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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Expression profiling and proteomic analysis of isolated photosynthetic cells of the non-Kranz C4 species Bienertia sinuspersici

Joonho Park A , Thomas W. Okita B and Gerald E. Edwards A C
+ Author Affiliations
- Author Affiliations

A School of Biological Sciences, Washington State University, Pullman, WA 99164-4236, USA.

B Institute of Biological Chemistry, Washington State University, Pullman, WA 99164-6340, USA.

C Corresponding author. Email: edwardsg@wsu.edu

Functional Plant Biology 37(1) 1-13 https://doi.org/10.1071/FP09074
Submitted: 4 April 2009  Accepted: 8 September 2009   Published: 5 January 2010

Abstract

Bienertia sinuspersici Akhani represents one form of C4 photosynthesis that occurs without Kranz anatomy in family Chenopodiaceae. Analysis of transcript profiles and proteomics were made to gain information on this single-cell C4 photosynthetic mechanism. Chlorenchyma cells were isolated and purified from mature leaves. From these cells, a cDNA library was made from which sequences were obtained on 2385 clones using conventional methods. To obtain a protein profile, the multi dimensional protein identification technique was used, resulting in identification of 322 unique proteins in chlorenchyma cells. After analysing datasets from the EST library and proteomics, genes and proteins were classified into 23 and 17 categories according to types of biological processes, respectively. These include photosynthesis and photorespiration, other biosynthetic and metabolic processes, cell wall modification, defence response, DNA repair, electron transport, other cellular and developmental processes, protein folding, protein targeting, protein modification, proteolysis, redox and ion homeostasis, response to biotic and abiotic stresses, RNA modification, transcription, translation, transport and unknowns. Sequence and phylogenetic analyses were made of C4 cycle enzymes to characterise the relationship between homologues found in Bienertia with public gene sequences from other chenopods and representative C3 and C4 species from other families. Identified photosynthetic genes and proteins are discussed with respect to the proposed function of an NAD-ME type C4 cycle in this single-cell C4 system.

Additional keywords: EST library, photosynthesis, proteomics.


Acknowledgements

This material is based upon work supported by the National Science Foundation under Grants IBN-0236959 and IBN-0641232. The authors thank Mr. Abdulrahman Alsirhan for providing seeds of Bienertia sinuspersici from Kuwait. We thank C. Cody for plant growth management and E. Roalson for advice on phylogenetics.


References


Akhani H, Barroca J, Koteeva N, Voznesenskaya E, Franceschi V, Edwards G, Ghaffari SM, Ziegler H (2005) Bienertia sinuspersici (Chenopodiaceae): a new species from Southwest Asia and discovery of a third terrestrial C4 plant without Kranz anatomy. Systematic Botany 30, 290–301.
Crossref | GoogleScholarGoogle Scholar | open url image1

Anisimova M, Gascuel O (2006) Approximate likelihood ratio test for branches: a fast, accurate and powerful alternative. Systematic Biology 55, 539–552.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Bayer EM, Bottrill AR, Walshaw J, Vigouroux M, Naldrett MJ, Thomas CL, Maule AJ (2006) Arabidopsis cell wall proteome defined using multidimensional protein identification technology. Proteomics 6, 301–311.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Berry J, McCormac D, Long J, Boinski JJ, Corey A (1997) Photosynthetic gene expression in amaranth, an NAD–ME type C4 dicot. Australian Journal of Plant Physiology 24, 423–428.
Crossref | GoogleScholarGoogle Scholar | open url image1

Breci L, Haynes PA (2007) Two-dimensional nanoflow liquid chromatography-tandem mass spectrometry of proteins extracted from rice leaves and roots. Methods in Molecular Biology (Clifton, N.J.) 355, 249–266.
PubMed |
open url image1

Castresana J (2000) Selection of conserved blocks for multiple alignments for their use in phylogenetic alignments. Molecular Biology and Evolution 17, 540–552.
PubMed |
open url image1

