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Dr. James O. Berry BERRY

Professor
Office: Cooke 355
Office Hours: Monday, Wednesday, Friday 11:00am – 12 noon
Tel: (716) 645-4997
E-mail: camjob@buffalo.edu

Research Summary

Our main research project is photosynthetic gene expression in C4 plants

Rubisco: Our research is focused on the expression of genes that encode Ribulose 1,5-bisphophate carboxylase/oxygenase (abbreviated as Rubisco) in plants that utilize the highly efficient C4 pathway of photosynthesis. Rubisco is the principle enzyme of photosynthetic carbon fixation in all plants, and is central to their viability, growth, and productivity. Located within the chloroplasts, it consists of eight large (LSU) and eight small (SSU) subunits. The rbcL gene encoding the LSU is transcribed and translated within the chloroplasts. The SSU, encoded by a nuclear RbcS gene family, is translated on cytoplasmic ribosomes as a precursor that is transported into the chloroplasts. Within chloroplasts, the two subunits combine to form the functional L8S8 Rubisco holoenzyme.

C4 Photosynthesis: Plants that use the C4 pathway of photosynthesis (C4 plants) have much higher rates of photosynthetic productivity than plants that utilize the more common and less efficient C3 pathway (C3 plants). C4 plants account for about a fourth of the primary productivity of earth’s biosphere, and yet only about 5% of terrestrial plant species actually use this pathway for photosynthetic carbon fixation. In addition to increased productivity, advantages associated with C4 photosynthesis include greater water use efficiency, enhanced nitrogen-use efficiency, and increased adaptability to marginal environments. These advantages allow C4 plants to thrive in areas of high temperature and/or low water availability, where the viability of C3 plants can be severely limited. The C4 pathway occurs across a wide variety of plant species and has evolved independently many times.

C4 photosynthesis incorporates novel leaf anatomy, metabolic specializations, and modified gene expression. C4 plants typically possess a distinctive Kranz (or wreath) leaf anatomy that consists of two morphologically and functionally distinct photosynthetic cell types, the bundle sheath (BS) and mesophyll (M) cells. Within M cells, C4 species utilize phosphoenolpyruvate carboxylase (PEPCase) as the initial primary CO2 fixation enzyme leading to the production of C4 acids in a first stage of photosynthetic reactions. In a second stage that occurs only in BS cells, decarboxylation of the C4 acids releases CO2, followed by the subsequent re-fixation of released CO2 by Rubisco (Calvin-Benson cycle). By separating these two photosynthetic stages, and partitioning Rubisco specifically within BS cells, C4 plants reduce or eliminate the photosynthetically wasteful reactions of photorespiration, thereby greatly enhancing their CO2 fixation ability.

An RNA binding protein that regulates Rubisco gene expression in C4 and C3 plants: In spite of the clearly defined biological parameters and advantages associated with C4 plants, molecular mechanisms responsible for C3 versus C4 photosynthetic gene expression patterns have remained highly elusive for many years. We have recently isolated a novel mRNA binding protein, the RBCL RNA S1-BINDING DOMAIN protein (RLSB), from chloroplasts of a C4 plant. This protein, encoded by the nuclear RLSB gene, is present and highly conserved among a wide variety of plant species. Co-localized with LSU to chloroplasts, RLSB is highly conserved across many plant species. Most significantly, RLSB localizes specifically to the Rubisco-containing BS cells in the leaves of C4 plants. Comparative functional analysis using maize (a C4 plant) and Arabidopsis (a C3 plant) reveals its tight association with rbcL gene expression in both species.

Our current findings indicate that specific binding of RLSB to rbcL mRNA and associated activation of rbcL gene expression within BS chloroplasts may be one determinant leading to the characteristic cell type-specific localization of Rubisco in C4 plants. Evolutionary modification of RLSB expression, from a C3 “default” state to BS cell-specificity, may represent one mechanism by which rbcL expression has become restricted to only one cell type in C4 plants.

Agricultural significance: Our ongoing research seeks to understand the mechanisms by which RLSB regulates the expression of rbcL gene expression in chloroplasts. Ultimately, regulatory processes such as this underlie the cell-type specific patterns of gene expression, the enhanced photosynthetic capabilities, and the environmental adaptability that characterize C4 plants. By integrating the use of advanced molecular biology and biochemistry methods, together with transgenic plants, state-of-the art confocal microscopy, and advanced genetic tools, we are uncovering exciting new insights into the molecular basis of C4 photosynthesis. This research has exciting prospects for agricultural development. Ultimately, our research may determine if the exploitation of RLSB can be used to enhance photosynthetic efficiency, thereby increasing biomass productivity of maize and other vital crop plants used for the production and food and biofuel.

