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

Functional Plant Biology

Volumn 37, Issue 1, 2010, Pages 1-13

  Park, Joonho ^a   Okita, Thomas W ^a   Edwards, Gerald E ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

EST library; Photosynthesis; Proteomics.

Indexed keywords

ABIOTIC STRESS; BIOLOGICAL PROCESS; CDNA LIBRARIES; CELL WALLS; CHENOPODIACEAE; CHLORENCHYMA; CONVENTIONAL METHODS; DATA SETS; DEFENCE RESPONSE; DNA REPAIR; ELECTRON TRANSPORT; EST LIBRARY; EXPRESSION PROFILING; GAIN INFORMATION; GENE SEQUENCES; ION HOMEOSTASIS; MATURE LEAVES; METABOLIC PROCESS; MULTI DIMENSIONAL; ONE-FORM; PHOTORESPIRATION; PHOTOSYNTHETIC GENES; PHYLOGENETIC ANALYSIS; PROTEIN IDENTIFICATION; PROTEIN MODIFICATIONS; PROTEIN PROFILES; PROTEIN TARGETING; PROTEOMIC ANALYSIS; PROTEOMICS;

CLONE CELLS; COMPOSITE MICROMECHANICS; GENES; MOLECULAR BIOLOGY; PHOTOSYNTHESIS; PHYSIOLOGY; PLANTS (BOTANY); PROTEIN FOLDING; RNA; TRANSCRIPTION;

BIOINFORMATICS;

ANATOMY; C4 PLANT; DICOTYLEDON; DNA; ENZYME ACTIVITY; GENE EXPRESSION; HERB; PHOTOSYNTHESIS; PHYLOGENETICS; PROTEIN; PROTEOMICS;

ACER PENSYLVANICUM; AMARANTHACEAE; BIENERTIA;

EID: 74049155841     PISSN: 14454408     EISSN: None     Source Type: Journal    
DOI: 10.1071/FP09074     Document Type: Article

References (57)