Chevenet F, Brun C, Banuls AL, Jacq B, Christen R (2006) TreeDyn: towards dynamic graphics and annotations for analyses of trees. BMC Bioinformatics 7, 439.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Christin PA, Salamin N, Savolainen V, Duvall MR, Besnard G (2007) C4 photosynthesis evolved in grasses via parallel adaptive genetic changes. Current Biology 17, 1241–1247.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Christin PA, Besnard G, Samaritani E, Duvall MR, Hodkinson TR, Savolainen V, Salamin N (2008) Oligocene CO2 decline promoted C4 photosynthesis in grasses. Current Biology 18, 37–43.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Christin PA, Salamin N, Kellogg EA, Vicentini A, Besnard G (2009a) Integrating phylogeny into studies of C4 variation in the grasses. Plant Physiology 149, 82–87.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Christin PA, Petitpierre B, Salamin N, Büchi L, Besnard G (2009b) Evolution of C4 phosphoenolpyruvate carboxykinase in grasses, from genotype to phenotype. Molecular Biology and Evolution 26, 357–365.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Chuong SD, Franceschi VR, Edwards GE (2006) The cytoskeleton maintains organelle partitioning required for single-cell C4 photosynthesis in Chenopodiaceae species. The Plant Cell 18, 2207–2223.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Drincovich MF , Lara MV , Maurino VG , Andreo CS (2009) C4 decarboxylases: different solutions for the same biochemical problem, the provision of CO2 in the bundle sheath cells. In ‘Photosynthesis and related CO2 concentrating mechanisms’. Advances in Photosynthesis Research series, (Eds A. Raghavendra, R. Sage) (Kluwer: The Netherlands), in press.

Edgar RC (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 32, 1792–1797. open url image1

Edwards GE , Walker DA (1983) ‘C3, C4: mechanisms, and cellular and environmental regulation, of photosynthesis.’ (Blackwell Scientific Publications: Oxford, UK)

Edwards GE, Franceschi VR, Voznesenskaya EV (2004) Single-cell C4 photosynthesis versus the dual-cell (Kranz) paradigm. Annual Review of Plant Biology 55, 173–196.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Fabre N, Reiter IM, Becuwe-Linka N, Genty B, Rumeau D (2007) Characterization and expression analysis of genes encoding α and β carbonic anhydrases in Arabidopsis. Plant, Cell & Environment 30, 617–629.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Fett JP, Coleman JR (1994) Characterization and expression of two cDNAs encoding carbonic anhydrase in Arabidopsis thaliana. Plant Physiology 105, 707–713.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Flanigan YS, Critchley C (1996) Light response of D1 turnover and photosystem II efficiency in the seagrass Zostera capricorni. Planta 198, 319–323.
Crossref | GoogleScholarGoogle Scholar | open url image1

Froehlich JE, Wilkerson CG, Ray WK, McAndrew RS, Osteryoung KW, Gage DA, Phinney BS (2003) Proteomic study of the Arabidopsis thaliana chloroplastic envelope membrane utilizing alternatives to traditional two-dimensional electrophoresis. Journal of Proteome Research 2, 413–425.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Futcher B, Latter GI, Monardo P, McLaughlin CS, Garrels JI (1999) A sampling of the yeast proteome. Molecular and Cellular Biology 19, 7357–7368.
PubMed |
open url image1

Glackin CA, Grula JW (1990) Organ-specific transcripts of different size and abundance derive from the same pyruvate, orthophosphate dikinase gene in maize. Proceedings of the National Academy of Sciences of the United States of America 87, 3004–3008.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Guindon S, Gascuel O (2003) A simple, fast and accurate algorithm to estimate larges phylogenies by maximum likelihood. Systematic Biology 52, 696–704.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Haberlandt G (1896) ‘Physiologische Pflanzenanatomie.’ (Wilhelm Engelman: Leipzig)