Collaborative projects: The many experimental tools and multiple levels of analysis developed and used in our laboratory have been applied to a number of collaborative projects. Our most recent collaboration resulted in a series of studies to determine the effects of agricultural antibiotic wastes on plant viability, and the possible use of some plants for natural soil remediation to eliminate such contaminants (with Diana Aga, Dept. of Chemistry, UB). We have also contributed to studies on plant-virus interactions using Cucumber Mosiac Virus (CMV) (with John Carr, Dept. of Plant Sciences, Univ. of Cambridge, UK), Nitrate transporter genes (with LiPing Yin, Capital Normal University, Beijing), Regeneration in plant tissue culture (with Minesh Patel), and a novel regulator of chloroplast gene expression in response to plant stress (with V.J. Hernandez, formerly of the UB Dept. of Microbiology).

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Recent Publications

  • Yerramsetty, P., M. Stata, R. Silford, T.L. Sage, R.F. Sage, G.K.-S. Wong, V.A. Albert, and J.O. Berry.  2016.  Evolution of RLSB, a nuclear-encoded S1 domain RNA binding protein associated with post-transcriptional regulation of plastid-encoded rbcL mRNA in vascular plants.  BMC Evolutionary Biology 16:141.  10.1186/s12862-016-0713-1
  • Koteyeva, N.K., E.V. Voznesenskaya, J.O. Berry, A.B. Cousins, and G.E. Edwards.  2016.  The unique structural and biochemical development of single cell C4 photosynthesis along longitudinal leaf gradients in Bienertia sinuspersici and Suaeda aralocaspica (Chenopodiaceae).  Journal of Experimental Botany 67:2587-2601.  doi: 10.1093/jxb/erw082.
  • Berry, J.O., P. Yerramsetty, and C.M. Mure.  2016.  Regulation of Rubisco gene expression in C4plants.  Current Opinion in Plant Biology 31:23-28.  doi 10.1016/j.pbi.2016.03.004.
  • Garner, D.M.G., C.M. Mure, P. Yerramsetty, and J.O. Berry.  2016.  Kranz anatomy and the C4 pathway.  In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net doi: 10.1002/9780470015902.a0001295.pub3
  • Li, Shuang Li, X. Zhang, X.-Y. Zhang, W. Xiao, J.O. Berry, P. Li, S. Jin, S. Tan, P. Zhang, W.-Z. Zhao, and L.-P. Yin.  2015.  Expression of Malus xiaojinensis IRT1 (MxIRT1) protein in transgenic yeast cells leads to degradation through autophagy in the presence of excess iron.  Yeast 32:499-517 10.1002/yea.3075
  • Shuang, L., X.-X. Pan, J.O. Berry, Y. Wang, Naren, S. Ma, S. Tan, X. Xiao, W-Z. Zhao, X.- Z. Song, X.-Y. Sheng, and L.-P. Yin.  2015.  OsSEC24, a functional SEC24-like protein in rice, improves tolerance to iron deficiency and high pH by enhancing H+ secretion mediated by PM-H+-ATPase.  Plant Science 233: 61-71  10.1016/j.plantsci.2015.01.001 
  • Zhang, P., S. Tan, J.O. Berry, P. Li, Naren, L. Shuang, G. Yang, W.-B. Wang, X.-T. Qi, and L.-P. Yin. 2014. An uncleaved signal peptide directs the Malus xiaojinensis iron transporter protein Mx IRT1 into ER for the PM secretory pathway. Int. J. Mol. Sci. 15: 20413-20433 (doi:10.3390/ijms151120413)
  • Rosnow, J, Yerramsetty P, Berry, JO, Okita TW, and Edwards GE 2014. Exploring mechanisms linked to differentiation and function of dimorphic chloroplasts in the single cell C4 species Bienertia sinuspersici. BMC Plant Biology 14, 34 doi:10.1186/1471-2229-14-34.
  • Bowman SM, Patel M, Yerramsetty P, Mure C, Zielinski AM, Bruenn JA, Berry, JO, 2013. A novel RNA binding protein affects rbcL gene expression and is specific to bundle sheath chloroplasts in C4 plants. BMC Plant Biology 13,138. doi:10.1186/1471-2229-13-138.