1. 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. doi: 10.1600/ 0363644054223684 (Pubitemid 40850167)
2. Anisimova M, Gascuel O (2006) Approximate likelihood ratio test for branches: a fast, accurate and powerful alternative. Systematic Biology 55, 539-552. doi: 10.1080/10635150600755453 (Pubitemid 43922340)
3. 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. doi: 10.1002/pmic.200500046 (Pubitemid 43142954)
4. 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. doi: 10.1071/PP97001
5. 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.
6. Castresana J (2000) Selection of conserved blocks for multiple alignments for their use in phylogenetic alignments. Molecular Biology and Evolution 17, 540-552.
7. 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. doi: 10.1186/1471-2105-7-439 (Pubitemid 44614263)
8. 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. doi: 10.1016/j.cub.2007.06.036 (Pubitemid 47053908)
9. 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. doi: 10.1016/j.cub.2007.11.058
10. 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. doi: 10.1104/pp.108.128553
11. Christin PA, Petitpierre B, Salamin N, Büchi L, BesnardG(2009b) Evolution of C4 phosphoenolpyruvate carboxykinase in grasses, from genotype to phenotype. Molecular Biology and Evolution 26, 357-365. doi: 10.1093/molbev/msn255
12. 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. doi: 10.1105/tpc.105. 036186 (Pubitemid 44484721)
13. 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.
14. Edgar RC (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 32, 1792-1797.
15. Edwards GE, Walker DA (1983) 'C3, C4: mechanisms, and cellular and environmental regulation, of photosynthesis.' (Blackwell Scientific Publications: Oxford, UK)
16. 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. doi: 10.1146/annurev.arplant.55. 031903.141725
17. Fabre N, Reiter IM, Becuwe-Linka N, Genty B, Rumeau D (2007) Characterization and expression analysis of genes encoding a and b carbonic anhydrases in Arabidopsis. Plant, Cell & Environment 30, 617-629. doi: 10.1111/j.1365-3040.2007.01651.x (Pubitemid 46540460)
18. Fett JP, Coleman JR (1994) Characterization and expression of two cDNAs encoding carbonic anhydrase in Arabidopsis thaliana. Plant Physiology 105, 707-713. doi: 10.1104/pp.105.2.707
19. Flanigan YS, Critchley C (1996) Light response of D1 turnover and photosystem II efficiency in the seagrass Zostera capricorni. Planta 198, 319-323. doi: 10.1007/BF00620046
20. Froehlich JE, Wilkerson CG, Ray WK, McAndrew RS, Osteryoung KW, GageDA, PhinneyBS(2003) Proteomic study of the Arabidopsis thaliana chloroplastic envelope membrane utilizing alternatives to traditional two-dimensional electrophoresis. Journal of Proteome Research 2, 413-425. doi: 10.1021/pr034025j (Pubitemid 36988420)
21. Futcher B, Latter GI, Monardo P, McLaughlin CS, Garrels JI (1999) A sampling of the yeast proteome. Molecular and Cellular Biology 19, 7357-7368.
22. 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. doi: 10.1073/pnas.87.8.3004
23. Guindon S, GascuelO(2003)Asimple, fast and accurate algorithmto estimate larges phylogenies by maximum likelihood. Systematic Biology 52, 696-704. doi: 10.1080/10635150390235520 (Pubitemid 37365050)
24. Haberlandt G (1896) 'Physiologische Pflanzenanatomie.' (Wilhelm Engelman: Leipzig)
25. Hatch MD (1987) C4 photosynthesis: a unique blend of modified biochemistry, anatomy and ultrastructure. Biochimica et Biophysica Acta 895, 81-106.
26. 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. doi: 10.1104/pp.93.2.825
27. Hatch MD, Osmond CB, Slatyer RO (1971) 'Photosynthesis and photorespiration.' (Wiley Interscience: New York)
28. Huffaker RC, Peterson LW (1974) Protein turnover in plants and possible means of its regulation. Annual Review of Plant Physiology 25, 363-392. doi: 10.1146/annurev.pp.25.060174.002051
29. 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. doi: 10.1023/A: 1005884515840 (Pubitemid 27354070)
30. Ku MSB, Edwards GE (1975) Photosynthesis in mesophyll protoplasts and bundle sheath cells of various types ofC4 plants V. Enzymes of respiratory metabolism and energy utilizing enzymes of photosynthetic pathways. Zeitschrift für Pflanzenphysiologie 77, 16-32.
31. 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. doi: 10.1104/pp.106.085829
32. 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. doi: 10.1104/pp.108.124008 (Pubitemid 352847593)
33. Lee J, Garrett WM, Cooper B (2007) Shotgun proteomic analysis of Arabidopsis thaliana leaves. Journal of Separation Science 30, 2225-2230. doi: 10.1002/jssc.200700151 (Pubitemid 47497023)
34. Majeran W, van Wijk KJ (2009) Cell-type-specific differentiation of chloroplasts in C4 plants. Trends in Plant Science 14, 100-109. doi: 10.1016/j.tplants.2008.11.006
35. 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. doi: 10.1105/tpc.105.035519
36. Martineau B, TaylorWC(1986) Cell-specific photosynthetic gene expression in maize determined using cell separation techniques and hybridization in situ. Plant Physiology 82, 613-618. doi: 10.1104/pp.82.2.613
37. Matsuoka M (1995) The gene for pyruvate orthophosphate dikinase in C4 plants: structure, regulation and evolution. Plant & Cell Physiology 36, 937-943.
38. Monson RK (2003) Gene duplication, neofunctionalization, and the evolution of C4 photosynthesis. International Journal of Plant Sciences 164(Suppl. 3), S43-S54. doi: 10.1086/368400
39. Moroney JV, Bartlett SG, SamuelssonG(2001) Carbonic anhydrase in plants and algae. Plant, Cell & Environment 24, 141-153. doi: 10.1111/j.1365-3040. 2001.00669.x
40. 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. doi: 10.1007/s00425-008-0836-8
41. Park J, Okita TW, Edwards GE (2009b) Salt tolerant mechanisms in singlecell C4 species Bienertia sinuspersici and Suaeda aralocaspica (Chenpodiaceae). Plant Science 176, 616-626. doi: 10.1016/j.plantsci. 2009.01.014
42. 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.
43. Sage RF (2004) The evolution of C4 photosynthesis. New Phytologist 161, 341-370. doi: 10.1111/j.1469-8137.2004.00974.x (Pubitemid 38126949)
44. 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. NewPhytologist 115, 603-608. doi: 10.1111/j.1469-8137.1990.tb00491.x
45. Sawers RJ, Liu P, Anufrikova K, Hwang JT, Brutnell TP (2007) A multitreatment experimental system to examine photosynthetic differentiation in the maize leaf. BMC Genomics 8, 12. doi: 10.1186/1471-2164-8-12 (Pubitemid 46242718)
46. Sheen J (1991) Molecular mechanisms underlying the differential expression of maize pyruvate, orthophosphate dikinase genes. The Plant Cell 3, 225-245.
47. Sheen J (1999) C4 gene expression. Annual Review of Plant Physiology and Plant Molecular Biology 50, 187-217. doi: 10.1146/annurev.arplant. 50.1.187
48. 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. doi: 10.1007/BF00046455
49. 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. doi: 10.1016/0003-9861 (91)90470-90474
50. Svensson P, Blasing OE, Westhoff P (2003) Evolution of C4 phosphoenolpyruvate carboxylase. Archives of Biochemistry and Biophysics 414, 180-188. doi: 10.1016/S0003-9861(03)00165-6 (Pubitemid 36627350)
51. 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. doi: 10.1111/j.1432-1033.1992.tb16674.x
52. 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. doi: 10.1104/pp.109.137513
53. 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. doi: 10.1104/pp.107.098152 (Pubitemid 47037447)
54. Tiwari A, Kumar P, Singh S, Ansari S (2005) Carbonic anhydrase in relation to higher plants. Photosynthetica 43, 1-11. doi: 10.1007/s11099-005- 1011-0 (Pubitemid 40589184)
55. Voznesenskaya EV, Franceschi VR, Kiirats O, Artyusheva EG, Freitag H, EdwardsGE(2002) Proof ofC4 photosynthesis without Kranz anatomy in Bienertia cycloptera (Chenopodiaceae). The Plant Journal 31, 649-662. doi: 10.1046/j.1365-313X.2002.01385.x
56. 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. doi: 10.3732/ajb.92.11.1784
57. 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 mesophylland bundle-sheath-specific cDNAs obtained by differential screening. Plant Molecular Biology 37, 319-335. doi: 10.1023/A:1005900118292 (Pubitemid 28209593)