Hatch MD (1987) C4 photosynthesis: a unique blend of modified biochemistry, anatomy and ultrastructure. Biochimica et Biophysica Acta 895, 81–106. open url image1

Hatch MD, Burnell JN (1990) Carbonic anhydrase activity in leaves and its role in the first step of C4 photosynthesis. Plant Physiology 93, 825–828.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Hatch MD , Osmond CB , Slatyer RO (1971) ‘Photosynthesis and photorespiration.’ (Wiley Interscience: New York)

Huffaker RC, Peterson LW (1974) Protein turnover in plants and possible means of its regulation. Annual Review of Plant Physiology 25, 363–392.
Crossref | GoogleScholarGoogle Scholar | open url image1

Imaizumi N, Ku MSB, Ishihara K, Samejima M, Kaneko S, Matsuoka M (1997) Characterization of the gene for pyruvate, orthophosphate dikinase from rice, a C3 plant, and a comparison of structure and expression between C3 and C4 genes for this protein. Plant Molecular Biology 34, 701–716.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ku MSB, Edwards GE (1975) Photosynthesis in mesophyll protoplasts and bundle sheath cells of various types of C4 plants V. Enzymes of respiratory metabolism and energy utilizing enzymes of photosynthetic pathways. Zeitschrift für Pflanzenphysiologie 77, 16–32. open url image1

Lara MV, Chuong SDX, Akhani H, Andreo CS, Edwards GE (2006) Species having C4 single-cell-type photosynthesis in the Chenopodiaceae family evolved a photosynthetic phosphoenolpyruvate carboxylase like that of Kranz-type C4 species. Plant Physiology 142, 673–684.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Lara MV, Offermann S, Smith M, Andreo CS, Edwards GE (2008) Leaf development in the single-cell C4 system in Bienertia sinuspersici: expression of genes and peptide levels for C4 metabolism in relation to chlorenchyma structure under different light conditions. Plant Physiology 148, 593–610.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Lee J, Garrett WM, Cooper B (2007) Shotgun proteomic analysis of Arabidopsis thaliana leaves. Journal of Separation Science 30, 2225–2230.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Majeran W, van Wijk KJ (2009) Cell-type-specific differentiation of chloroplasts in C4 plants. Trends in Plant Science 14, 100–109.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Majeran W, Cai Y, Sun Q, van Wijk KJ (2005) Functional differentiation of bundle sheath and mesophyll maize chloroplasts determined by comparative proteomics. The Plant Cell 17, 3111–3140.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Martineau B, Taylor WC (1986) Cell-specific photosynthetic gene expression in maize determined using cell separation techniques and hybridization in situ. Plant Physiology 82, 613–618.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Matsuoka M (1995) The gene for pyruvate orthophosphate dikinase in C4 plants: structure, regulation and evolution. Plant & Cell Physiology 36, 937–943.
PubMed |
open url image1

Monson RK (2003) Gene duplication, neofunctionalization, and the evolution of C4 photosynthesis. International Journal of Plant Sciences 164(Suppl. 3), S43–S54.
Crossref | GoogleScholarGoogle Scholar | open url image1

Moroney JV, Bartlett SG, Samuelsson G (2001) Carbonic anhydrase in plants and algae. Plant, Cell & Environment 24, 141–153.
Crossref | GoogleScholarGoogle Scholar | open url image1

Park J, Knoblauch M, Okita TW, Edwards GE (2009a) Structural changes in the vacuole and cytoskeleton are key to development of the two cytoplasmic domains supporting single-cell C4 photosynthesis in Bienertia sinuspersici. Planta 229, 369–382.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Park J, Okita TW, Edwards GE (2009b) Salt tolerant mechanisms in single-cell C4 species Bienertia sinuspersici and Suaeda aralocaspica (Chenpodiaceae). Plant Science 176, 616–626.
Crossref | GoogleScholarGoogle Scholar | open url image1

