem II in Arabidopsis thaliana. Proc Natl Acad Sci U S A. 104:15947-15952. 

Lichtenthaler HK, Buchanan BB, Douce R. (2008) Honoring Andrew Benson in Paris : a tribute on his 90th birthday. Photosynth Res. 96:181-183. 

Schürmann P, Buchanan BB. (2008) The ferredoxin/thioredoxin system of oxygenic photosynthesis. Antioxid Redox Signal. 10:1235-1274. 

Dominguez-Solis, J. R., He, Z., Lima, A., Ting, J., Buchanan, B.B., Luan S. (2008) A cyclophilin links redox and light signals to cysteine biosynthesis and stress responses in chloroplasts. Proc. Natl. Acad. Sci. USA 105, 16386-16391.

Balsera, M., Goetze, T.A., Kovács-Bogdán, E., Schürmann, P., Wagner, R., Buchanan, B.B., Soll, J., Bölter, B. (2008) Characterization of Tic110, a channel-forming protein at  the inner envelope membrane of chloroplasts, unveils a response to Ca2+ and a stromal regulatory disulfide bridge. J. Biol. Chem. 284, 2603-2616.

Wong, J. H., Lau, T., Cai, N., Singh, J., Pedersen, J. F., Vensel, W. H., Hurkman, W. J., Lemaux, P. G. and Buchanan, B. B. (2009) Digestibility of protein and starch from sorghum (Sorghum bicolor) is linked to biochemical and structural features of grain endosperm. J. Cereal Sci. 49, 73-82.

Li, Y., Ren, J., Cho, M.-J., Zhou, S., Kim, Y.-B, Guo, H., Wong, J.H., Niu, H., Kim, H.K., Morigasaki, S. , Lemaux, P.G., Frick, O.L., Yin, J. and Buchanan, B.B. (2009) The level of expression of thioredoxin is linked to fundamental properties and applications of wheat seeds. Mol. Plant 2, 430-441.

Michalska, J., Zauber, H., Buchanan, B.B., Cejudo, F.J. and Geigenberger, P. (2009) NTRC links built-in thioredoxin to light and sucrose in regulating starch synthesis in chloroplasts and amyloplasts. Proc. Natl. Acad. Sci. USA 106, 9908-9913.

Lan W., Lee, S.C., Buchanan, B.B. and Luan, S. (2009) A protein kinase-phosphatase pair interacts with an ion channel to regulate ABA signaling in plant guard cells. Proc. Natl. Acad. Sci. USA 106, 21419-21424.

Stengel, A., Benz, J.P., Buchanan, B.B., Soll, J. and Bölter, B. (2009) Preprotein import into chloroplasts via the Toc and Tic complexes is regulated by redox signals. Mol. Plant. 2, 1118-1197.

Meng, L., Wong, J.H., Feldman, L.J., Lemaux, P.G. and Buchanan, B.B. (2010) A membrane-associated thioredoxin required for plant growth moves from cell-to-cell suggestive of a role in intercellular communication. Proc. Natl. Acad. Sci. USA 107, 3900-3905.

Lan, W., Wang, W., Wang, S., Gao, J., Buchanan, B.B., Lin, H., and Luan, S. (2010) A high-affinity potassium transporter (HKT) in rice conceals a calcium-permeable cation channel. Proc. Natl. Acad. Sci. USA. 107, 7089-7094.

Meng, L., Buchanan, B.B., Feldman, L.J. and Luan, S. (2012) CLE-like (CLEL) peptides control the pattern of root growth and lateral root development in Arabidopsis. Proc. Natl. Acad. Sci. USA. 109, 1760-1765. 

Meng, L., Buchanan, B.B., Feldman, L.J. and Luan, S. (2012) A Putative Nuclear CLE-Like (CLEL) Peptide Precursor Regulates Root Growth in Arabidopsis. Mol. Plant 5, 955-957.

Wong, J.H., Pedersen, J.F., Buchanan, B.B. and Lemaux, P.G. (2012) Western Blot Analysis Uncovers Clues to Prolamin Digestibility in Raw and Cooked Meal from Sorghum and Corn. Eur. J.  Plant Sci. Biotech. 6, 56-65.