     

    *This article was highlighted in “Biome”, in a synopsis under the heading “Photosynthetic divisions”: http://www.biomedcentral.com/biome/regulating-rubisco-insights-into-the-molecular-basis-of-photosynthesis/

    *Identified as Highly Accessed

    *Recommended by Faculty of 1000: http://f1000.com/prime/718117974?bd=1&ui=12681

  • Berry, J.O., P. Yerramsetty, C. Mure, and A.M. Zielinski. 2013. Photosynthetic gene expression in higher plants. doi 10.1007/s11120-013-9880-8. This is an invited review for a special issue of Photosynthesis Research, focusing on “Photosynthesis Education”.
  • Bowman, S.M., K.D. Drzewiecki, E.-R. Mojica, A.M. Zielinski, A. Siegel,, D.A. Aga, and J.O. Berry  2011.  Toxicity and reductions in intracellular calcium levels following?uptake of a tetracycline antibiotic in ArabidopsisEnvironmental Science &Techology 45:8958-8964
  • Berry, J.O., A.M. Zielinski, and M. Patel,  2011.  Gene expression in mesophyll and bundle sheath cells of C4 plants.  In: A.S. Raghavendra and R.F. Sage (Eds.) C4 Photosynthesis and Related CO2 Concentrating Mechanisms.  Advances in Photosynthesis and Respiration.  Volume 32.   Springer, Dordrecht, The Netherlands, pp 221-256. 
  • Koteyeva. N.K., E.V. Voznesenskaya, S.D.X. Chuong, J.O. Berry, V.R. Franceschi, and G.E. Edwards.  2011.  Development of structural and biochemical characteristics of C4 photosynthesis in two Kranz anatomy subtypes in genus Suaeda (family Chenopodiaceae).  Journal of Experimental Botany 62:3197-3212. 
  • Farkas, M.H., E.-R. Mojica, M.Patel, D.S. Aga, and J. O. Berry.  2009.  Development of a rapid biolistic assay to determine changes in relative levels of intracellular calcium in leaves following tetracycline uptake by pinto bean plants.  The Analyst 134:1594-1600. 
  • Patel M and J.O. Berry.  2008.  Rubisco gene expression in C4 plants.  Journal of Experimental Botany 59:1625-1634.
  • Berry, J.O.  and M. Patel.  2008.  Kranz anatomy and the C4 pathway.  In:  Encyclopedia of Life Sciences, http://onlinelibrary.wiley.com/doi/10.1002/9780470015902.a0001295.pub2/abstract John Wiley & Sons, Ltd, Chichester UK. 
  • Yin, L.-P., P. Lia, B. Wen, D.J. Taylor, and J.O. Berry.  2007.  Characterization and expression of a high-affinity nitrate system transporter gene (TaNRT2.1) from wheat roots, and its evolutionary relationship to other NTR2 genes.  Plant Science 172:621-631.
  • Ziebell H., T. Payne, J.O. Berry, J.A. Walsh and J.P. Carr  2007.  A cucumber mosaic virus mutant lacking the 2b counter-defence protein gene provides protection against wild- type strains.  Journal of General Virology 88: 2862-2871.   Farkas M, J.O. Berry, and D.S. Aga  2007.  Determination of enzyme kinetics and glutathione conjugates of chlortetracycline and chloroacetanilides using liquid chromatography–mass spectrometry.  The Analyst 132:664–671.  * featured on the inner cover
  • Farkas, M., J.O. Berry and D. Aga. 2007. Chlortetracycline detoxification in maize via induction of glutathione s-transferases after antibiotic exposure.  Environmental Science&Technology 41: 1450-1456.
  • Patel, M., A. Siegel, and J.O. Berry.  2006.  Untranslated regions of FbRbcS1 mRNA mediate bundle sheath cell-specific gene expression in leaves of C4 Flaveria bidentisJournal of Biological Chemistry 281: 25485 – 25491. 
  • Patel, M., N.L. Darvey, D.R. Marshall, and J.O. Berry.  2004.  Optimization of media for improved plant regeneration efficiency from wheat microspore culture.  Euphytica 140:197-204. 
  • Givens, R.M., M.-H. Lin, D.J. Taylor, U. Mechold, J.O. Berry*, and V.J. Hernandez*.   2004.  Inducible Expression, Enzymatic Activity, and Origin of Higher Plant Homologues of Bacterial RelA/SpoT stress proteins in Nicotiana tabaccum J. Biol. Chem. 279:7495-7504.  * both authors contributed equally to this work.
  • Patel, M., A.C. Corey, L.-Y. Yin, S. Ali, W.C. Taylor, and J.O. Berry.  2004.  Untranslated regions from C4 amaranth AhRbcS1 mRNAs confer translational enhancement and preferential bundle sheath cell expression in transgenic C4 Flaveria bidentisPlant Physiology 136:3550–3561.