Ramsperger VC, Summers RG, Berry JO (1996) Photosynthetic gene expression in meristems and during initial leaf development in a C4 dicotyledonous plant. Plant Physiology 111, 999–1010.
PubMed |
open url image1

Sage RF (2004) The evolution of C4 photosynthesis. New Phytologist 161, 341–370.
Crossref | GoogleScholarGoogle Scholar | open url image1

Sahrawy M, Chueca A, Hermoso R, Lazaro JJ, López Gorgé J (1990) Role of light in the biosynthesis and turnover of photosynthetic fructose-1,6-bisphosphatase in pea (Pisum sativum L.) seedlings. New Phytologist 115, 603–608.
Crossref | GoogleScholarGoogle Scholar | open url image1

Sawers RJ, Liu P, Anufrikova K, Hwang JT, Brutnell TP (2007) A multi-treatment experimental system to examine photosynthetic differentiation in the maize leaf. BMC Genomics 8, 12.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Sheen J (1991) Molecular mechanisms underlying the differential expression of maize pyruvate, orthophosphate dikinase genes. The Plant Cell 3, 225–245.
Crossref | PubMed |
open url image1

Sheen J (1999) C4 gene expression. Annual Review of Plant Physiology and Plant Molecular Biology 50, 187–217.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Son D, Sugiyama T (1992) Molecular cloning of an alanine aminotransferase from NAD–malic enzyme type C4 plant Panicum miliaceum. Plant Molecular Biology 20, 705–713.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Son D, Jo J, Sugiyama T (1991) Purification and characterization of alanine aminotransferase from Panicum miliaceum leaves. Archives of Biochemistry and Biophysics 289, 262–266.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Svensson P, Blasing OE, Westhoff P (2003) Evolution of C4 phosphoenolpyruvate carboxylase. Archives of Biochemistry and Biophysics 414, 180–188.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Taniguchi M, Sawaki H, Sasakawa H, Hase T, Sugiyama T (1992) Cloning and sequence analysis of cDNA encoding aspartate aminotransferase isozymes from Panicum miliaceum L., a C4 plant. European Journal of Biochemistry 204, 611–620.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Tanz SK, Tetu SG, Vella NGF, Ludwig M (2009) Loss of the transit peptide and an increase in gene expression of an ancestral chloroplastic carbonic anhydrase were instrumental in the evolution of the cytosolic C4 carbonic anhydrase in Flaveria. Plant Physiology 150, 1515–1529.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Tetu SG, Tanz SK, Vella N, Burnell JN, Ludwig M (2007) The Flaveria bidentis b-carbonic anhydrase gene family encodes cytosolic and chloroplastic isoforms demonstrating distinct organ-specific expression patterns. Plant Physiology 144, 1316–1327.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Tiwari A, Kumar P, Singh S, Ansari S (2005) Carbonic anhydrase in relation to higher plants. Photosynthetica 43, 1–11.
Crossref | GoogleScholarGoogle Scholar | open url image1

Voznesenskaya EV, Franceschi VR, Kiirats O, Artyusheva EG, Freitag H, Edwards GE (2002) Proof of C4 photosynthesis without Kranz anatomy in Bienertia cycloptera (Chenopodiaceae). The Plant Journal 31, 649–662.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Voznesenskaya EV, Koteyeva NK, Chuong SDX, Akhani H, Edwards G, Franceschi V (2005) Differentiation of cellular and biochemical features of the single-cell C4 syndrome during leaf development in Bienertia cycloptera (Chenopodiaceae). American Journal of Botany 92, 1784–1795.
Crossref | GoogleScholarGoogle Scholar | open url image1

Wyrich R, Dressen U, Brockmann S, Streubel M, Chang C, Qiang D, Paterson AH, Westhoff P (1998) The molecular basis of C4 photosynthesis in sorghum: isolation, characterization and RFLP mapping of mesophyll- and bundle-sheath-specific cDNAs obtained by differential screening. Plant Molecular Biology 37, 319–335.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1