Yu, F., Qian, L., Nibau, C., Duan, Q., Kita, D., Levasseur, K.,  Li, X., Lu, C., Li, H., Hou, C., Li, L., Buchanan, B.B., Chen, L., Cheung, A.Y., Li, D. and Luan, S. (2012) FERONIA Receptor Kinase Pathway Suppresses Abscisic Acid Signaling in Arabidopsis by Activating ABI2 Phosphatase. Proc. Natl. Acad. Sci. USA. 109, 14693-14698.

Balsera, M., Uberegui, E., Susanti, D., Schmitz, R.A., Mukhopadhyay, B., Schürmann, P. and Buchanan, B.B. (2012) Ferredoxin:thioredoxin reductase (FTR) links the regulation of oxygenic photosynthesis to deeply rooted bacteria. Planta Cover Feature of Special Issue


Historical Article/Video

Buchanan, B.B., Wong, J.H. (2012) A conversation with Andrew Benson: Reflections on the discovery of the Calvin-Benson cycle. Photosyn. Res. Epub ahead of print. Link to video on youtube.

Reviews

Schürmann P. and  Buchanan B. B. (2008) The ferredoxin/thioredoxin system of oxygenic photosynthesis. Antioxid. Redox Signal. 10, 1235-1274.

Montrichard, F., Alkhalfioui, F., Yano, H., Vensel, W.H., William J. Hurkman, W. J., and Buchanan, B. B. (2008) Thioredoxin targets in plants: The first 30 years. Proteomics 72, 452-474.

Meyer, Y., Buchanan, B.B, Vignols, F. and Reichheld, J.P. (2009) Thioredoxins and Glutaredoxins: Unifying elements in redox biology. Annu. Rev. Genetics 43, 335-367.

Buchanan, B.B., Holmgren, A., Jacquot, J.-P. and Scheibe, R. (2012) Fifty years in the thioredoxin field and a bountiful harvest. Biochim. Biophys. Acta 1820, 1822-1829.

Special Issues of Journals

Buchanan, B.B., Douce, R. and Lichtenthaler, H K.  (2007) Editors, A Tribute to Andrew A. Benson, Special Issue of Photosynthesis Research, Vol. 92, No. 2, pp. 142-271.

Buchanan, B.B, Dietz, K.-J., Geigenberger, P., Jacquot, J.-P., and Schürmann, P. (2009) Editors, Special Issue on Redox Biology. Molecular Plant Vol. 2, No. 2, March 2009

Buchanan, B.B., Dietz, K.-J., Geigenberger, P., Jacquot, J.-P., and Schürmann, P. (2009) Editors, Redox Biology II Special Issue of Molecular Plant. Vol. 2, No. 3, May 2009.

Honors & Awards

Lifetime Achievement Award - Rebeiz Foundation, 2012
Honorary Professor - Nanging University, 2009
Humboldt Research Award - Alexander von Humboldt Foundation - 2007
Career Achievement Award - College of Natural Resources - 2007
Honorary Professor - Henan Agricultural University - Zhengzhou, China - 2007
Fellow - American Society of Plant Biologists - 2007
Fellow - American Academy of Microbiology - 2006
The Stephen Hales Prize - American Society of Plant Biologists - 2005
The William and Martha DeFriece Award - Emory and Henry College - 2005
Who’s Who in America - Marquis - 2004
Book Award - Association Trends - 2001
Silver Book Award - Society of National Association Publications - 2001
Endowed Lecture - Bob B. Buchanan Annual Lecture - Dept. of Plant & Microbial Biology - 2000
Distinguished Achievement Award - Emory & Henry College - 2000
Charles F. Kettering Award for Excellence in Photosynthesis - American Society of Plant Biologists (formerly Physiologists) - 1998
Fellow - American Association for the Advancement of Science - 1997
Fellow - American Academy of Arts and Sciences - 1997
Member - National Academy of Sciences - 1995
Bessenyei Medal - György Bessenyei College & Hungarian Ministry of Education - 1987
Fellowship - Organisation de Cooperation et Developpement Economiques - 1986
Senior Scientist Award - National Science Foundation - 1984
Special Creativity Award - National Science Foundation - 1982
Fellowship - Guggenheim Foundation - 1974
Fellowship - National Institutes of Health Postdoctoral - 1962
Fellowship - National Institutes of Health Predoctoral - 1960
Fellowship - Duke University – 1958-59